crosson 1985 subcortical language

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BRAIN AND LANGUAGE 25, 257-292 (1985)

Subcortical Functions in Language: A Working ModelBRUCE CROSSON

Veterans Administration Medical Center and Department of Psychiatry and BehavioralSciences, University of Oklahoma Health Sciences Center, Oklahoma CityThe current paper explains a model of subcortical language functions thatfocuses on dynamic interactions between the cortex, the thalamus, and the basal

ganglia in the production of spoken language. The model was derived from (a)studies of subcortical lesions and language, (b) studies of subcortical stimulationand language, (c) knowledge regarding neural pathways between various corticaland subcortical structures, and (d) indications that preverbal monitoring of languageoccurs. In the current model, the thalamus plays roles in cortical arousal andactivation and in preverbal semantic monitoring. The basal ganglia function toregulate the degree of excitation conveyed from the thalamus to the cortex andto time the release of formulated language for motor programming. Consistencywith classical syndromes of aphasia and potential applications to other areas inthe neurosciences are discussed. The current theory, unlike previous formulations,is specific enough that testable hypotheses can be derived. o 1985 Academic PXSS.Inc.

Aphasia, difficulty in the production, use, or comprehension of languagecaused by brain dysfunction, has been studied for more than a century.Much of what is known about how brain mechanisms produce, understand,and use language comes from the study of aphasia and its concomitantbrain lesions. In addition to the study of aphasia, however, other methodshave been used to study brain-language relationships, such as responseto electrical stimulation of brain nuclei and tracts or the study of languagefunctions in persons having unimpaired brain functioning. This researchhas spawned many theories regarding how the brain produces language.

The author thanks Reg L. Warren, Ph.D. (Center for Communication Disorders, BraintreeHospital), and Oscar A. Parsons, Ph.D. (Department of Psychiatry and Behavioral Sciences,University of Oklahoma Health Sciences Center), for their helpful comments on thismanuscript. Appreciation is also extended to Carroll W. Hughes, Ph.D. (Department ofPsychiatry, University of Kansas College of Health Sciences), and John Rhoades, Ph.D.(Department of Psychology, University of New Mexico), for their critique of the theory.Send correspondence and requests for reprints to Bruce Crosson, Psychology Service(183), Veterans Administration Medical Center, 921 Northeast 13th St., Oklahoma City,OK 73104.

2570093-934X185$3.00

Copyright 0 1985 by Academic Press, Inc.All rights o f reproduction in any form reserved.


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258 BRUCE CROSSONUntil recently, consensus regarding aphasia and language function wasthat the overwhelming majority of language functions were performed

by the outer layers of the cerebral hemispheres, the cerebral cortex.Penfield and Roberts (1959) were among the first to challenge this view,suggesting that one structure deep within the dominant hemisphere, thethalamus, played a role in the integration of language functions. Today,there are numerous reports of aphasia after dominant thalamic lesion(hemorrhage, infarction, thalamectomy, etc.). The issue of thalamic aphasiahas been a controversial subject; indeed, Luria (1977) rejected the ideathat language changes with thalamic lesion were true aphasias. Eventhough some variability regarding symptoms reported exists betweenstudies of language after dominant thalamic lesion, a core syndrome ofthalamic aphasia nonetheless has emerged. This syndrome is discussedin some detail below. Further, a few earlier reports and more recentliterature have indicated that even structures lying lateral to the thalamus,the basal ganglia, are implicated in language functions.At this point in time, studies of subcortical functions in language haveused mainly inductive reasoning to explain these functions. In otherwords, investigators have sought to describe language phenomena aftersubcortical lesions, and from these observations, they have inferred certainmechanisms must exist. Exploration of subcortical participation in languagehas suffered to some degree because such theoretical explanations havenot had the degree of specificity from which hypotheses can be deducedand subsequently tested in new cases. Thus, exploration of subcorticalaphasias has not been approached from the standpoint of systematicallytesting hypotheses. For this reason, important phenomena may be over-looked or misunderstood.The thesis of this paper is that enough evidence is now available toconstruct a more detailed theory regarding the role of subcortical structuresin language. The model postulated herein begins to explain the formulation,monitoring, and refinement of spoken language and the role of subcorticalstructures in this dynamic process. It has its roots to some degree bothin the classical model (Geschwind, 1972) and the functional systemsapproach as broadly defined by Luria (1973). The reader may recognizecertain components of this model as having been explored previously inthe literature, but until now, no attempts have been made to integratethese different components into a comprehensive model of language pro-duction. It should be emphasized that the current work is a theory ofspoken language formulation. The motor execution of language (i.e.,speech) is not detailed in this paper. Further, language comprehension,the production and comprehension of written language, and the generationof the ideas expressed in language are not detailed in the current work.These concerns must await further development of the model.The following discussion is divided into four sections. Before discussing


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SUBCORTICALFUNCTIONSINLANGUAGE 259hypotheses regarding the role of subcortical mechanisms in language,some background information must be presented. The first section discussesthe classical model of aphasia (language function), and a few pertinentstudies which have forced some reconceptualization of this model. Becausethe literature relating cortical functions to language is so voluminous andbecause the emphasis is on the role of subcortical structures, the reviewof cortical studies must be selective. The purpose of the first section isto provide the background from which gross cortical functions can beposited. Only then can the relationship between cortical and subcorticalmechanisms be explored. The second section is a synopsis of the literatureon subcortical functions in language. Both the thalamus and the basalganglia are reviewed; studies include both reports of language functionsafter lesion and reports of language functions during electrical stimulation.Some attention is also paid to neuroanatomical pathways; with the exceptionof studies like Damasio, Damasio, Rizzo, Varney, & Gersh (1982), thistype of evidence has been only superficially considered. Inasmuch asthe directionality of these pathways constrains the possible ways in whichvarious language structures in the brain can interact, information aboutthese pathways constitutes important evidence concerning the ways inwhich various structures interact to produce language. The theory itselfis presented in the third section, integrating the available evidence con-cerning cortical, thalamic, and basal ganglia functions. Finally, the fourthsection discusses implications and limitations of the current model.

THE CLASSICAL MODEL OF APHASIAThe classical model of aphasia was most succinctly stated by Geschwind(1972) and has been a basis for other influential works in aphasia (e.g.,Goodglass & Kaplan, 1983). Basically, the classical model states thatthere is an area in the posterior portion of the inferior frontal gyrus,

Brocas area, which is responsible for the motor programming of language.Damage to this area produces slow, awkward speech with impaired in-tonation, a severely limited variety of grammatical constructions, andseverely limited vocabulary. Originally, comprehension of language wasconsidered to be nearly normal in Brocas aphasia. The classical modelalso postulated an area in the posterior portion of the superior temporalgyrus, Wernickes area, responsible for the comprehension of spokenlanguage. Damage to this area produces severe deficits in the comprehensionof language. In contrast to Brocas aphasia, language output in Wernickesaphasia shows relatively preserved rate, rhythm, variety of grammaticalconstructions, and articulation. However, language output is remarkablydevoid of content and contains substitutions of one word or sound foranother, circumlocutions, and incomprehensible jargon.The classical model of aphasia also proposes an area in the inferior


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260 BRUCE CROSSONparietal lobe (angular gyrus) which is responsible for the association ofspoken language symbols with information from other modalities, par-ticularly the visual modality. Damage to this area might result in readingor writing difficulties because of an inability to associate spoken languagesymbols with their visual counterparts, or it might result in an inabilityto name objects (anomia) because of an inability to associate languagesymbols with characteristics in other modalities of the objects which thesymbols represent. In the latter instance (anemic aphasia), language outputcontains circumlocutions and vague descriptions of intended concepts.In contrast to Wernickes aphasia, comprehension remains relativelyintact in an anemic aphasia. The classical model also notes that Brocasand Wernickes areas are connected by a fiber bundle called the arcuatefasciculus. Damage to this tract leaves language output fluent becauseBrocas area is intact and language comprehension relatively normalbecause Wernickes area is intact. However, the patient has a dispro-portionate difficulty repeating heard language because Wernickes areacannot relay the auditory patterns to Brocaa area. This syndrome isreferred to as the conduction aphasia.In the classical model, transcortical aphasias occur when Brocas andWernickes areas and the connections between them are intact but isolatedfrom other areas of the cortex by lesions in surrounding areas and tracts.Transcortical sensory aphasia demonstrates preserved repetition in thecontext of language output and comprehension which is otherwise likethat of Wernickes aphasia. Transcortical motor aphasia shows relativelypreserved repetition and comprehension in the context of extremely lim-ited conversational speech with at least some nonfluent characteristics(Goodglass & Kaplan, 1983).The classical model of aphasia can be criticized on several counts.For example, the classical model does not acount for all aphasia syndromes.Whitaker (1984) noted that only about 60% of patients tested can beclassified into the various classical syndromes by the Boston DiagnosticAphasia Examination (Goodglass & Kaplan, 1983). It may well be thatmany symptom clusters can be understood better by looking at subcorticalaphasias since these aphasias are different from cortical aphasias andsince the classical model considers mainly cortical phenomena. Thismatter is discussed further below.A second criticism of the classical model is that it does not explainhow language is formulated. Because of the deterioration of languageoutput in Wernickes aphasia, it is obvious that the damaged mechanismsplay some role in formulating language; however, this role is not clearlydefined. If language output was merely formulated posteriorly and conveyedforward for motor programming via the arcuate fasciculus, then thereshould be no difference in language output between conduction aphasiaand Wernickes aphasia. However, conduction aphasia demonstrates dis-


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SUBCORTICAL FUNCTIONS IN LANGUAGE 261proportionate difficulty with repetition, and substitutions are mainly ofone sound for another. In contrast, patients with Wemickes aphasiademonstrate difficulty in all language output with sound substitutions,word substitutions, neologisms, circumlocutions, and jargon (Goodglass& Kaplan, 1983). The classical model also does not explain why thereshould be two types of transcortical aphasia if Brocas area, Wernickesarea, and the arcuate fasciculus are intact in both forms.The classical model has also been criticized as a schema for classificationin aphasia research. Schwartz (1984) has noted that the classical syndromeshave evolved into polytypic structures. In other words, no deficit isessential for classification into a particular syndrome, and some char-acteristics are included in several syndromes. This situation can lead toconfusion and differences in classification criteria between studies. Car-amazza (1984) has also criticized the classical classifications because thedefining symptoms have not been specific enough. In other words, weshould not consider just comprehension deficits, but specific types ofcomprehension deficits such as difficulty with syntactic comprehension.Further, recent research necessitates, at the very least, revision ofmany of the classical assumptions. Some of the more important findingshave concerned the syndrome of Brocas aphasia. For instance, Mohret al. (1978) studied their own cases and reviewed the literature concerningthe relationship between Brocas area and Brocas aphasia. The authorsconcluded that cases of infarction had to extend considerably beyondBrocas area to produce Brocas aphasia. Casesof Brocas aphasia includeddamage to the frontal, parietal, and temporal opercula, the insula, andsurrounding white matter. Infarcts limited to Brocas area might initiallyproduce mutism, but mutism quickly evolves into rapidly improving dys-praxic and effortful articulation. Lasting language deficits, such as agram-matism, were not found with infarcts limited to Brocas area. Kertesz,Hat-lock, and Coates (1979) differed from the above authors in that theydescribed Brocas aphasia acutely in lesions of Brocas area and in thatthey found language deficits lasting at least 3 months in five of six patients.However, Kertesz et al. supported the findings of Mohr et al. (1978) inthat lesions producing a chronic Brocas aphasia did include the frontal,parietal, and temporal opercula, and the insula.Two further findings with respect to Brocas aphasia are important.Tonkonogy and Goodglass (1981) noted that symptoms of Brocas aphasiaincluded word-finding difficulties and articulatory difficulties of the kindoften associated with nonfluent aphasias. The authors found cases inwhich these functions could be separated, with differing anatomical lo-cations. The articulatory difficulty, related to deficient motor programming,was placed in the Rolandic operculum, while they located word-findingfunctions in the posterior, inferior frontal gyrus. The second developmentshowed that agrammatism in Brocas aphasia is not merely limited to


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262 BRUCE CROSSONlanguage output. Recent research cited by Blumstein (1981) indicatesthat patients with Brocas aphasia show difficulty comprehending complexgrammatical forms.The ability to self-monitor language was raised as early as 1972 byGoodglass and Kaplan. Goodglass and Kaplan suggested that the reasonfor deterioration of language in Wernickes aphasia is the breakdown inthe internal monitoring of language output by damaged language com-prehension mechanisms. Marshall and Tompkins (1982) studied self-cor-rection behaviors in groups of aphasic patients which they broke downby classical categories of aphasia. The authors discussed the importanceof their results in terms of their patients ability to monitor their ownlanguage. Although Marshall and Tompkins found no differences betweengroups of aphasic patients in the number of attempts to correct erroneousresponses in a series of structured language tasks, they found that patientswith Wernickes aphasia were the least successful in eventually correctingerroneous responses. These data supported the idea of Goodglass andKaplan (1972) regarding poor self-monitoring skills in Wemickes aphasia.The observations of Kertesz et al. (1979) also generally supported atemporal lobe focus for Wernickes aphasia, though the lesion of onepatient extended anteriorly.

Finally, there is evidence from the cortical stimulation literature thatlanguage formulation and production are not limited to the more anteriorzones associated with Brocas aphasia, even by Mohr et al. (1978). Thisholds true for both the phonological and the semantic aspects of language.Ojemann (1983) showed that there was a large overlap in cortical siteswhere stimulation interfered with the ability to discriminate speech soundsand where stimulation interfered with the ability to mimic sequences oforofacial movements. These sites were in the inferior posterior frontal,inferior parietal, and superior posterior temporal lobes. The author in-terpreted the data as indicating a link between motor speech and speechperception mechanisms. Not surprisingly, electrical stimulation evokedchanges in naming from sites in the same areas. The one area showingnaming changes in most patients was in the inferior frontal lobe immediatelyanterior to the motor cortex. This was the same area implicated in namingby Tonkonogy and Goodglass (1981). It was a little more surprising,however, that when patients were asked to name objects silently, elec-trographic potentials could be recorded concurrently from both frontaland temporoparietal sites (Ojemann, 1983). This suggests that both sitesmay be involved in word finding.The purpose of reviewing the literature described above primarily wasto provide an understanding of issues which will assist in unravelling therole of subcortical structures in language. A consensus is emerging thatthe classical model of aphasia (e.g., Geschwind, 1972) can not accountfor many phenomena in aphasia and does not provide an adequate system


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SUBCORTICAL FUNCTIONS IN LANGUAGE 263for classifying aphasias, especially for research purposes. For these reasons,a new framework with greater explanatory power and heuristic value isneeded.Thus, several inadequacies in the classical model are handled as follows.The controversy regarding the localization of Brocas aphasia is ac-knowledged, in this paper, primarily by using the terms anterior andtemporoparietal to refer to language zones. The split between word-finding and motor-programming functions in language suggested aboveis expanded upon. The participation of temporoparietal areas n monotoringlanguage output is incorporated into the theory in a way which is consistentwith evidence supporting the participation of these structures in languageoutput. These themes are expanded upon later in the theoretical sectionof this paper.

STUDIES OF SUBCORTICAL LANGUAGE FUNCTIONSAs previously stated, understanding of the role of subcortical structuresin language may explain phenomena which are unexplained by the classicalmodel of aphasia; indeed, this is a major thesis of this paper. In thissection, research regarding language functions of the thalamus and basalganglia of the language-dominant hemisphere is reviewed. A relatively

detailed knowledge of the anatomy of the basal ganglia and, especially,of the thalamus is necessary to read this paper. A detailed descriptionof these structures is beyond the scope of this paper, but the unfamiliarreader may wish to refer to a more detailed neuroanatomy text, such asCarpenter and Sutin (1983) or Matzke and Foltz (1983).A pictorial representation of the thalamus and its major nuclei (Fig. 1)

MEDIAL

ANTERIOR

VENTRAL POSTERIOR MEDIAL NUCLEUSLATERAL NUCLEUSFIG. 1. The left thalamus, showing the major nuclei. (From A Synopsis of Neuroanatomyby H. A. Matzke and F. M. Foltz, 1983, New York: Oxford University Press. Copyright1983 by Oxford University Press. Adapted by permission.)


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264 BRUCE CROSSONhas been provided for reference during the discussion of thalamic structures.Most of the thalamic structures generally thought to be involved in languagelie within the lateral nuclear complex. Evidence regarding the pulvinar,ventral anterior, and ventral lateral nuclei is discussed below. It shouldbe noted that a few authors have implicated other thalamic structuresin language, though their views are not necessarily shared by others.Ojemann (1983) speculated that the intralaminar nuclei might be involvedin language as a part of the thalamocortical activating system. Brown(1979) implicated the dorsal medial nucleus as being involved with anteriorlanguage zones, and thereby responsible for nonfluent aphasias whenthey occur with thalamic lesion. In this paper, the term basal gangliais used to refer to the caudate nucleus, putamen, and globus pallidus,collectively. A band of white matter, the anterior limb of the internalcapsule, lies between the putamen and the caudate nucleus. As discussedbelow, all of these structures have been implicated in language.The following is a brief synopsis of evidence regarding subcorticalmechanisms in language. This discussion is divided into three sections.The first section discusses thalamic mechanisms in language, and thesecond discusses mechanisms within the basal ganglia and internal capsule.The final section discusses pathways between the various cortical andsubcortical structures implicated in language. This evidence subsequentlyis used to construct a model of language generation including both corticaland subcortical mechanisms.Studies of Language and the Thalamus

Language has been studied both in cases of thalamic lesion and byelectrical stimulation of thalamic nuclei. The issue of thalamic aphasiahas been a controversial one with some authors questioning the existenceof such a syndrome (e.g., Benson 1979; Luria, 1977). Nonetheless, anincreasing number of scientists are beginning to accept and speculateabout a role for the dominant thalamus in language. An in-depth reviewof this literature is beyond the scope of this paper; the reader interestedin such detail may find Crosson (1984) helpful. A brief synopsis is offeredbelow.Although there has been variability between studies of language functionsafter naturahy occurring vascular lesions of the thalamus, a core syndromeof thalamic aphasia has occurred. The features are (a) relatively fluentlanguage with substitutions of one word for another and with spokenlanguage sometimes deteriorating into incomprehensible jargon, (b) com-prehension that is less impaired than the type of language output wouldnormally indicate, and (c) relatively preserved repetition (e.g., Alexander& LoVerme, 1980; Cappa & Vignolo, 1979; Crosson, Parker, Warren,LaBreche, & Tully, 1983; Jenkyn, Alberti, & Peters, 1981; Mohr, Watters,8z Duncan, 1975; Reynolds, Turner, Harris, Ojemann, & Davis, 1979).


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SUBCORTICALFUNCTIONSINLANGUAGE 265Perseveration and a lack of spontaneous speech are also common. Themost notable exceptions to this pattern are individual cases presentedby Brown (1979), Glosser, Kaplan, and LoVerme (1982), and McFarling,Rothi, and Heilman (1982). In particular, these three cases showed elementsof nonfluent output ranging from muteness in the former to impairmentof intonation and articulatory agility in the latter. Sometimes, nonfluentlanguage has been reported with thalamic degeneration (e.g., Daniels,Chokroverty, & Barr-on, 1969; Shulman, 1957), but it has been difficultto separate language deficits from the dementia normally exhibited bythese cases. Benson (1979) stated that aphasia after naturally occurringdominant thalamic lesion tends to remit rapidly. However, in 20 casesof vascular lesion reviewed by Crosson (1984) which were followed overtime, 17 showed aphasia persisting from 2 months to as long as 4 years.Aphasia has also been reported after thalamotomies which target theventral lateral nucleus for lesion. The reported incidence has ranged from3% (Gillingham, Watson, Donaldson, & Naughton, 1960) to as high as42% in lesions of the dominant ventral lateral nucleus (Selby, 1967).Although aphasia symptoms rarely have been reported in detail afterthalamotomy, those studies that have detailed symptoms described languagedysfunctions similar to those previously described for vascular lesion(Allen, Turner, & Gadea-Ciria, 1966; Bell, 1968; Darley, Brown, & Swen-son, 1975; Samra et al., 1969). In general, thalamotomy studies havereported aphasia to remit rapidly when it occurs (Crosson, 1984). Mostlikely, this pattern of rapid remission indicates that the ventral lateralnucleus is not directly involved in language. This is consistent with thefact that the ventral lateral thalamus is primarily a motor nucleus, receivinginputs from the basal ganglia, the cerebellum, and the motor cortex, andsending outputs to the motor cortex. The language symptoms probablyresulted from temporary disturbance of surrounding nuclei or pathways.

Two studies have shown no significant language changes after dominantpulvinectomies which created cryogenic or electrocoagulation lesionsusing stereotactic techniques (Brown, 1979; Vilkki & Laitinen, 1976):Ordinarily, one would interpret these data as indicating that the pulvinaris not involved in language; however, there have been other data stronglyimplicating a portion of the pulvinar. Kameyama (1976/1977) ound aphasiain lesions of the dominant ventral posterior lateral nucleus only whenlesions extended into the pulvinar. Other autopsied cases which werenot described as involving the entire dominant thalamus have demonstratedinvolvement of the pulvinar (Ciemans, 1970; Crosson, 1984; Mohr et al.,1975). Ojemann (1977) has reported greater density of naming errorsduring dominant pulvinar than dominant ventral lateral stimulation. Inparticular, his studies have implicated the anterior superior lateral pulvinar.Studies of retrograde degeneration of thalamic nuclei after cortical aphasiashave shown involvement of the anterior lateral pulvinar (Van Buren,


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266 BRUCE CROSSON1975; Van Buren & Borke, 1969). Degeneration of this area of the pulvinardid not occur when language was preserved. The most likely explanationfor the apparent discrepancy between pulvinectomy studies and otherstudies of the pulvinar is that pulvinectomies have not extended thelesion to the anterior superior lateral margin of the nucleus. Other studies(Schaltenbrand, 1965, 1975) have implicated the ventral anterior nucleusor surrounding structures, showing compulsary speech when this nucleuswas stimulated. Subjects in these studies have not been able to inhibitspeech during ventral anterior stimulation, even when they tried.McCarthy and Warrington (1984) have shown that there are at leastpartially separated semantic and phonological functions in language pro-duction. Although the issue of semantic versus other types of paraphasiahas not often been addressed in thalamic aphasia, Alexander and LoVerme(1980), Cappa and Vignolo (1979) and Crosson et al. (1983) have describeda predominance of semantic errors in the 13 cases of thalamic aphasiacollectively described by these studies. All authors interpreted their dataas suggesting a semantic role for the thalamus in language. Indeed, Crosson(1981) has speculated that the symptoms of thalamic aphasia describedabove are exactly what one would expect if a mechanism for semanticmonitoring were selectively damaged. Other theories have emphasizedthat the thalamus might be involved at a deeper level of language processingor formulation (e.g., Brown, 1975;Riklan & Levita, 1%5), that the thalamusmight be involved in activating cortical language mechanisms (e.g., Hor-enstein, Chung, & Brenner, 1978; Luria, 1977; McFarling et al., 1982;Riklan & Cooper, 1975), that the thalamus might regulate access to storesof language information (e.g., Botez & Barbeau, 1971; Reynolds et al.,1979), or that the thalamus might be involved in some combination ofsuch activities (e.g., Cooper et al., 1968; Samra et al., 1969).In summary, a syndrome of thalamic aphasia does appear to accompanydominant thalamic lesions. This syndrome is characterized by fluent butparaphasic language which sometimes degenerates into jargon. Languagecomprehension is usually less impaired than this type of output normallywould indicate, and repetition is minimally impaired or normal. Casesof nonfluent language after dominant thalamic lesion are rare but doexist; however, a paucity of spontaneous language is frequently seen.Perseveration in speech is also common. This pattern has been seen innaturally occurring vascular lesion and thalamotomy. Although aphasiaoften has often remitted rapidly after thalamotomy, it has persisted moreoften than not in reported cases of vascular lesions of the thalamus.Stimulation data, lesion data, and retrograde degeneration studies implicatedthe anterior superior lateral pulvinar in language; this area probably wasspared in pulvinectomies, where no language changes occurred. Transientlanguage symptoms after ventral lateral thalamotomy probably resultedfrom temporary disturbance of surrounding tracts or structures ratherthan direct involvement of this motor nucleus in language. One series


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SUBCORTICALFUNCTIONSINLANGUAGE 267of stimulation studies producing compulsary language implicated thedominant ventral anterior nucleus.Studies of Language and the Basal Ganglia and Internal Capsule

Language functions of the basal ganglia have been studied both incases of basal ganglia lesion and by electrical stimulation of the basalganglia. In naturally occurring vascular lesions, the internal capsule isfrequently involved along with the basal ganglia; therefore, these structuresare considered together. Although the functions have not been as ex-tensively studied as the thalamus, increasing attention has been paid totheir language functions. Indeed, one recent study (Wallesch et al., 1983)indicates that lesions of the basal ganglia in the language-dominant hem-isphere may have longer lasting severe effects on language than lesionsof the dominant thalamus. A synopsis of this literature is offered below.Lesions in the area of the internal capsule and putamen in the language-dominant hemisphere have resulted in both fluent and nonfluent languageoutput. Naeser et al. (1982) found that lesions extending from this regionanteriorly and ventrally to include the periventricular white matter deepto Brocas area generally produced language output with many nonfluentcharacteristics and lesser impairments of comprehension and repetition.When lesions extended posteriorly across the auditory radiations, speechwas fluent and comprehension poor. Alexander and LoVerme (1980)generally described fluent language in 6 lesions with a putaminal focus(extent of capsular involvement was not detailed). Brunner, Kornhuber,Seemuller, Suger, and Wallesch (1982) described Brocas aphasia withtranscortical features in one or two of their cases of lesions in theputamen and surrounding structures. Later in this paper, some importis placed on connections in the anterior limb of the internal capsule inthe language-dominant hemisphere. Again, both fluent and nonfluent lan-guage output can be found with lesions in the anterior limb. Of 15 subcorticallesion cases in the literature which involve part of the anterior limb(Aram, Rose, Rekate, & Whitaker, 1983; Damasio et al., 1982; Naeseret al., 1982), 11 have nonfluent characteristics and 4 were reported asfluent. Again, the Naeser et al. data indicated that language was morelikely to be nonfluent when lesions of the anterior limb extended furtherventrally and laterally.In naturally occurring subcortical vascular lesions producing aphasia,the globus pallidus of the language-dominant hemisphere has seldom beenmentioned. Patterns of vascular supply indicate a probability of involvementof the anterior pallidum when the anterior putamen has a vascular lesion(Carpenter & &tin, 1983). One case involving the posterior globus pallidus,posterior medial putamen, and other structures in an 1 -year-old childshowed dysarthria (i.e., difficulties in the motor execution of speech)but no language symptoms (Aram et al., 1983).In the subcortical aphasias of Damasio et al. (1982), lesions extended


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268 BRUCE CROSSONinto the caudate head or body in four cases. Language was nonfluent inthree and fluent in one, and one case with such a lesion had normallanguage. All cases but the latter with normal language also had lesionsin the anterior limb of the internal capsule. Data from Brunner et al.(1982) showed that aphasia was likely to .be more severe and more persistentif lesions of Brocas area extended to the caudate head. Language dem-onstrated nonfluent characteristics in such cases.In the early stages of stereotactic surgery for Parkinsonism, lesionswere created in the globus pallidus instead of the ventral lateral thalamus.Svennilson, Torvik, Lowe, and Leksell(l960) described aphasia in somepatients after creating lesions in the dominant globus pallidus. The targetwas in the lateral medial segment of the nucleus. Objectively, word-finding difficulty and paraphasia were noted, though more detailed de-scriptions of language were not available. Subjectively, one patient de-scribed the difficulties as a lack of coordination between thought andspeech. Other studies reported similar findings for lesions involvingboth the globus pallidus and ventral lateral thalamus (Cooper, 1958;Hermann, Turner, Gillingham, & Gaze, 1966).A few electrical stimulation studies have provided information aboutthe basal ganglia. Hermann et al. (1966) demonstrated the arrest of ongoingspeech with electrical stimulation in the globus pallidus as well as inthalamic nuclei. This effect may be related to the aphasias resultant fromlesions in these structures; this possibility is explored at greater lengthbelow. The work of Van Buren (1963, 1966) has provided evidence ofinvolvement of the caudate head in language. This investigator foundarrest of ongoing speech when he stimulated frontocaudate pathwaysnear the caudate head of the dominant hemisphere. Further, when stim-ulation was moved into the caudate head itself, ongoing speech was notonly interrupted, but there was also inappropriate spontaneous speech.Such inappropriate speech was not observed during stimulation of theventral lateral nucleus of the thalamus, the internal capsule, or globuspallidus. The importance of this distinction in response between thefrontocaudate pathways and the caudate head is discussed further below.To summarize, language symptoms from lesions in the basal gangliaand internal capsule do not cohere into a single syndrome as well assymptoms accompanying dominant thalamic lesion. Data from Damasioet al. (1982) and Van Buren (1963, 1966) indicated that small differencesin location within these structures and tracts may produce dramaticdifferences in language after lesion or during electrical stimulation. Theputamen, globus pallidus, and anterior limb of the internal capsule haveall been implicated. Lesions in the anterior limb of the internal capsuletend to produce nonfluent language output, especially if they extendventrally and anteriorly. Stimulation of the frontocaudate pathways pro-duced interruptions of ongoing language while stimulation of the caudate


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SUBCORTICAL FUNCTIONS IN LANGUAGE 269head produced inappropriate but fluent language. Lesions of Brocasarea extending into the caudate nucleus tended to cause a longer lastingand more severe nonfluent aphasia. Both fluent and nonfluent languagehas been reported in putaminal lesions.Neuroanatomical Pathways between Cortical and SubcorticalStructures Implicated in Language

It is highly unlikely that the various cortical and subcortical structuresinvolved in language operate in isolation from one another to producethe phenomena we know as language. It is more probable that thesestructures operate in an organized and coordinated fashion to produceand comprehend language. In order to understand how these structuresfunction and how they are coordinated, then, it is necessary to understandhow information flows between them. It follows that knowledge of thepathways connecting the various structures involved in language couldshed some light on how they interact. Indeed, the possible ways in whichthe structures might interact is constrained by the direction in whichinformation can flow between them. With the exception of Damasio etal. (1982), few authors have noted the importance of these connectionsin language. Connections between the centers most often implicated inlanguage are discussed below. These centers include the inferior frontal,insular, and opercular cortex, the temporoparietal cortex, the ventralanterior nucleus of the thalamus, the ventral lateral nucleus of the thalamus,the pulvinar of the thalamus, the caudate nucleus, the putamen, and theglobus pallidus. Readers desiring more detail should consult Carpenterand Sutin (1983) or Ingram (1976).The temporoparietal and anterior language zones of the cortex areconnected by the arcuate fasciculus which transmits information bothanteriorly and posteriorly. The caudate nucleus and putamen both receiveinput from most regions of the cortex, though the strength of representationof different cortical regions may vary between the two nuclei. Anteriorly,for example, the motor cortex projects primarily to the putamen, thepremotor cortex projects to both nuclei, and the prefrontal cortex projectsprimarily to the caudate nucleus. Although there are these prolific con-nections from the cortex to the caudate nucleus and putamen, there areno fibers of any consequence which travel in the opposite direction, fromthe caudate and putamen to the cortex. The main outputs from the basalganglia are channeled through the globus pallidus which receives fibersfrom both the caudate nucleus and the putamen (Carpenter & Sutin,1983).Of the structures discussed in previous sections of this work, the globuspallidus projects to the ventral lateral and ventral anterior nuclei of thethalamus. The ventral lateral thalamus receives inputs from the globuspallidus, the cerebellum, and the motor cortex. This nucleus sends fibers


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270 BRUCE CROSSONto the motor cortex. This pattern of connections leads to the conclusionthat the ventral lateral nucleus is primarily a motor nucleus. Thus, it ismore likely to be involved in speech than language; thalamotomy studiessupport this conclusion since dysarthria is more common and more per-sistant after ventral lateral lesion than aphasia (e.g., Cooper et al., 1968).The ventral anterior nucleus receives input from the globus pallidus(anterior portions) and from the premotor and prefrontal cortex. Ingram(1976) described direct connections to the ventral anterior nucleus fromthe brainstem reticular formation, but Carpenter and Sutin (1983) em-phasized input to the ventral anterior nucleus from the intralaminar thalamicnuclei which in turn receive fibers from the brainstem reticular formation.The ventral anterior nucleus sends outputs to the premotor and prefrontalcortex. The pulvinar has bidirectional connections with the temporoparietalcortex. There are indications of bidirectional connections of the pulvinarwith the frontal cortex (Carpenter & Sutin, 1983).These connections between structures implicated in language tell ussomething about the way in which the structures may be organized inlanguage functions. The cortical language centers may influence the caudatenucleus or putamen; however, due to an absence of direct connections,the caudate nucleus and putamen can have no direct influence on corticallanguage centers. Rather, any influence of the basal ganglia on corticallanguage centers must be mediated by thalamic centers. More specificially,influences from the basal ganglia upon the anterior cortical languagecenters must be mediated through the ventral anterior nucleus. Throughdirect or indirect inputs from the brainstem reticular formation, the ventralanterior nucleus may also transmit arousal or activation impulses to theanterior cortical language zones. Thalamic nuclei and cortical languagecenters, however, may have reciprocal influences by virtue of bidirectionalconnections. The ventral anterior nucleus may have reciprocal influenceswith the anterior cortical language zones. The pulvinar may have reciprocalinfluences with the temporoparietal cortex, and perhaps even the anteriorlanguage zones.When considered with lesion and stimulation data, the nature anddirection of neuroanatomical pathways becomes an important piece ofthe puzzle of cortical-subcortical relationships in language. One keyexample should illustrate this point. In several subjects, Van Buren (1963,1966) found that stimulation of the caudate head in the language-dominanthemisphere resulted in the interruption of ongoing language by the flowof irrelevant material into language. It is clear from the examination ofneuroanatomical pathways that however stimulation of the caudate headinfluences the language cortex to produce irrelevant material must bemediated through the globus pallidus then the ventral anterior (or possiblythe ventral lateral) nucleus because the basal ganglia have no directoutput to the cortex. Van Buren further found that stimulation of front-


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272 BRUCE CROSSONCortical Functions

In the present model, language formulation is presumed to be a functionof the more anterior language zones, which most likely include the posteriorinferior frontal gyrus, the frontal operculum, the parietal operculum, thetemporal operculum, and the insula. The term language formulationencompasses the conceptual, word-finding, and syntactic processes nec-essary for the encoding of language. The reader will recall that Tonkonogyand Goodglass (1981) found that the word-finding and motor-programmingfunctions of these areas were separable. Extending the findings of Ton-konogy and Goodglass, language formulation (i.e., language encoding)is assumed to be partially separated from, but in close physical andtemporal contiguity with, the motor programming of language. This ex-tension from the narrower word-finding function to the broader languageformulation function is justified by findings discussed above. First wasthat both agrammatism in verbal output and comprehension of complexsyntax are associated with lesions in the more anterior language zones(Blumstein, 1981; Mohr et al., 1978). Syntactic as well as word-findingmechanisms are, of course, needed for language encoding. Second wasthat these same difficulties with syntax were found in Tonkonogy andGoodglass (1981) patient with word-finding but not articulatory problems.Finally, from an ontological standpoint, language formulation can beconsidered an extremely complex motor function, and as such, shouldbe located in the anterior language zones in proximity with other suchmotor functions, not in the posterior cortical areas devoted to sensoryfunction as some authors have suggested.In light of recent research regarding the comprehension of complexsyntax (e.g., Blumstein, 1981), the function of the posterior temporoparietalcortex also must be described in a more circumscribed manner than inthe classical model. Instead of assigning all comprehension functions tothis region, the current model proposes that the decoding of languagesymbols is accomplished in this area. Such decoding may even extendto the level of the phrase or simple sentence, but the comprehension ofcomplex syntax requires the participation of more anterior regions oncethe language symbols have been initially decoded.Observations of Luria (1973) are also relevant. He divided comprehensionof language symbols into the discrimination of phonemes and the designationof semantic attributes. The latter can occur only after the phonologicalstructure has been decoded. A further observation is that the semanticfunctions of the temporoparietal cortex are based, at least to some degree,on the association of language symbols with the characteristics of theobjects they represent in other modalities (e.g., visual, tactile). For example,the word ball would be associated with a visual representation of around object.


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SUBCORTICAL FUNCTIONS IN LANGUAGE 273Finally, the temporoparietal language areas are connected to the anteriorlanguage areas by the arcuate fasciculus. A case described by Naeser

and Hayward (1979) supports the role of this structure in conductionaphasia, where repetition is disproportionately impaired in comparisonwith other language functions. Evidence also suggests that this pathwayis involved in conveying phonological information in language. For example,the most common type of substitution error in conduction aphasia is thesubstitution of one sound for another rather than the substitution of oneword for another (Goodglass & Kaplan, 1983). McCarthy and Warrington(1984) also showed that repetition could be facilitated in conductionaphasia by repetition tasks which required active semantic processing.The authors concluded that a phonological processing mechanism wasdamaged in conduction aphasia and that improvement in the semanticallyloaded repetition tasks was due to the involvement of intact semanticmechanisms.Cortical mechanisms discussed above have been schematically rep-resented in Fig. 2. To summarize the role of cortical centers, languageformulation (including conceptual, word-finding, and syntactic processes)is performed in the anterior language zones. Language formulation isclosely associated with, but separate from, motor programming. Decodingof complex grammar is also performed anteriorly. The phonological andsemantic decoding of language symbols is performed by the temporoparietalcortex. Semantic monitoring relies heavily on the association of languagesymbols with information in other modalities. The arcuate fasciculus,connecting the anterior and temporoparietal language zones, is involvedin phonological processing, which is discussed further below.

FIG. 2. Schematic drawing representing cortical language mechanisms and their inter-connection. FOR = language formulator (anterior cortex), MP = motor programmer(anterior cortex); DEC = language decoder (temporoparietal cortex); AF = arcuate fasciculus.


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274 BRUCECROSSONThalamic Functions

In 1981, Crosson presented a paper at the meeting of the AmericanPsychological Association proposing that the thalamus, with its reciprocalconnections to cortical language areas, provided one mechanism throughwhich the temporoparietal area, involved in language decoding, monitoredthe encoding of language peformed by anterior mechanisms prior to theactual execution of encoded material in speech. In other words, cortico-thalamo-cortical pathways provide the mechanism through which thetemporoparietal area checks the encoded language for semantic accuracy.The author had reasoned that if such a semantic feedback mechanismexisted, damage to it would result in a syndrome where verbal outputwas more impaired than language comprehension because the decodingmechanism would be left intact while the mechanism for monitoringsemantic accuracy would be damaged. As previously mentioned, thishas indeed been the picture presented by most cases of thalamic aphasia(e.g., Alexander & LoVerme, 1980; Cappa & Vignolo, 1979; Crosson etal., 1983; Jenkyn et al., 1981; Mohr et al., 1975; Reynolds et al., 1979).The predominance of semantic paraphasias in thalamic aphasia (Alexander& LoVerme, 1980; Cappa & Vignolo, 1979; Crosson et al., 1983) alsosupports the idea of an interruption in semantic monitoring. Relativelyintact repetition is explained by reliance on a separate system for thetransmission of phonological linguistic information used to perform theact of repetition (McCarthy & Warrington, 1984).In order for preverbal semantic monitoring of language formulation totake place, semantic information must be conveyed from anterior languageareas where language is formulated to temporoparietal areas where languageis decoded and monitored. The most likely pathway for this transmissionof semantic information is from the anterior language zones to the thalamusvia the connections with the ventral anterior thalamus, from ventralanterior thalamus to the pulvinar (probably via the internal medullarylamina), and from the thalamus to the temporoparietal cortex throughconnections with the pulvinar.The work of Ojemann and his colleagues has shown that anomia indominant ventral lateral stimulation was much more likely when electrodeswere close to the internal medullary lamina and that perseveration ofthe same wrong word during dominant ventral lateral stimulation wasmuch more common when electrodes were near the ventral anteriornucleus (Ojemann, 1975, 1977, 1983; Ojemann & Ward, 1971). Thesedata can be seen as confirmation of the role of the internal medullarylamina and the ventral anterior nucleus in language. However, it shouldbe noted that there is evidence of pathways from the pulvinar to thefrontal lobes (Carpenter & Sutin, 1983), and conceivably, semantic in-formation might flow between the anterior and posterior language areas


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SUBCORTICAL FUNCTIONS IN LANGUAGE 275primarily through the pulvinar. As stated above, electrical stimulationdata (Ojemann, 1977), postmortem data (Ciemans, 1970; Crosson, 1984;Kameyama, 1976/1977; Mohr et al., 1975), and retrograde degenerationdata (Van Buren, 1975; Van Buren & Borke, 1969) support the role ofthe pulvinar in language. Also, in order for monitoring to be effectivewhen refinement of semantic content is necessary, the message must beconveyed from the temporoparietal monitoring mechanism to the languageencoder in the anterior cortex to initiate refinement. This message wouldbe conveyed through the pathways mentioned above, but in the oppositedirection since the cortico-thalamo-cortical pathways mentioned werebidirectional.

In order for anterior cortical mechanisms to produce language, it isalso necessary that an optimal arousal level of these mechanisms bemaintained. Since it receives afferents from the reticular formation (director indirect), thought to be involved in cortical arousal, and since it sendsefferents to the frontal cortex, the ventral anterior nucleus of the dominantthalamus is the likely site to provide such excitatory influences. Thefunction of the ventral anterior nucleus would be to selectively distributeexcitatory influences from the reticular formation to frontal mechanismsfor language production via the anterior limb of the internal capsule.Primarily in the dominant thalamus, electrical stimulation in and aroundthe ventral anterior thalamus, as demonstrated by Schaltenbrand (1965,1975), often elicited spoken language which had little relevance to ongoingevents and could not be voluntarily inhibited. These phenomena areprobably related to perseveration during naming from anterior ventrallateral stimulation (Ojemann, 1983), as discussed above.Recent studies (Aram et al., 1983; Damasio et al., 1982; Naeser et al.,1982) also indicated that destruction of the anterior limb of the internalcapsule produces dysfluent but often grammatical language, particularlywhen lesions extend anteriorly and ventrally into this region. Connectionsbetween the ventral anterior nucleus and the anterior language zones ofthe cortex traverse this portion of the internal capsule, and the dysfluentlanguage can be explained by the interruption of excitatory influencesfrom the ventral anterior nucleus to the language formulation centers.The occasionally dysfluent cases of thalamic aphasia (Brown, 1979; Glosseret al., 1982; McFarling et al., 1982) and the frequent lack of spontaneousspeech in thalamic aphasia may also be due to the interruption of excitatoryinfluence from the thalamus to the cortex.

The cortical and thalamic mechanisms for language mentioned up tothis point in the development of the model have been schematicallyrepresented in Fig. 3. To summarize thalamic functions in language,bidirectional cortico-thalamo-cortical pathways are involved in semanticmonitoring mechanisms. Internal semantic monitoring of language for-mulated by the anterior language zones is performed by the temporoparietal


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276 BRUCE CROSSON

FIG. 3. Schematic drawing representing cortical language mechanisms, thalamic languagemechanisms, and their interconnections. FOR = language formulator (anterior cortex);MP = motor programmer (anterior cortex); DEC = language decoder (temporoparietalcortex); AF = arcuate fasciculus; VA = ventral anterior thalamus; PUL = pulvinar(thalamus); IML = internal medullary lamina (thalamus); RF = reticular formation.

cortex prior to the execution of the language segments in speech. Suchmonitoring may result in the refinement of formulated language segmentsprior to their release for motor programming. Pathways through thethalamus (particularly the anterior superior lateral pulvinar) act as aconduit for semantic information and messages o refine semantic contentduring this monitoring process. Excitatory impulses are also conveyedfrom the ventral anterior nucleus to the anterior language zones whichprovide the proper level of activation for language formulation. Twoquestions remain to be answered, however: First, how are languagesegments held in abeyance from execution while the semantic monitoringtakes place? Second, how are the excitatory influences from the ventralanterior nucleus regulated? For the answers to these questions, we mustturn our attention to the mechanisms of the basal ganglia.Basal Ganglia

Of the structures involved in language, the least data exist on the basalganglia. Nonetheless, key data do exist allowing the formulation of tentativehypotheses regarding their role in language. Not least among these datais the anatomical position of the basal ganglia relative to the cortex andthe thalamus. As previously highlighted, the putamen and caudate nucleusreceive input primarily from the cortex, but these structures do not sendany output directly to the cortex. Most output from the basal ganglia ismediated through the globus pallidus which sends numerous fibers tothe ventral anterior and ventral lateral nuclei of the thalamus. Thesethalamic nuclei then send outputs to the frontal and motor cortex, re-


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SUBCORTICAL FUNCTIONS IN LANGUAGE 277spectively. Thus, the basal ganglia are in a position to receive input fromvarious parts of the cortex, and on the basis of these inputs, the basalganglia can in turn influence outputs from the thalamus to the cortex.The current model proposes that the basal ganglia are involved in twomechanisms which influence language production by integrating inputsfrom the cortex and subsequently influencing thalamic mechanisms. First,the basal ganglia influence tone in the anterior cortical language areasby regulating the flow of excitatory impulses from the ventral anteriorthalamus. If tonic cortical excitation is maintained at too high a level,extraneous material will enter into the encoding (language formulation)and motor-programming processes. If tone is too low, language formulationwill be inefficient or not occur spontaneously at all. The second mechanismis a motor release mechanism which allows language segments to bereleased at the proper time, after semantic monitoring has taken place.These two mechanisms are detailed in the following paragraphs.The mechanism directly affecting tonic activation of the anterior languagecortex by the ventral anterior nucleus of the thalamus is most likelylocated in the globus pallidus. Fluent language output was described aftersurgical lesions of the globus pallidus (Svennilson et al., 1960). Further,the arrest of ongoing language during stimulation of the globus palliduswas reported (Hermann et al., 1966). The most parsimonious explanationfor these two pallidal phenomena is that the globus pallidus maintainsan inhibitory influence over the ventral anterior thalamus in such a wayas to regulate the amount of excitation conveyed to the anterior languagecortex. Thus, lesion of the globus pallidus would create disinhibition ofthe ventral anterior thalamus, leading to overactivation of the anteriorcortical language zones. This overactivation would in turn result in theprogramming of extraneous material in language, for example, the par-aphasias noted by Svennilson et al. (1960). Stimulation of the globuspallidus, however, would excite inhibitory mechanisms resulting in theinhibition of the ventral anterior nucleus and the interruption of ongoinglanguage, as noted by Hermann et al. (1966).* A complete understandingof the tonic mechanisms, though, is dependent upon the understandingof the response release mechanisms.

Precedents for such tonic and response release mechanisms exist elsewhere in thenervous system, for example, the tonic and phasic changes in sudomotor response asmeasured by skin conductance.2 There are several possible explanations of stimulation data besides the excitation ofprocesses (Crosson, 1984). However, it should be noted that there is ample precedent forthe excitation of sensory and motor processes in subcortical stimulation. Ojemann (1976)discussed the importance of eliciting sensory or motor responses in his work, and Selby(1967) used the elicitation of motor responses to place electrodes in surgery for Parkinsonssyndrome. Further, excitation explanations become much more probable when it can beshown that stimulation and lesion produce opposite effects.


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278 BRUCE CROSSONHowever, one digression is necessary before discussing the responserelease mechanisms. The reader might now ask the following question:

If tonic control of the ventral anterior nucleus resides in the globuspallidus, then why does the literature on vascular lesion more frequentlyimplicate the putamen than the globus pallidus? There are two possibleanswers. The first is that the inhibitory mechanism actually resides inthe putamen, and its influence is only transmitted by the globus pallidusto the thalamus. The second possibility is that lesions of the putamenproducing aphasia directly or indirectly involve the globus pallidus. Thereader will recall that the globus pallidus is immediately adjacent andmedial to the putamen. It is quite likely that the six cases of dominantputaminal hemorrhage discussed by Alexander and LoVerme (1980) atleast transmitted pressure effects to the globus pallidus during the acutestages. In reported cases of infarction (e.g., Damasio et al., 1982; Naeseret al., 1982), it is rare for the putamen alone to be involved. In casesinvolving the anterior putamen, it is also likely that the anterior globuspallidus is involved because of overlap in circulation (Carpenter & Sutin,1983). This portion of the globus pallidus receives input from the caudatenucleus. The importance of this latter fact is discussed shortly. The readeralso will recall that Aram et al. (1983) also reported dysarthria but noaphasia in one case of lesion in the posterior portions of the dominantglobus pallidus and putamen. Damasio et al. (1982) reported similar findingsin one of their cases.The response release mechanisms of the basal ganglia are closely relatedto the tonic mechanisms. Actually, both tonic and response release mech-anisms involve both the globus pallidus and the caudate nucleus, asexplained below. The purpose of the response release mechanism is toallow a temporary increase in excitation from the ventral anterior thalamusto the anterior language cortex which is timed to allow the motor pro-gramming of semantically verified language for speech. This responserelease function is performed by the head of the caudate nucleus throughits input from the anterior and posterior language cortex and its outputto the globus pallidus.The response release mechanism works as follows. Activity in thecaudate head exerts an inhibitory influence over the inhibitory mechanismsof the globus pallidus. Thus, when required, activity from the caudatehead will temporarily inhibit pallidal inhibitory mechanisms, thereby re-leasing the ventral anterior nucleus from pallidal inhibition, which in turnincreases excitation to anterior cortical mechanisms allowing the releaseof semantically verified language for motor programming. Normally (i.e.,when a person is not speaking), the caudate inhibitory link is underinhibition from the decoding mechanisms in the temporoparietal cortex,leaving the pallidal inhibitory mechanisms active, and there is no temporaryincrease in excitation of the anterior language mechanisms. Once semantic


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SUBCORTICAL FUNCTIONS IN LANGUAGE 279verification of a verbal message (formulated anteriorly) has occurred,however, the temporoparietal structures release the caudate mechanismfrom inhibition. This action subsequently causes the caudate mechanismto inhibit the pallidal inhibitory mechanism, freeing the ventral anteriorthalamus to excite anterior mechanisms to the level where motor pro-gramming is initiated, which eventually leads to verbal expression of thelanguage segment. Once programming of the segment has been completed,the anterior cortical mechanisms terminate activity of the caudate mech-anism through frontocaudate pathways, restoring the relationship betweentemporoparietal and caudate mechanisms to its normal state, i.e., inhibitionof caudate by temporoparietal mechanisms.

Two sets of evidence support this role for the caudate head in language.First, when Van Buren (1963, 1966) stimulated frontocaudate pathwaysnear the caudate head, he usually produced the arrest of ongoing speech.This result would be predicted from the current model because stimulationin that area excites the frontocaudate pathway responsible for terminatingmotor programming and reestablishing temporoparietal inhibition of caudatemechanisms. Furthermore, Van Buren found that when stimulation wasmoved into the caudate head itself, ongoing speech was interrupted bythe flow of irrelevant material into speech. Again, this result can beexplained by the current model. Caudate stimulation at the wrong timeduring the alternating sequences of excitation and inhibition would interruptthe organization of language sequences and allow irrelevant material intothe encoding and programming processes because the result of stimulatingcaudate mechanisms is to free the excitatory mechanisms in the ventralanterior thalamus from pallidal inhibition. In the second set of supportingdata, Brunner et al. (1982) found Brocas aphasia to be relatively permanentonly when the caudate head was damaged in addition to anterior corticalmechanisms. This finding is also consistent with the present model becausedamage to the caudate would leave pallidal inhibition of ventral anteriorexcitatory influences active, and it would be difficult to release languagefor motor programming. The result, of course, would be nonfluent language.Thus, the present model provides a parsimonious explanation for phe-nomena noted with stimulation of frontocaudate pathways, with stimulationof the caudate head, and with lesions extending into the caudate head.The model is also consistent with research and conceptualizations regardingthe basal ganglia. For example, Evarts (1979) noted that cells in the basalganglia fire in advance of volitional movement. In the case of language,this activity could represent activation of the response release mechanismin the caudate head which inhibits pallidal inhibitory mechanisms, allowingtemporary excitation of anterior cortical programming mechanisms bythe ventral anterior thalamus.Caudate mechanisms also play a role in regulating cortical tone byinfluencing the inhibitory mechanism of the globus pallidus. For example,


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280 BRUCE CROSSONif excitation of frontal mechanisms occurs through pathways other thanthose discussed above (e.g., the limbic system), then it might be necessaryto limit the amount of excitation conveyed through the ventral anteriornucleus. This would prevent the summation of limbic and thalamic inducedexcitation from causing an overactivation of anterior language mechanismsleading to the admission of irrelevant material into the encoding process.This type of adjustment for anterior excitation through other mechanismsis accomplished through frontocaudate then caudopallidal pathways.Although motor execution of language (i.e., speech) is not the topicof this paper, a few words should be said regarding the relationship ofmotor execution and the phonological aspects of spoken language. It hasalready been mentioned that the arcuate fasciculus is involved in thephonological aspects of language. In light of the above discussion, it islikely that this pathway is involved in phonological monitoring in a waysimilar to the mechanisms discussed for semantic monitoring. In otherwords, the temporoparietal structures responsible for phonemic discrim-ination would monitor the motor programming of language through thearcuate fasciculus, determining whether the motor program is associatedwith the desired phonological pattern. Most likely this phonological mon-itoring is closely associated with motor programming since the correctplacement and timing of movements of the vocal structures determinewhether the correct phonemes are produced (e.g., see Blumstein, 1981).The reader will remember that there is overlap in the frontal, temporal,and parietal sites where stimulation interfered with the ability to discriminatespeech sounds and where stimulation interfered with the ability to mimicsequences of orofacial movements (Ojemann, 1983).The latter data indicatesome relationship between anterior motor-programming mechanisms andposterior phonological decoding mechanisms in speech output. It is likelythat the final execution of language in speech is released by mechanismsin the putamen and ventral lateral thalamus which parallel the languagemechanisms in the caudate and ventral anterior thalamus discussed above.The smooth flow of conversational speech is dependent upon the si-multaneous activity of the mechanisms described herein. While one segmentof language is being executed in speech, the next segment is being pro-grammed for motor execution, the ensuing segment is being verified forsemantic content, and another segment s in the process of being formulated.In this way, the alternating excitation and inhibition of frontal motor-programming and motor-execution mechanisms for language must betaking place in rapid succession to allow the smooth flow of language.In the child just learning language, it is likely that semantic verificationtakes place at a word for word (or even morpheme for morpheme) level.Efficiency in a more complex adult language probably requires that semanticverification takes place at a phrase level. This would require comprehensionof simple grammar by temporoparietal mechanisms, though the morecomplex grammar would require anterior assistance for decoding.


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SUBCORTICAL FUNCTIONS IN LANGUAGE 281The development of the model for language production is now complete,and the mechanisms mentioned in the model have been schematically

represented in Fig. 4. To summarize this model of language productionand the participation of the basal ganglia, anterior cortical mechanismsare responsible both for the formulation of language and the motor pro-gramming of language for speech. Prior to motor programming, tem-poroparietal mechanisms monitor semantic aspects of the language whichhas been encoded by anterior mechanisms. Prior to spoken execution,phonological aspects of language are monitored in conjunction with motorprogramming via the arcuate fasciculus. Semantic aspects are monitoredthrough reciprocal connections between the anterior cortical and tem-poroparietal areas which pass through thalamic structures (the anteriorsuperior lateral pulvinar, and possibly the ventral anterior nucleus andinternal medullary lamina). When semantic errors are discovered duringthe monitoring process, information is carried back to the anterior languagezones via the thalamic pathway, and a process of semantic refinementis initiated. Refinement of the phonological aspects of language, whennecessary, is probably carried out via the arcuate fasciculus which canexcite a phonological refinement process.Activation of anterior cortical language mechanisms for formulationof meaningful language is performed by the ventral anterior nucleus ofthe thalamus which regulates the flow of excitation from the reticularformation to the anterior language mechanisms. Inhibitory influencesexercised by the globus pallidus over the ventral anterior nucleus determinehow much excitation is allowed to pass to the anterior cortical mechanisms.

FIG. 4. Schematic drawing representing cortical language mechanisms, thalamic languagemechanisms, basal ganglia language mechanisms, and their interconnections. FOR = languageformulator (anterior cortex); MP = motor programmer (anterior cortex); DEC = languagedecoder (temporoparietal cortex); AF = arcuate fasciculus; VA = ventral anterior thalamus;PUL = pulvinar (thalamus); IML = internal medullary lamina (thalamus); RF = reticularformation; CA = caudate nucleus (basal ganglia); PUT = putamen (basal ganglia); GP =globus pallidus (basal ganglia).


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282 BRUCE CROSSONAt a tonic level, it is necessary to limit the level of anterior corticalexcitation to prevent the entrance of extraneous material into the encodingprocess, yet to allow enough excitation for the encoding process to occurat appropriate times.In the response release mechanism, control of excitation conveyed toanterior language mechanisms by the ventral anterior nucleus is alsoexercised by cortical mechanisms through the caudate nucleus which,in turn, inhibits pallidal inhibitory mechanisms. Normally, this caudatemechanism is under inhibition from temporoparietal mechanisms; however,once encoded language has been verified for semantic content, the tem-poroparietal mechanisms will release the caudate head from inhibition,This action then causes the caudate head to inhibit the mechanism inthe globus pallidus which is responsible for limiting the flow of excitationfrom the ventral anterior thalamus to frontal language mechanisms. Theresult is a temporary increase in excitation of anterior mechanisms thatinitiates motor programming of the semantically verified language, even-tually leading to expression of the language in speech. Once the motor-programming process has been completed, impulses from the frontalmechanisms to the caudate reestablish the inhibitory control over thecaudate by temporoparietal mechanisms until the next language segmenthas been semantically verified and is ready to be programmed. Fron-tocaudate connections also influence tonic activation of anterior languagemechanisms to prevent over- or underactivation of these mechanisms byinfluences not directly associated with language, e.g., the limbic system.

IMPLICATIONS AND LIMITATIONS OF THE CURRENT MODELThe viability of any theoretical model of brain functioning dependsupon the amount of available data for which it can account and its degreeof consistency with established principles. The phenomena of subcortical

aphasia which the present theory explains, for the most part, have beendiscussed above. It also should be mentioned, however, that the theoryis consistent with many theoretical discussions of thalamic mechanismsin language which are already in the literature. For example, one groupof theorists has hypothesized that the role of the thalamus in languageinvolves the arousal or activation of cortical language mechanisms (Luria,1977; McFarling et al., 1982; Riklan & Cooper, 1973, and another grouphas proposed that the thalamus is involved in the integration of language(Botez & Barbeau, 1971; Ojemann et al., 1968; Penfield & Roberts, 1959;Schuell, Jenkins, & Jimenez-Pabon, 1965). A third group of theorists hasproposed the role of the thalamus to involve both integration and activationfacets (Cooper et al., 1968; Samra et al., 1969). Indeed, the presenttheory fits the latter category, weaving both integration and activationthreads into a theory treating the generation of language as a dynamicprocess involving not only the thalamus and cortex, but also the basalganglia and the reticular formation.


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SUBCORTICALFUNCTIONSINLANGUAGE 283The theory also should be consistent with phenomena related to corticalaphasias. For example, recent discoveries have indicated difficulties com-

prehending complex syntax (e.g., Blumstein, 1981) and apparent separationof word-finding and motor-programming problems (e.g., Tonkonogy &Goodglass, 1981) in nonfluent aphasias. These discoveries have beenincorporated into the theory as explained above.The fluent jargon in Wernickes aphasia perhaps needs further elab-oration. According to the current theory, there are two processes re-sponsible for this jargon. First, as suggested by Goodglass and Kaplan(1983), is that preverbal semantic and phonological monitoring of verbaloutput has been lost because the area responsible for this monitoring isdysfunctional. The second process is that the normal temporoparietalinhibition of the caudate is lost. This loss of inhibition results in greateractivity of caudate mechanisms which, in turn, frees the ventral anteriorthalamus from inhibition by the pallidum. The result is not only thesubstitution of one word or sound for another, but also the flow ofextraneous material into the encoding process.The empty language in anemic aphasia also can be explained withsome elaboration upon the current model. Goodglass and Kaplan (1983)have pointed out that there is a lack of substantives in this fluent language,resulting in vagueness and circumlocution. Luria (1973) discussed evidencethat this pattern in anemic (amnestic) aphasia can be caused by aninability to associate the auditory patterns of words with the visual attributesof the actual objects the words represent (though other causes mightexist as well). The defect in this particular association process is a resultof dysfunction in the left parieto-occipital area which links visual andauditory areas. This associative linkage most likely occurs in other mo-dalities such as tactile and kinesthetic as well. Spreen, Benton, and VanAllen (1966) have shown dissociation between visual and tactile namingin some aphasic patients.In the current model, verification of semantic content in languagewould require the association of the auditory patterns of words withactual physical attributes of the objects themselves which are recognizedin other modalities, such as the visual modality. In other words, monitoringsemantic content depends extensively upon these associations betweenthe auditory modality and other sensory modalities. When the mechanismfor such associations is not operative during the monitoring processdescribed above, then a message s conveyed back to the language encoder,via thalamic pathways, that the language based upon such associationscannot be verified (i.e., must be incorrect), and a process of correctingsemantic content is initiated. Even when the language encoder has selectedsemantically accurate information, it will not be released for motor pro-gramming if it involves associations in other modalities. The only languagethat can be verified, resulting in release for motor programming, is languagebased upon associations which occur exclusively within the auditory-


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284 BRUCE CROSSONverbal modality. Thus, the language system attempts to communicateusing descriptions based entirely upon auditory associations which containvague verbal approximations of the intended concepts. This accountsfor the circumlocutions and the vagueness of speech in anemic aphasiacaused by left parietal occipital lesion.The current model also accounts for the language output in the trans-cortical aphasias where repetition remains relatively intact. It has beenargued that repetition is accomplished via intact decoding and motor-programming mechanisms via functional pathways in the arcuate fasciculus.In the current model, this would mean that repetition is accomplishedprimarily through phonological mechanisms. In transcortical motor aphasia,verbal output is variable but often nonfluent. From the discussion ofthalamic mechanisms above, this type of language could be created bylesions in the anterior limb of the internal capsule which interrupt thetransmission of excitation from the ventral anterior thalamus to the fron-tal language mechanisms. The degree of agrammatism may depend uponwhether lesions extend to the insula or nearby structures (Mohr et al.,1978). Repetition is preserved if dysfunction does not extend to thearcuate fasciculus. This implies that frontal motor-programming mech-anisms for language can be activated by temporoparietal mechanisms viathe arcuate fasciculus, but such activation can only initiate repetition.Activation of spontaneous, propositional language requires thalamic ac-tivation of the language formulation system. There is some support inthe literature for this view. Many cases with lesions in the anterior limbof the internal capsule show relatively preserved repetition (and com-prehension) with dysfluent language soon after the lesion occurs (Damasioet al., 1982; Naeser et al., 1982). Further, McCarthy and Warrington(1984) showed that adding a semantic component to a repetition taskadversely affected performance in transcortical motor aphasia. This latterfinding would be consistent with repetition accomplished by intact su-perficial phonological pathways (arcuate fasciculus), but interruption ofdeep semantic pathways (thalamic).Transcortical sensory aphasia results in fluent jargon, impaired com-prehension, and relatively intact repetition. Again, unimpaired repetitionimplies intactness of the auditory phonological mechanisms in the tem-poroparietal cortex, the arcuate fasciculus, and the frontal motor pro-grammer. The jargon would result from lesions in white matter underlyingthe dominant temporoparietal region. An interruption of the pathwaybetween the temporoparietal area and the caudate would cause the flowof extraneous material into language encoding as explained above. Further,semantic monitoring would also be dysfunctional because of interruptionof pathways between the pulvinar and temporoparietal cortex. Disturbedcomprehension would imply disruption of semantic decoding.Though this model of aphasia does account for language output in themajor cortical and subcortical syndromes, it has only briefly dealt with


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SUBCORTICAL FUNCTIONS IN LANGUAGE 285the complexities of comprehension. In particular, it is of interest thatpatients with subcortical aphasias often show some comprehension deficits,even though comprehension usually is less impaired than verbal output.There are several possible explanations for this phenomenon, and thereasons may vary from case to case. First, in order to participate in theunderstanding of complex grammatical structures, anterior languagemechanisms must receive semantically decoded information from tem-poroparietal structures. In the current model, thalamic pathways act asa conduit for this semantic information; therefore, patients with thalamicaphasias should have difficulty understanding complex grammar. Thecase of Glosser et al. (1982) showed this pattern. Second, semanticinformation must also be conveyed from the decoder to other anteriormechanisms which are responsible for organizing responses to variouscommands and requests during testing. Again, this involves thalamicpathways. Third, the basal ganglia may also be involved in the motorprogramming of responses to commands or requests in a way similar totheir involvement in the programming of responses to commands orrequests in a way similar to their involvement in the programming oflanguage. Thus, dysfunction in this area could create an inability torelease programmed responses for execution or the admission of extraneousresponses into response sequences. In other words, responses to com-prehension tasks might be disrupted after the initial semantic decodingsequence.It is also possible that some subcortical lesions could prevent auditoryinformation from reaching the language decoder in the left hemisphere.This could happen by interrupting the auditory radiations from medialgeniculate to the primary auditory cortex and auditory input to the languagedecoder from the right hemisphere via the corpus callosum. Indeed,Naeser and her colleagues (1982) ound disrupted comprehension in patientswhere lesions extended across the auditory radiations from the medialgeniculate nucleus of the thalamus. Another mechanism through whichthe thalamus may be involved in comprehension is activation of thedecoding mechanisms in the temporoparietal cortex. Luria (1973) ascribedactivation of the posterior, sensory cortex to the frontal cortex. It maybe through the thalamic participation in language described above thatthe specific activation of language decoding mechanisms is optimized.Finally, it has also been accepted that certain thalamic structures (i.e.,the dorsomedial nucleus) may be involved in memory (McEntee, Biber,Perl, & Benson, 1976; Speedie & Heilman, 1983). To the extent thatmemory is involved in some comprehension tasks (e.g., four- or five-stage commands), dysfunction of those thalamic structures involved inmemory might affect comprehension. It is possible that memory andlanguage mechanisms both could be involved in some cases of thalamiclesions, particularly hemorrhage where pressure effects are likely.Another limitation of the theory as expressed herein is that it discusses


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286 BRUCE CROSSONmotor programming but only briefly deals with motor execution. Sincedysarthria is a good deal more common than aphasia after surgical lesionsof the ventral lateral nucleus of the thalamus (Cooper et al., 1968; Hermannet al., 1966), it is likely that this structure is involved in the motorexecution of speech. This also makes sense from the standpoint of atferentsto the ventral lateral nucleus from both the cerebellum and the globuspallidus and efferents from the ventral lateral nucleus to the motor cortex(Carpenter & Sutin, 1983). t was hypothesized above that speech sequencesmay be released for execution after phonological verification by an impulsefrom the temporoparietal cortex to the putamen (i.e., similar to therelease of language sequences for motor programming).

Unlike prior theoretical discussions of subcortical aphasia, the presentmodel does provide clear predictions regarding what happens to languageafter damage to various structures. For example, a lesion close to thecaudate head might interrupt fibers from the temporoparietal area to thecaudate. According to the model, this would prevent temporoparietalinhibition of caudate mechanisms which would lead to the flow of ex-traneous material into language. A lesion a few millimeters away insidethe caudate head might damage the caudate mechanisms themselves,which inhibit the inhibitory mechanisms of the globus pallidus. The resultwould be a limitation of excitation conveyed to anterior mechanisms,producing dysfluent language. A lesion of the frontocaudate fibers wouldprevent the termination of motor programming when programming of alanguage segment is complete. The result would be perseveration of aninitially programmed language segment.Yet, future verification of the theory will not be as easy as it mightseem. Lesions varying just a few millimeters could damage differentmechanisms which produce entirely the opposite results from one another.Damasio et al. (1982) discussed the possibility that small differences inbasal ganglia/capsular lesions might account for differences in two oftheir patients, one fluent, the other nonfluent. Such small differences inlocation may also be reflected in the variability of symptoms seen inthalamic aphasia. For example, the differences discussed by Alexanderand LoVerme (1980) or the unusual dysfluencies seen in the cases ofBrown (1979), Glosser et al. (1982), or McFarling et al. (1982). Mostneuroscientists would concede that current CT scans cannot distinguishsmall differences in location such as those discussed above. Thus, ver-ification of some of the finer points of the current theory may await thedevelopment of higher resolution structural imaging than is now available,or careful postmortem verification when such rare opportunities areavailable.A final word should be said regarding the implications of this modelof language production for other areas in the neurosciences. Obviously,certain specific roles have been hypothesized for the thalamus and basalganglia. In 1979, Evarts pointed out that the basal ganglia play an as yet


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SUBCORTICALFUNCTIONSINLANGUAGE 287not understood role in translating thought into action. In the realm oflanguage production, the current model takes a step toward such anunderstanding. The mechanisms postulated herein can be applied to otherproblems involving thought and movement. For example, if the mechanismsfor tone and response release in language formulation and programmingwere extended to movement, there would be implications for syndromesinvolving the basal ganglia such as Parkinsons disease and Huntingtonsdisease. The disturbance of tonic mechanisms in movement is consistentwith concepts of Parkinsons disease. Accompanying changes in mentationwith this syndrome might be related to a decrease in tonic activation offrontal mechanisms. In Huntingtons disease, on the other hand, thechoreiform movements, sometimes resembling fractions of voluntarymovements, might be related to response release mechanisms and therandom release of movements for programming. Accompanying changesin mentation with this syndrome might be related to disruption of responserelease mechanisms related to frontal function.Given the current hypotheses, it should be noted that these basalganglia diseases (i.e., Parkinsons and Huntingtons diseases) do notnormally manifest language deficits. It may be that the gradual onsetpresent in most instances of these diseases gives the brain some time toreorganize vital communicative functions. For example, Hutton, Arsenina,Kotik, and Luria (1977) described a lack of language deficits in a casewhen most of the left (language-dominant) hemisphere was removed inthree separate operations with some time intervening between operations.Nonetheless, a complete understanding of the role of the basal gangliain language requires the understanding of why acute vascular lesions canproduce lasting effects on language, but degenerative diseases of thebasal ganglia do not.With recent dopaminergic hypotheses in schizophrenia (e.g., Meltzer& Stahl, 1976), it also is tempting to apply the concepts of the currenttheory to this disorder. Nigrostriatal pathways, of course, are one of themajor dopaminergic pathways in the brain, and some theorists (e.g.,Klawans, Goetz, & Westheimer, 1972) have implicated the basal gangliain schizophrenia. Again, if the idea of tonic levels of excitation for frontalmechanisms is invoked and if present concepts are extended to formsof thought other than language generation and programming, tentativehypotheses can be generated. As applied to mechanisms for languagegeneration and programming, mechanisms for tonic anterior cortical ex-citation are mediated through the thalamus and basal ganglia. An ov-eractivation of frontal mechanisms associated wit

crosson 1985 subcortical language

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