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FROM THE ACADEMY: COLLOQUIUM INTRODUCTION

In the light of evolution VII: The humanmental machineryCamilo J. Cela-Conde

a

, Ral Gutirrez Lombardob

, John C. Avisec

,and Francisco J. Ayalac,1

aEvocog GroupInstituto de Fsica Interdisciplinar y Sistemas Complejos, Consejo Superior de

Investigaciones Cientcas, and Universidad de las Islas Baleares, 07122 Palma de Mallorca,

Spain; bCentro de Estudios Filoscos Polticos y Sociales Vicente Lombardo Toledano,

Colonia Ex-Hacienda de Guadalupe Chimalistac, C.P. 01050 Mxico D.F., Mexico; andcDepartment of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697

In his Notebook C, Darwin gave us one ofhis rst insights into human nature. There,referring to the human being, Darwin wrote:He is Mammalianhis origin has not been

indenitehe is not a deity, his end underpresent form will come, (or how dreadfullywe are deceived) then he is no exception.hepossesses some of the same general in-stincts, & moral feelings as animals.theyon the other hand cannot reasonbut Manhas reasoning powers in excess. Instead ofdenite instinctsthis is a replacement inmental machineryso analogous to whatwe see in bodily, that it does not staggerme. (1)

As Darwin noted, our mental machinerymakes us different. For instance, it allows us

to ask about ourselves, about what a humanis. It enables us to question what we are andthe ways in which we reached our currentnature. One thing we have discovered is thathumans possess certain unique mental traits.Self-reection, as well as ethic and aestheticvalues, is among them, const ituting anessential part of what we call the humancondition. The human mental machinery ledour species to have self-awareness but, atthe same time, a sense of justice, willing topunish unfair actions even if the consequen-ces of such outrages harm our own interests.

Also, we appreciate searching for novelties,listening to music, viewing beautiful pictures,or living in well-designed houses.

However, why is this so? What is themeaning of our tendency, among otherparticularities, to defend and share values,to evaluate the rectitude of our actions andthe beauty of our surroundings? The humanmental machinery obviously refers to thebrain, so the answer to the preceding ques-tions must come from neural considerations.What brain mechanisms correlate with thehuman capacity to maintain inner speech, orto carry out judgments of value? To what

extent are they different from other pri-mates comparable behaviors?

This collection of colloquium papers aimsto survey what has been learned about the

human mental machinerysince Darwinsinsights. The colloquium brought togetherleading scientists who have worked on brainand mental traits. Their 16 contributions fo-cus the objective of better understanding hu-man brain processes, their evolution, andtheir eventual shared mechanisms with otheranimals. The articles are grouped into threeprimary sections: current study of the mind/brain relationships; the primate evolutionarycontinuity; and the human difference: fromethics to aesthetics.

Current Study of the Mind/Brain

Relationships

John Searle (2) opens the proceedings witha philosophical introduction to the still elu-sive question of consciousness. To discuss theeventual scientic approach to a Theory ofMind (ToM), the author analyzes the rela-tionships between subjective feelings, likemental issues, and objective (i.e., scientic)approaches to them. Distinguishing betweenontologic and epistemic approaches to thesubjectivity/objectivity issue, Searle holds thatmental issues, such as consciousness, can bescientically reached, concluding in this way:I think the future of this entire discussion wehave been having [in the colloquium] lies ina better understanding of the brain.Indeed,this is the objective that initially led to theorganization of this Sackler colloquium.

ToM is also the approach chosen byRobert Seyfarth and Dorothy Cheney (3) inthe next contribution. As the authors state, asubconscious, reexive appreciation of othersintentions, emotions, and perspectives liesat the roots of human ToM. The adaptiveadvantages of an attribution of thoughts andintentions to predict othersbehavior mainly

consist of helping to form strong, permanentsocial bonds. Empirical study of monkeysrelationships shows these bonds. Followingthis point, Seyfarth and Cheney give data ondifferent kinds of social challenges amongfemale baboons that are better solved bymeans of afliative behavior.

Even if ToM is a good hypothesis to linkclose social relationships to mental constructsand reproductive success, an eventual bordermight separate human consciousness fromnonhuman primates more instinctivebehaviors. George Mashour and Michael

Alkire (4) focus on this eventual difference.On the grounds of a comparative review ofneurobiology, psychology, and anesthesi-ology, the authors hold that the basicneurophysiologic mechanisms supportingconsciousness in humans are found at theearliest points of vertebrate brain evolution.Mashour and Alkire propose to study thisevolution by means of models coming fromthe recovery of consciousness after generalanesthesia in animals.

Primate Evolutionary Continuity

Shared neurologic mechanisms are the mainargument in favor of continuity betweennonhuman and human primates minds.Several contributors to this Sackler collo-quium have studied these common mech-anisms in the eld of memory and its braincounterparts. Robert Clark and Larry Squire(5) offer a history of the scientic debateprovoked by Owens proposal (6) of a lack ofevolutionary continuity between human and

This paper serves as an introduction to this PNAS supplement,

which resulted from the Arthur M. Sackler Colloquium of the

National Academy of Sciences, In the Light of Evolution VII: The

Human Mental Machinery,

held January 10

12, 2013 at theArnold and Mabel Beckman Center of the National Academies of

Sciences and Engineering in Irvine, CA. It is the seventh in a series

of colloquia under the general title In the Light of Evolution(ILE;

see Box 1). The complete program and audio les of most pre-

sentations are available on the NAS Web site at www.nasonline.

org/evolution_vii. Papers from the rst six colloquia in the In the

Light of Evolutionseries titled Adaptation and Complex Design,

Biodiversity and Extinction, Two Centuries of Darwin, The

Human Condition, Cooperation and Conict, and Brain and

Behaviorwere published in earlier volumes of PNAS.

Author contributions: C.J.C.-C., R.G.L., J.C.A., and F.J.A. wrote

the paper.

The authors declare no conict of interest.

1To whom correspondence should be addressed. E-mail: fjayala@

uci.edu.

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other primates on the grounds of several

brain traits, hippocampus minor (HM)

among them (7). Because HM was proposed

to have a strong role in the organization of

memory, the possibility of using animal

models appeared, thus supporting evolu-

tionary continuity for the neuroanatomy of

human memory. Clark and Squire examine

such cross-species similarities in the eld of

the multiple-memory systems paradigm, of-

fering challenges to the animal model when

concurrent discrimination tasks are consid-

ered in both humans and monkeys.Two articles focus on the evolution of

memory. Peter Carruthers (8) points outthat, despite being fundamental to learning,speech, reading comprehension, prospection,

and planning, as well as to re

ective serialconscious reasoning, working memory (WM)has been scarcely investigated from anacross-species perspective. On the groundsof current research, Carruthers holds thatWM is a homologous trait shared by humansand nonhuman primates although our spe-cies is unique in aspects like inner speech.Also, humans may be unique in making fre-quent task-independent use of their WMabilities. However, in the absence of directcomparative studies, claims on the WMcontinuity or discontinuity remain some-what speculative.

Timothy Allen and Norbert Fortin (9)offer a complementary analysis of the largebody of research on the evolution of episodicmemory (EM). The authors propose thatproto-EM systems link avian and human

phylogenies, supporting the homologouscharacter of traits, such as hippocampal-parahippocampal-prefrontal pathways thatwould be shared from a common neuralancestry, as opposed to the alternative pos-sibility of evolutionary convergence. Despitethis shared capacity, Allen and Fortin discusseventual divergences, such as with regard tohuman language, self-consciousness, empa-thy, and ToM, holding that these constitutespecies-specic attributes associated withthe expansion in human brains of pre-frontal areas.

Differences in social behavior betweenspecies rely in part on the neuromodulatoryregulation of neural circuits. Steve Changet al. (10) offer clues on how biologicalspecializations for social function transformancestral mechanisms by means of duplica-tion, repurpose, or differential regulation atmultiple levels of organization, from neu-rons and circuits to hormones and genes.Social behavior shapes the structure andfunction of these mechanisms in a feedbackway. Therefore, the authors hold that a neu-roethological approach to the study of hu-man and nonhuman primate social behavior

might clarify the phylogeny of interactionsbetween social behavior and neuromodu-latory regulation.

The counterpart of phylogeny is ontoge-netic development. Comparisons betweenhuman and macaque neocortical develop-ment show differences that might relate therelatively prolonged neuronal maturation in

humans to the enhancement of social learn-ing and transmission of cultural practices,including language. However, few data existon the ontogenetic neural development of theapes that are more closely related to humans.By means of an experimental analysis, SerenaBianchi et al. (11) show for the rst time howPan paniscus synaptogenesis matches thehuman case, with a peak of synapse densityduring the juvenile period (25 y of age).Also, chimpanzees and humans share a latedevelopment of dendrites of prefrontal py-ramidal neurons, compared with sensorimo-tor areas, offering a common potential forenhanced developmental plasticity. The au-thors hold that their ndings suggest thatseveral key features of human brain ontogenyemerged before the divergence of the chim-panzee and human lineages.

Human Difference: From Ethics to

Aesthetics

As stated above, our species and other pri-mates share different memory systems.However, James McGaugh (12) argues in hiscontribution that, although forgetting is thecommon fate of most of our experiences,

mechanisms exist that somehow permit us tocreate lasting memories of our more impor-tant experiences. The author explores suchmechanisms. Several neurobiological systemslink this selective capacity to emotionalarousal, giving clues about how humans andother animals reach memory-enhancementepisodes by means of an activation of brainregions such as the amygdala. The fact thatsome subjects are able to keep highly superiorautobiographical memory raises the questionof how this capacity might be associated togenetic and brain particularities.

Self-awareness and the capacity to evaluateothers acts and their consequences areamong the main components of altruisticbehavior. Three articles in these proceedingsdeal with different aspects of altruism andits more extreme related behaviors. BarbaraOakley (13) examines the mechanistic basesof biased altruism, in which attempts topromote the welfare of others results in un-anticipated harm. She defends the need forquantitative models of altruistic behavioralong a spectrum ranging from strong benetto extreme harm. These models might help toscientically distinguish between benecial

Box 1.In the light of evolution. In 1973, Theodosius Dobzhansky (21) penned a shortcommentary entitled Nothing in biology makes sense except in the light of evolu-tion. Most scientists agree that evolution provides the unifying framework forinterpreting biological phenomena that otherwise can often seem unrelated and per-haps unintelligible. Given the central position of evolutionary thought in biology, itis sadly ironic that evolutionary perspectives outside the sciences have often beenneglected, misunderstood, or purposefully misrepresented. Biodiversitythe geneticvariety of lifeis an exuberant product of the evolutionary past, a vast human-sup-

portive resource (aesthetic, intellectual, and material) of the present, and a rich legacyto cherish and preserve for the future. Two urgent challenges, as well as opportunities,for 21st-century science are to gain deeper insights into the evolutionary processes thatfoster biotic diversity and to translate that understanding into workable solutions forthe regional and global crises that biodiversity currently faces. A grasp of evolutionaryprinciples and processes is important in other societal arenas as well, such as edu-cation, medicine, sociology, and other applied elds including agriculture, pharma-cology, and biotechnology. The ramications of evolutionary thought also extend intolearned realms traditionally reserved for philosophy and religion. The central goal ofthe In the Light of Evolution (ILE) series is to promote the evolutionary sciencesthrough state-of-the-art colloquiain the series of Arthur M. Sackler colloquiasponsored by the National Academy of Sciencesand their published proceedings.Each installment explores evolutionary perspectives on a particular biological topic

that is scientically intriguing but also has special relevance to contemporary societalissues or challenges. Individually and collectively, the ILE series aims to interpretphenomena in various areas of biology through the lens of evolution, address some ofthe most intellectually engaging as well as pragmatically important societal issues ofour times, and foster a greater appreciation of evolutionary biology as a consolidatingfoundation for the life sciences.

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and harmful egoistic behavior, as well asclarify the relationships among egoism, al-truism, and pathological altruism.

Sarah Brosnan (14) begins her contribu-tion with a question: What leads us to careabout justice? She proposes a comparativeapproach to clarify why justice, which is ahighly important component of our values, is

so dif

cult to achieve. By means of experi-ments on primates answers to perceivedinequities in social interactions, Brosnanconcludes that humans are not alone inresponding negatively to differential treat-ment. Although nonhuman primates do notshow a sense of justice in the same sense thathumans do, understanding their responsesmay help to anticipate, prevent, and perhapssolve problems arising from the human per-ception of inequity.

Beyond direct perception of equality/in-equality in social relationships, altruism and,more generally, human cooperation can berelated to indirect reciprocity based on rep-utation. Because social reputation is directlyobserved, but widely spread by communica-tion, indirect reciprocity can reach highlysophisticated patterns. Erez Yoeli et al. (15)offer experimental results on large-scale (atotal of 2,413 participants) cooperation be-tween small groups under laboratory con-ditions. Because the subjects were Californiaresidents of 15 homeowners associationsthat voluntarily participated in an energy-saving program, the experiment matchedreal world conditions of cooperation. Yoeli

et al.s results provide evidence that ob-servable participation in favor of publicgoods promotes cooperative behavior. Theauthors hold that reputational concerns werethe driving force to reach such a high levelof indirect cooperation, suggesting easy andpractical ways to improve future publicpolicy initiatives.

Robert Zatorre and Valorie Salimpoor (16)review empirical evidence for the neuralsubstrates of several aspects of musical per-ception. First, the authors identify the audi-tory cortical circuits that are responsible for

encoding and storage of tonal patterns. Then,they study the functional role of brain areas,such as the nucleus accumbens, codifying thereward value of music. The authors suggestthat the cortical system, highly evolved, de-codes tonal or rhythmic relationships presentin music, thereby generating expectationsabout upcoming events based on the subjectsformer events. In turn, the striatal dopami-nergic system would add the emotionalarousal associated with these predictions.

Experimental approaches to visual issuesconstitute the next contribution to thecolloquium. Leanne Chukoskie et al. (17)

study how subjects search a novel scene fora target whose location was stochasticallydrawn on each trial from a xed prior dis-tribution. Participants rapidly learn where tosearch, looking near previously rewardedlocations and avoiding previously unre-warded sites. A reinforcement-learningmodel, similar to that used previously to ex-

amine both foraging animal behavior andneuronal ring of dopaminergic cells, candescribe the resulting search performance. Inaddition, this search performance approachesthe theoretical optimum on this task. Thus,the authors offer a framework for consideringhow prior experience guides saccade choiceduring natural vision.

A complementary phenomenon providesthe focus for Oshin Vartanian et al. (18), whoprovide for the rst time clues on how vari-ation in contour impacts aesthetic judgmentsand approach decisions about the places inwhich we live and work, thereby inuencinghow we feel and act. Subjects are more likelyto judge spaces as beautiful if they are cur-vilinear rather than rectilinear. Curvilinearspaces activate the medial orbitofrontal cor-tex, a region strongly implicated in reward,which is particularly activated among archi-tects compared with nonarchitects whenassessing the aesthetic value of buildings. Incontrast, contour has no impact on approachdecisions. Contemplating curvilinear spacesactivates the precentral gyrusa region en-gaged in motor imagery and the planning ofvoluntary motor movement. Although curvi-

linear spaces did not result in a greater like-lihood of deciding to enter such areas, theymight facilitate the production of visual andmotor imagery consistent with movementplanning in that context. The authors con-clude that their research sheds light on afundamental questionwhy is it that wehave come to prefer the places that we do?

Finally, by analyzing the dynamics of brainfunctional connectivity, Camilo Cela-Conde

et al. (19) offer therst identication of brainnetworks engaged within distinct time framesduring the appreciation of beauty. A fastaesthetic perception of the beautiful/not-beautiful condition of each visual stimulusappears within 250750 ms whereas furtheraesthetic appreciation processes are sub-sequently performed in the 1,000-to 1,500-ms

range. The delayed processes activate a brainnetwork matching the default mode network,present during subjectsresting state.

Concluding Note

The explicit objective of this colloquiumimproving our knowledge of the content ofDarwins mental machineryconstitutes anendless task. However, the colloquium papersoffer fresh perspectives coming from in-terdisciplinary approaches that open newresearch elds and constitute the state-of-the-art in some important aspects of the mind/brain relationships. An intriguing contradic-

tion seems sketched from the contributionsto the colloquium. On the one hand, conti-nuity exists between the mental machinery ofhumans and nonhumans primates. On theother hand, humans manifest conspicuousevolutionarily derived, i.e., exclusive, mental/neural traits. Darwin himself solved this ap-parent paradox. In chapters III, IV, and V ofThe Descent of Man(20), Darwin holds thathuman moral and mental faculties differfrom those of animals, but not in a fun-damental way. Coming back again to theNotebook C annotation (1): [Man] possesses

some of the same general instincts, & moralfeelings as animals [. . .] but Man has rea-soning powers in excess [. . .] this is a re-placement in mental machinery.

ACKNOWLEDGMENTS. The organizers and foundingeditors of the In the Light of Evolutionseries (J.C.A. andF.J.A.) are the academic grandson and son, respectively,of Theodosius Dobzhansky, to whose fond memory thisseries is dedicated. May Dobzhanskys words and insightscontinue to inspire rational scientic inquiry into naturesmarvelous operations.

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