doi: 10.1098/rstb.2011.0195, 37-47367 2012 Phil. Trans. R. Soc. B

 William D. Hopkins, Jamie L. Russell and Jennifer A. Schaeffer study on a unique form of social tool usechimpanzees: a magnetic resonance image and behavioural The neural and cognitive correlates of aimed throwing in  

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Phil. Trans. R. Soc. B (2012) 367, 37–47

doi:10.1098/rstb.2011.0195

Research

* Authoagnessco

One concomparaevolutio

The neural and cognitive correlates ofaimed throwing in chimpanzees: a magneticresonance image and behavioural study on a

unique form of social tool useWilliam D. Hopkins1,2,*, Jamie L. Russell2 and Jennifer A. Schaeffer2

1Department of Psychology and Neuroscience, Agnes Scott College, 141 E. College Avenue,Decatur, GA 30030, USA

2Division of Developmental and Cognitive Neuroscience, Yerkes National Primate Research Center,Atlanta, GA 30322, USA

It has been hypothesized that neurological adaptations associated with evolutionary selection forthrowing may have served as a precursor for the emergence of language and speech in early homi-nins. Although there are reports of individual differences in aimed throwing in wild and captiveapes, to date there has not been a single study that has examined the potential neuroanatomical cor-relates of this very unique tool-use behaviour in non-human primates. In this study, we examinedwhether differences in the ratio of white (WM) to grey matter (GM) were evident in the homologueto Broca’s area as well as the motor-hand area of the precentral gyrus (termed the KNOB) in chim-panzees that reliably throw compared with those that do not. We found that the proportion of WMin Broca’s homologue and the KNOB was significantly higher in subjects that reliably throw com-pared with those that do not. We further found that asymmetries in WM within both brain regionswere larger in the hemisphere contralateral to the chimpanzee’s preferred throwing hand. We alsofound that chimpanzees that reliably throw show significantly better communication abilities thanchimpanzees that do not. These results suggest that chimpanzees that have learned to throw havedeveloped greater cortical connectivity between primary motor cortex and the Broca’s area homol-ogue. It is suggested that during hominin evolution, after the split between the lines leadingto chimpanzees and humans, there was intense selection on increased motor skills associatedwith throwing and that this potentially formed the foundation for left hemisphere specializationassociated with language and speech found in modern humans.

Keywords: throwing; Broca’s area; chimpanzees

1. INTRODUCTIONVisitors to the zoo are sometimes treated to the sight ofchimpanzees throwing objects (often faeces or wetchow) at each other or at them. What most zoo visitorsdo not appreciate is the rarity with which throwingoccurs in non-human animals. Save for a few unsyste-matic and anecdotal reports of throwing in monkeysand great apes [1–9], there is little evidence thatthrowing occurs in other animals [10]. Thus, throwingappears to have come under positive selection pressurein hominins. From an evolutionary standpoint, somehave suggested that throwing may have offered manyadvantages to early hominins such as the ability tokill larger prey without putting oneself at risk ofbeing wounded or killed [11]. The ability to killlarge game for the purposes of nutrition while

r for correspondence (whopkin@emory.edu, whopkins@tt.edu).

tribution of 12 to a Theme Issue ‘From action to language:tive perspectives on primate tool use, gesture, and the

n of human language’.

37

simultaneously minimizing one’s personal risk ofinjury or death (i.e. increased survival) would havebeen selectively advantageous [12]. Among non-human primates, throwing has most frequently beenobserved in wild and captive chimpanzees, thoughthere are reports in other great ape species [1,5,6,8]and, to a lesser extent, in monkeys [13–15]. Throwinghas been described as a form of tool use in chimpan-zees at a number of long-term field sites in Africa,including Gombe, Mahale, Bossou and the Tai forest[16–19]. In the wild and in captivity, throwing hasmostly been recorded in the context of both interand intraspecies agonistic encounters, although somehave described it as a means of initiating play orcommunication [20–22].

From a psychological and neurological standpoint,aimed throwing is very interesting for several reasons.First, it has been hypothesized that some instances ofaimed throwing by chimpanzees reflect foresight orfuture planning on the part of the apes, an abilityoften described as uniquely human [23]. For instance,Osvath [7] eloquently describes a zoo-living male

This journal is q 2011 The Royal Society

Figure 1. Four sequential frames demonstrating a chimpanzee throwing a polyvinylchloride (PVC) pipe towards a human ina tower above the subject. The chimpanzee stands bipedally, brings the PVC pipe back and then throws the object. Note thatthe force of the chimpanzees’ throw causes him to leave the ground. This reflects the whole body function of throwing in some

of the chimpanzees.

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chimpanzee (named Santino) that hides rocks out ofsight of the care staff, waiting to reveal and throwthem at approaching visitors at the most opportunetime. Evidence of planning comes from the observationthat Santino searches for the rocks from a moat insidethe enclosure prior to the arrival of the care staff andvisitors, and caches the rocks out of sight, only to pullthem out when the visitors arrive. We have made similarobservations of this type of the so-called planning be-haviour in the chimpanzees housed at the YerkesNational Primate Research Centre (YNPRC) and theUniversity of Texas M. D. Anderson Cancer Centre[4]. Some of the chimpanzees will pile faeces or wetchow in their cage and wait for visitors to pass bybefore throwing this at them. We would further arguethat aimed throwing in the YNPRC chimpanzees,though often agonistic in function and consequence, isnot part of the apes’ display behaviour. Indeed, mostinstances of aimed throwing that we have observedoccur without any accompanying display behaviourssuch as pilo-erection, hooting or charging, furthersuggesting an element of planning on the part of theindividual ape.

Throwing, as a form of social tool use, is alsounique because it likely develops in captive chimpan-zees (and possibly wild apes) by way of very differentprocesses and reinforcement contingencies comparedwith other forms of tool use, notably those describedfor the purposes of food extraction. For instance,nut-cracking, termite-fishing and ant-dipping are byfar the most common forms of tool use observed inwild chimpanzees and each of these is used for thepurposes of obtaining otherwise unattainable food.Thus, in purely operant conditioning terms, the sub-jects learn to use these types of tools and maintaintheir use because they have been reinforced withfood for successful use. Presumably, food is positivelyreinforcing and therefore increases the probability ofsubsequent occurrence of tool-use behaviour (thoughwe would acknowledge that some forms of tool usemay be maintained without explicit reinforcement).

In contrast, the rewards associated with throwing arequite different because they are not nutritive in form.Throwing in wild chimpanzees is seldom, if ever,observed for the purposes of obtaining food, butrather is almost always directed towards other chimpan-zees or humans. In captivity, it is difficult to imagine thathuman caretakers would overtly reward a chimpanzee

Phil. Trans. R. Soc. B (2012)

with food immediately after they had just been soiledwith faeces by the very same ape. In short, what appearsto be the main reward for throwing is the simple abilityto control or manipulate the behaviour of the targetedindividual (ape or human). For example, in our labora-tory, chimpanzees will patiently wait for strangers orvisitors to approach and then will throw at them. Theydo not conceal their intentions and they will oftenstand bipedal and threaten to throw by cocking theirarm with the projectile in their hand in preparation forthrowing (figure 1). The passers-by can see this andwill often try and negotiate with the chimpanzees toput down the projectile, or they will try to trick theape by stopping, then dashing rapidly past the apeenclosure. This seems to be the reaction the apes hopeto get from the humans and, in operant conditioningterms, is the only ‘reward’ the chimpanzees receivefor throwing.

Neurologically, throwing is complex because itdemands coordinated precision in timing the velocityand release window of a projectile in relation to thespeed of movement and distance of the target (i.e.prey). Some have suggested that the increased selectionfor neural synchrony of rapid muscular sequencing rou-tines associated with actions such as throwing are similarto the motor programming demands of language andspeech, and therefore engage similar neural systems,notably Broca’s area [24]. Moreover, because the lefthemisphere is dominant for language, some haveargued that the foundations for left hemisphere laterali-zation in language may have evolved from an initialpreadaptation for right-handedness in throwing [11].In Western cultures, a significant majority of individualsself-report preferring the right-hand for throwing [25],and studies in non-traditional societies have reportedright-hand biases in throwing actions, such as inthe use of spears [26]. Two previous studies havereported that captive chimpanzees show population-level right-handedness for throwing, which suggestsleft hemisphere dominance [4]. Hopkins et al. [4] havealso found that posture influences handedness forthrowing. Within the subsample of 89 chimpanzeesthat were observed to reliably throw by Hopkins et al.[4], 90 per cent of right-handed individuals preferred tothrow overhand compared with underhand. A majorityof the overhand throws were made when the chimpan-zees were standing bipedally. In contrast, a significantmajority of the left-handed individuals threw underhand

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when they were in a quadrupedal posture. Thus, hand-edness was strongly linked to the posture and style ofthrowing adopted by the apes. Despite the long-standingtheoretical interest in throwing in relation to brain evol-ution, few studies to date have examined the potentialneural correlates of throwing in non-human prima-tes, notably chimpanzees [27]. In a previous study,Cantalupo & Hopkins [27] found that chimpanzeesthat had learned to throw reliably had significantlylarger cerebella than those that had not. Throwingoffers a unique opportunity to consider cortical plas-ticity in chimpanzees because, as noted already, thereare considerable individual differences in terms of itsoccurrence and lateralization.

One aim of this study was to examine whethervariation in either grey matter (GM) or white matter(WM) within premotor and primary motor cortex wasassociated with the occurrence and lateralization ofthrowing in captive chimpanzees. Specifically, magneticresonance image (MRI) scans were obtained in 76chimpanzees and the proportions of WM to GM inthe left and right hemispheres were computed for twocortical motor regions, including the motor-hand areaof the precentral gyrus (termed the KNOB) and theinferior frontal gyrus (IFG). The KNOB was selectedas a region of interest because it is the anatomicalregion of the precentral gyrus where the hand is rep-resented, and studies in humans and chimpanzeeshave shown that asymmetries in this brain area areassociated with hand preference [28–30]. Additionally,we measured the IFG because it is the homologue toBroca’s area in the human brain [31,32] and previousstudies in humans and chimpanzees have shown thatvariation in asymmetries in this region are associatedwith hand use for tool use [33–35]. If handedness forthrowing is associated with asymmetries in these twomotor regions, then we hypothesized that right-handed throwers would show leftward asymmetrieswhile left-handed throwers would show rightward asym-metries. We further hypothesized that if learning tothrow promotes the development of connectionsbetween cortical regions, then chimpanzees that reliablythrow would show increased WM within the IFG andKNOB regions compared with individuals that havenot learned to throw. We were particularly interestedin WM because recent diffusion tensor imaging (DTI)studies have shown that training experiences can havea significant effect on cortical connectivity. For instance,Scholz et al. [36] measured WM connectivity in asample of naive human participants and subsequentlyhad them learn how to juggle. Post-training DTI ima-ging revealed increased cortical WM in several brainregions, but notably in regions underlying the intrapar-ietal sulcus. More germane to this study, Quallo et al.[37] imaged three monkeys before and after trainingthem on a tool-use task. Using voxel-based morphome-try, significant increases in GM were found in severalregions, including the intraparietal and superior tem-poral sulci. Furthermore, increased levels of WM werefound bilaterally in the cerebellum—a brain structurethat is critically involved in motor learning andcoordination—after learning the tool-use task.

A second aim of this study was to test whetherchimpanzees that have learned to throw are socially

Phil. Trans. R. Soc. B (2012)

more sophisticated or intelligent than those that havenot. As noted above, we and others have noted thatchimpanzees that throw exhibit a considerable degreeof planning in their actions and seem to know thatthey can use their throwing actions to manipulate orchange the behaviours of other social beings, notablynaive human observers. This suggests that these apesare more sensitive to how their actions influence thebehaviours of others. Leavens et al. [38] argued thatmost ape gestural communication observed in captiveindividuals’ functions in a similar manner. That is,when apes point to otherwise unattainable foods inthe presence of humans, they are instrumentally con-trolling or manipulating the human to get the foodfor them, or in essence the human becomes the tool.For this reason, we hypothesized that apes that throwmight be more socially or communicatively sophisti-cated than those that have not learned to throw. Wetested this hypothesis by comparing the chimpanzeesthat reliably throw to non-throwers on a series of cog-nitive tasks that quantify physical and social cognitionin apes. Specifically, Herrmann et al. [39] havedescribed a series of tasks, referred to as the primatecognition test battery (PCTB), which allegedlymeasures the abilities of human children and non-human primates to use social and physical cues tosolve different types of learning problems. Broadly,the tasks assess communication abilities, comprehen-sion of causality, spatial cognition and memory,quantity discrimination and theory of mind. We haverecently tested more than 90 chimpanzees on thesetasks [40] and, in this study, we compared the per-formance of throwing and non-throwing apes toexamine whether performance differences were evi-dent in these groups.

2. METHODS(a) Subjects

Magnetic resonance images were obtained from asample of 78 chimpanzees, including 24 males and 54females. The subjects ranged in age from 6 to 51 years(mean ¼ 23.05, s.d. ¼ 11.80). All the chimpanzeeswere members of a captive colony housed at YNPRCin Atlanta, GA, USA. Within the sample, there were38 chimpanzees that reliably threw, and these individ-uals were matched on the basis of sex, age andscanning protocol with 38 chimpanzees that did notreliably throw. This was done to control for these poten-tial confounding variables within the sample.

(b) Image collection and procedure

For the in vivo scanning, subjects were first immobilizedby ketamine injection (10 mg kg21) and subsequentlyanaesthetized with propofol (40–60 mg (kg h21)21)following standard procedures at the YNPRC. Subjectswere then transported to the MRI facility. The subjectsremained anaesthetized for the duration of the scansas well as the time needed to transport them betweentheir home cage and the imaging facility (total timeapproximately 2 h). Subjects were placed in the scannerchamber in a supine position with their head fittedinside the human-head coil. Scan duration rangedbetween 40 and 60 min as a function of brain size.

T1-weightedFO

PCI

IFG

KNOB

CS

grey matter white matter(a)

(b)

Figure 2. (a) T1-weighted axial view of a chimpanzee MRIscan followed by the segmented grey matter (GM) andwhite matter (WM) view. The landmarks used to quantifythe IFG are indicated as well as the object maps as theywere applied to the two segmented volumes. (b) Axial view

of the KNOB region traced T1-weighted MRI scan withthe object maps then applied to the GM and WM volumes.CS, central sulcus; FO, fronto-orbital sulcus; IFG, inferiorfrontal gyrus; PCI, precentral inferior sulcus.

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A portion of the subjects were scanned using a 1.5 Tscanner (Phillips, Model 51), while the remaining chim-panzees were scanned using a 3 T scanner (SiemensTrio, Siemens Medical Solutions USA, Inc., Malvern,Pennsylvania, USA) at the YNPRC.

For all chimpanzees scanned in vivo using the1.5 T machine, T1-weighted images were collected inthe transverse plane using a gradient echo protocol(pulse repetition ¼ 19 ms, echo time ¼ 8.5 ms,number of signals averaged ¼ 8, and a 256 � 256matrix). For the chimpanzees scanned using the 3 Tscanner, T1-weighted images were collected using athree-dimensional gradient echo sequence (pulserepetition ¼ 2300 ms, echo time ¼ 4.4 ms, number ofsignals averaged ¼ 3, matrix size ¼ 320 � 320).

After completing MRI procedures, the subjectsscanned in vivo were returned to the YNPRC and tem-porarily housed in a single cage for 6–12 h to allow theeffects of the anaesthesia to wear off, after which theywere returned to their social group. The archived MRIdata were transferred to a PC running Analyze 7(Mayo Clinic, Mayo Foundation, Rochester, MN,USA) software for post-image processing. Prior todata collection, two raters blind to the hemisphereand handedness of the chimpanzees independentlymeasured the IFG and KNOB in 10 specimens.Inter-rater correlations between the two tracers werepositive and significant for both regions [30,41].Prior to measurement, the raw T1-weighted MRIscans were aligned in the axial, coronal and sagittalplanes along the AC-PC line.

(i) Inferior frontal gyrusThe IFG was quantified separately for the leftand right hemispheres in the axial (transverse) planefollowing procedures that have been described else-where [41] (figure 2a). The most dorsal point of theIFG slice was defined as the slice on which boththe precentral inferior (PCI) and fronto-orbital (FO)sulci could be seen. Using a freehand tool, PCIwas traced to the lateral portion of the brain andwas followed until meeting FO. FO was then tracedto its most medial point and the most medial pointsof FO and PCI were then connected with a straightline to create an estimate of the area of the gyrusbetween these two sulci for each slice. Both sulcihad to be present to be considered a traceable slice.Successive 1 mm slices were traced using these land-marks until either FO or PCI were no longer visible.The areas within the traced regions were subsequentlysummed to derive volumes of the IFG for eachhemisphere. These IFG object maps for the rightand left hemispheres were saved for each individualsubject and subsequent application to the segmentedvolumes.

(ii) Motor-hand area or KNOBAs with the IFG, the KNOB was quantified separa-tely for the left and right hemispheres in the axial(transverse) plane (figure 2b) following procedurespreviously used in human and chimpanzee brain speci-mens [29,42]. The dorsal and ventral edges of theKNOB along the central sulcus (CS) served as markers

Phil. Trans. R. Soc. B (2012)

for defining the boundaries of the area. The area of theentire KNOB was traced on each slice and hemisphereusing a mouse-driven pointer (figure 2b). The areaswithin the traced regions were subsequently summedto derive volumes of the KNOB for each hemisphere.These KNOB tracings for the right and left hemisphereswere saved for each individual subject.

(c) Image segmentation and region of interest

measurements

The aligned T1-weighted MRI scans were skull-stripped and subsequently segmented into GM, WMand cerebral spinal fluid (CSF) tissue using FSL (Analy-sis Group, FMRIB, Oxford, UK) [43] (figure 2a,b).Because the segmented volumes were in the samestereotaxic space as the T1-weighted scans on whichthe object maps for the IFG and KNOB were drawn,the object maps were then applied to the segmentedGM and WM, and the number of voxels that fellinside the object maps were calculated for each region,subject and hemisphere. We then divided the numberof voxels by the total size of the object maps and multi-plied by 100 to compute the percentage of GM or WMwithin each region and hemisphere. To simplify theanalyses, we calculated WM-to-GM ratios for eachhemisphere and region by dividing the WM percentageby the GM percentage (WM_GM ratio). Thus, the leftand right hemisphere WM percentages for theKNOB and IFG were divided by the left and rightGM percentages. We then computed average WM-to-GM ratios for the KNOB (WMGM_KNOB) andIFG (WMGM_IFG) by adding the values for the leftand right hemispheres and dividing by two. Wealso computed asymmetry quotients (AQ) for theKNOB_AQ and IFG_AQ by using the formula AQ ¼(R 2 L)/((R þ L)�0.5), where R and L reflect theWM-to-GM ratios for the right and left hemisphe-res. Positive AQ values reflected right hemisphere

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asymmetries, while negative values indicated lefthemisphere biases.

(d) Primate cognition test battery

(i) ProceduresSubjects were tested on a modified version of thePCTB originally described by Herrmann et al. [39].The PCTB attempts to assess subjects’ abilities in var-ious areas of physical and social cognition. For ourstudy, some aspects of the original PCTB were elimi-nated owing to time and housing constraints. Thepreviously published procedures were followed as clo-sely as possible but some tasks were modified to betteraddress the questions at hand, given the past experi-ence and environmental constraints of our subjects.Each task is described briefly below with notes madewhen procedures were altered from those describedby Herrmann et al. [39]. Subjects were generallytested in the order that the tasks are presented belowand testing was completed over three to five testingsessions, depending on the motivation and attentionof the subject. Most subjects were tested alone; how-ever, some individuals are uncomfortable beingseparated from their group. These individuals weretested with one other conspecific with whom theywere comfortable. All testing was done in the subject’shome enclosure.

(e) Physical cognition tasks

Eight tasks were used in the ‘Physical Cognition’ por-tion of our test, including tasks exploring the apes’spatial memory and understanding of spatial relation-ships, ability to differentiate between quantities,understanding of causality in the visual and auditorydomains and their understanding of tools. Our testdiffered from the original PCTB in several ways.We excluded the Addition task as well as certaincomponents of the Tool Properties tasks.

(i) Spatial memory (three trials)This test assessed subjects’ ability to remember thelocations of food rewards. In this task, the subjectwatched as food was hidden in two of three possiblelocations (opaque cups turned upside down) on atest table in front of them. The subject was thenallowed to search the locations one by one. If the sub-ject located one of two hidden food rewards, they weregiven the reward and allowed to search for the secondhidden reward. Subjects that located both hidden fooditems without searching the unbaited location werescored as successful. Each subject received all threepossible combinations of baited locations.

(ii) Object permanence (nine trials)Here, we tested an individual’s ability to follow a foodreward after invisible displacement, given three differentpossible displacements. During single displacementtrials, only one of three possible locations was mani-pulated and thus potentially baited. In the doubledisplacement trials, two of three possible locationswere manipulated, meaning that either location couldpotentially be baited. Double displacement trials werefurther divided by whether or not the baited locations

Phil. Trans. R. Soc. B (2012)

were adjacent to one another. In order to be consideredsuccessful, the subject must locate the hidden food itemwithout searching in the location that was notmanipulated.

(iii) Rotation (nine trials)In the third task, subjects’ ability to track a foodreward as it is spatially rotated either 1808 or 3608was examined. In this task, subjects watched as afood reward was hidden in one of the three locations(opaque cups turned upside down) lined up on a plat-form. The platform was then rotated on a horizontalplane, with the three locations being rotated as aunit. Three different manipulations were employed.In 1808 middle trials, the middle location was baitedand the platform was turned 1808. In 3608 side and1808 side trials, either the left or right location wasbaited, and the platform was then rotated 3608 or1808, respectively. Subjects successfully completed aRotation trial by tracking and identifying the correctlocation of the hidden reward.

(iv) Transposition (nine trials)In this task, subjects watch as a food reward is hiddenin one of three possible locations and then as thebaited location is changed in one of the three ways.In one condition, the baited location is switched withone of the unbaited locations. In the second condition,the baited location is switched with one of theunbaited locations and then the two unbaited locationsare switched. In the last condition, the baited locationis switched with one of the unbaited locations and thenwith the other unbaited location. Subjects receivedthree trials of each condition. To be considered suc-cessful on this task, the subject must track thereward and choose the baited location.

(v) Relative numbers (13 trials)In the fifth task, subjects were tested for their ability todiscriminate between different quantities by being pre-sented with two plates containing different amounts ofequally sized food pieces. Each subject received thesame set of 13 different quantity pairings as those usedin the original PCTB (1 : 0, 5 : 1, 6 : 3, 6 : 2, 6 : 4, 4 :3, 3 : 2, 2 : 1, 4 : 1, 4 : 2, 5 : 2, 3 : 1 and 5 : 3). Duringeach trial, the subject was allowed to choose only oneplate and received whatever reward was on the chosenplate. A correct response was recorded when the subjectchose the plate containing the larger quantity of food.We did not include the task by Herrmann et al. [39]referred to as Addition Numbers.

(vi) Causality noise (six trials)In the sixth task, subjects’ understanding of causalrelationships based on sound was assessed. In thistask, the experimenter placed a hard food reward (i.e.peanut) in one of the two metal containers such thatthe container with the food reward made a soundwhen shaken, while the unbaited container did not.In ‘Full’ trials, the metal container containing thefood reward was lifted and shaken and then theunbaited container was lifted. In the ‘Empty’ trials,the empty container was lifted and shaken and then

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the baited container was lifted. Subjects were thenallowed to choose one of the two containers. A correctchoice was recorded when the subject chose the baitedcontainer.

(vii) Causality visual (six trials)In the seventh task, subjects were tested for their causalunderstanding of the physical world in the visualdomain. Specifically, in one trial type, a food rewardwas placed underneath one of two boards lying flat onthe testing table. The food caused the baited board tobe tilted, while the unbaited board remained flat. Inthe second trial type, a food reward was placed under-neath one of two pieces of cloth laying flat on thetesting table. The reward created a visible bump in thebaited cloth, while the unbaited cloth lay flat. Subjectsreceived three trials with both the board and cloth. Inboth trial types, the subject had to choose the baiteditem to be considered successful.

(viii) Tool properties (six trials)The last Physical Cognition task explored the apes’understanding of the physical properties of tools andhow those relate to achieving a goal. In each task, thesubject is presented with a choice between two similartools. However, one tool can be used to obtain a foodreward, while the other tool is ineffective. For the firsttask, subjects are presented with two identical piecesof paper. One piece of paper has a food reward sittingon top of the far end, while the second piece of paperhas a food reward sitting beside it. The subject couldpull either piece of paper into their cage, but only bypulling the paper with the food sitting on top of itwould they be able to retrieve the food reward. In thesecond task, one tool was identical to the effective toolin the first task. The second tool consisted of two smallerpieces of paper with a small gap between them, visuallyemphasizing that they are disconnected. The foodreward is placed on the out-of-reach piece of the two dis-connected pieces of paper. The subject could pull in thereward using the effective tool, but pulling the piece ofthe disconnected paper is ineffective in obtaining thereward. Each subject received three trials for each toolproperty task. Note that we did not include three toolproperties tasks from the original PCTB, ‘Bridge’,‘Broken Wool’ and ‘Tray Circle’ [39].

(f) Social cognition tasks

The tasks designated as ‘Social Cognition’ in thePCTB that we used are fourfold. The first two aredesigned to test the apes’ ability to understand andto produce communicative signals. The third set oftasks assesses their sensitivity to the attentional stateof an experimenter and their ability to use appropriatecommunicative modalities based on this information.The last social cognition task is designed to assessrudimentary aspects of Theory of Mind by testingtheir ability to follow gaze. Owing to housing andtime constraints, we excluded the Social Learningtasks done in the original PCTB and made somemodifications to several of the other Social Cognitiontasks noted as follows.

Phil. Trans. R. Soc. B (2012)

(i) Comprehension (six trials)For the first task, we chose a slightly different strategyfrom that of Herrmann et al. [39] to assess the apes’abilities to comprehend communicative signals. Theoriginal task implemented the same table-and-cupset-up as used in many of the other physical cognitiontasks. However, in our task, a target was placed on theleft and right sides of the enclosure, while the subjectwas centred. The experimenter then used either gaze(three trials) or gaze combined with a manual point(three trials) to direct the subject to one of the two tar-gets. The subject had to move to and touch thedesignated target to be considered successful on thistask. Note that we did not include the ‘Mark’condition conducted by Herrmann et al. [39].

(ii) Production (four trials)For the second task, following the established PCTBmethods, the apes’ ability to produce communicativesignals to indicate a hidden food item was tested infour trials [39]. In this task, the ape watched as anexperimenter baited a location on either the far leftor far right side of the enclosure. A second exper-imenter then approached the cage, centred thesubject and waited for the subject to indicate whichlocation contained the hidden food. The subject wasgiven 60 s to indicate the correct location using anovert communicative signal, such as a manual gesturetowards the hidden food.

(iii) Attentional state (eight trials)In the third task, we followed the methods outlined byHerrmann et al. [39] but added an additional test.First, an experimenter placed a piece of food on theground outside of the subject’s enclosure. Then asecond experimenter approached the cage and alteredtheir attentional state in one of four ways. In the firsttrial, the experimenter’s face and body were directedtowards the food item and the subject. In the secondtrial, the experimenter’s body faced the subject, buther face was turned away. In the third trial, the exper-imenter stood with her body facing away from theenclosure, but then turned her head to look at the sub-ject. In the last trial, the experimenter’s body and facewere oriented away from the subject. In order to be suc-cessful, the subject had to use a communicative signal inthe modality appropriate to the experimenter’s atten-tional state. For example, if the experimenter waslooking at the subject, he/she could use a visual signal,such as a manual gesture to indicate the food. However,if the experimenter was facing away from the subject, thesubject had to first use an auditory or tactile signal, suchas a cage bang or a spit to get the attention of the exper-imenter and then once the experimenter was looking athim/her, use a visual signal to indicate the food. Tofurther explore this topic, we added an additional setof four trials using the same basic conditions. However,the trials were conducted in a more familiar setting withthe experimenter sitting at the testing table, placing apiece of food on the table and then carrying out thefour variations of attentional state. The same require-ments regarding modality-specific communication

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(±

s.e.

)

Figure 3. Mean white-to-grey matter ratio (Mean WM_GMRatio) (+ s.e.) for chimpanzees that reliably throw

(THROWþ; narrow-striped bars) and those that do not(THROW2; wide-striped bars).

0.400.35

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0.150.100.05

–0.050

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M A

Q (

± s.

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were required for the subject to be considered successfulon any given trial.

(iv) Gaze following (three trials)For the last social cognition test, we examined eachape’s ability to follow gaze in three trials. In this task,an experimenter sat on a stool approximately 1 m fromthe subject’s enclosure. The experimenter capturedthe subject’s attention and centred him/her by offeringa piece of food. The experimenter then shifted herhead and eyes to gaze at a point directly above herhead for a period of 10 s. In order to be successful, thesubject had to follow the gaze of the experimenter bylooking upward. Note that we did not test our subjectson two of the gaze following tasks, ‘Back’ and ‘Eyes’,used in the original PCTB [39].

(v) Data analysisThe mean proportion of correct trials was calculatedfor each of the 12 tasks. From these data, we computedaverage performance scores for the five basic cognitivedimensions originally described by Hermann et al.,which include COMMUNICATION (Comprehension,Production and Attentional State), CAUSALITY(Visual Causality, Tool Properties and Noise), SPACE(Spatial Memory, Object Permanence, Rotation andTransposition), QUANTITY (Relative Numbers) andTHEORY OF MIND (Gaze Alternation).

–0.40–0.35

–0.25

–0.15–0.10

–0.30

–0.20

KNOB IFGbrain region

mea

n W

M

Figure 4. Mean WM_GM AQ scores (+ s.e.) for the IFGand KNOB in right- and left-handed throwing chimpanzees.

Narrow-striped bars, left; wide-striped bars, right.

3. RESULTS(a) Neuroanatomical correlates

In our initial analyses, we compared the proportion ofWM to GM within the IFG and KNOB betweenmales and females. These analyses were compared onboth the WMGM_KNOB and WMGM_IFG andKNOB_AQ and IFG_AQ values. For both analyses,no significant main effects or interactions were found.Thus, male and female chimpanzees did not differin the proportion of WM to GM nor in lateralizationfor the IFG and KNOB.

We next considered the influence of throwing on theproportion of WM to GM within the KNOB and IFG.For this analysis, we performed a mixed model analysisof variance (ANOVA) with region (WMGM_IFG,WMGM_KNOB) serving as the within-subject factor,while throwing classification (THROWþ, THROW2)was the between-group factor. Significant main effectsfor region (F1,74 ¼ 41.02, p , 0.001) and throwingclassification were found (F1,74¼ 5.6820, p , 0.03).The proportions of WM found within the regionobject maps were significantly higher for the KNOBcompared with those for IFG. Moreover, for bothregions, the proportion of WM was significantlyhigher in the THROWþ than in the THROW2 chim-panzees. The mean WGGM_KNOB andWMGM_IFG in THROWþ and THROW2 chimpan-zees are shown in figure 3.

(b) Neuroanatomical correlates of laterality

in throwing

We next considered whether interhemispheric differ-ences in the ratio of WM to GM were found forleft- and right-handed chimpanzees on the basis of

Phil. Trans. R. Soc. B (2012)

their preferred hand for throwing. For this analysis,we performed a mixed model ANOVA with theKNOB_AQ and IFG_AQ values serving as thewithin-subject factor, while throwing preference(LEFT, RIGHT) was the between-group factor. A sig-nificant main effect for throwing hand was found(F1,36 ¼ 5.462, p , 0.03; figure 4). Right-handedthrowers rather than left-handed throwers showedsignificantly greater leftward asymmetries in theWM-to-GM ratio for the IFG and KNOB.

(c) Cognitive correlates of throwing

As noted earlier, our laboratory has administeredthe PCTB test to 91 chimpanzees, and within thissample, there were 39 apes that threw consistently(THROWþ) and 52 that did not (THROW2). Inthis next analysis, we compared THROWþ andTHROW2 individuals in their performance on thePCTB task. To test whether differences in cognitive abil-ities were evident between the two groups, we conducteda multiple analysis of variance (MANOVA) with themean PCTB scores serving as dependent measures,while sex and throwing group served as the between-group factors. The MANOVA revealed a significant

0.8

0.7

0.6

0.5

communicate space causality

cognitive construct

quantity TOM

0.4

0.3

0.2

0.1

mea

n pe

rcen

tage

cor

rect

(±

s.e.

)

0

p < 0.001

Figure 5. Mean percentage correct (+ s.e.) for the five cognitive abilities tested with the PCTB tasks in the chimpanzees(see text for description of the tasks). Narrow-striped bars, THROWþ; wide-striped bars, THROW–.

44 W. D. Hopkins et al. Throwing in chimpanzees

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main effect for throwing group (F5,86¼ 3.642, p ,

0.001). Subsequent univariate F-tests indicated that theonly significant difference between the throwing groupswas for COMMUNICATION (F1,87¼ 11.388, p ,

0.001) with THROWþ apes performing significantlybetter than the THROW2 individuals (figure 5). Noother significant differences were found.

4. DISCUSSIONIn terms of the neuroanatomical correlates of throwing,the results reported here indicate that the presence ofthrowing skills in chimpanzees is correlated withincreased cortical connectivity in Broca’s area as wellas in the motor-hand area of the precentral gyrus. Theprincipal result in support of this conclusion is theobservation that THROWþ apes had significantlyhigher proportions of WM to GM within the IFG andKNOB regions than THROW2 individuals. Becauseincreased WM indicates more myelinated interneuronsthat connect different cortical regions, this result wouldsuggest that learning to throw may alter the connectivitybetween premotor and primary motor cortex in thechimpanzee. The results from comparing right- andleft-handed throwers also support this conclusion,because differences in WM are hemisphere-specificand contralateral to the preferred hand that the chim-panzees use for throwing. The association betweenhand preferences for throwing and asymmetries withinthe IFG and KNOB are also consistent with previousstudies showing that handedness for other forms oftool use, such as simulated termite-fishing and nut-cracking, is linked to lateralization in the corticallanguage area homologues of chimpanzees [33,44]. Itshould also be noted that asymmetries in hand use formanual gestures are associated with asymmetrieswithin the IFG [45] Thus, the results reported hereare consistent with the evolutionary hypothesis that

Phil. Trans. R. Soc. B (2012)

throwing may have served as a preadaptation for theneural adaptation of motor programmes necessary forcomplex motor actions, including language andspeech [11].

It should also be noted that hand preferencesfor throwing are linked to variation in handedness forother measures of tool use and communication, but notnon-tool-use measures of manual action. For instance,we have a large sample of hand preference data inchimpanzees for actions such as simple reaching, coordi-nated bimanual actions, simulated termite-fishingtool use and manual gestures [46–49]. Interestingly,right- (n ¼ 44) and left-handed (n ¼ 37) throwers differsignificantly in their handedness for simulated termitefishing t79 ¼ 2 2.50, p , 0.02 and manual gesturest79 ¼ 2 2.59, p , 0.02, but not for simple reach-ing t79 ¼ 2 1.20, n.s. or for coordinated bimanualactions t79 ¼ 2 0.62, n.s. (figure 6). Thus, as with theneuroanatomical data, there is an explicit link betweenthrowing, simulated termite fishing and gesturalcommunication in terms of lateralization of function.

We also found that chimpanzees that have learnedto throw are better at communication tasks than chim-panzees that have not. Interestingly, these two cohortsof chimpanzees do not differ on cognitive tasks thatassess dimensions of physical cognition. These resultssuggest an explicit association between the cognitivefoundations for throwing and the ability to engage insuccessful intraspecies communication, at least asassessed by the PCTB. Leavens et al. [38] haveargued that, in captivity, chimpanzees learn to gestureto humans for foods that are otherwise unavailable tothem by solving the referential problem space. Thatis, the chimpanzees want the food, but the foodcannot be reached owing to physical barriers prevent-ing the apes from attaining the foods. What thechimpanzees have learned to do with their gesturesand other signals, such as attention-getting sounds,

gesture–0.2

–0.1

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n ha

nded

ness

inde

x (±

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)

0.3

0.4

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0.7p < 0.01

p < 0.01

0

tool use

handedness measure

reaching tube

Figure 6. Mean handedness index (HI) scores (+ s.e.) forhandedness measured in chimpanzees that prefer to throwwith the right hand compared with those with the left. HIscores are computed by using the formula AQ ¼ (R 2 L)/

R þ L), where R and L reflect the number of right- andleft-hand responses. Positive HI values reflect right-handpreferences and negative values reflect left-hand preferences,respectively. Narrow-striped bars, THROWþ; wide-stripedbars, THROW–.

Throwing in chimpanzees W. D. Hopkins et al. 45

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is to manipulate humans to obtain the food for them.Thus, in essence, the human becomes a tool for them.Indeed, we would argue that if a physical tool wasavailable in these contexts, such as a long stick, thechimpanzees would use them to get the food ratherthan wait for a human caretaker to come by andretrieve the food for them.

Cognitively, we believe that the development andacquisition of throwing skills by chimpanzees operatesin a manner similar to the emergence of manual ges-tural communication. As noted previously, themotivation for throwing in chimpanzees is largely toalter the behaviour of other individuals (be it humanvisitors or conspecifics). For this reason, the apesthat have learned to throw have acquired an ability tounderstand how their behaviour affects the behavioursof others. If the same individuals apply these basicskills within the context of (i) understanding gestures,(ii) producing gestures, and (iii) using attention-gettingbehaviours when a human experimenter is inattentive tothem, then it would follow that the THROWþ individ-uals should outperform the THROW2 apes on thePCTB test. Moreover, these same skills may not offerany advantage in tasks that are not communicativein function.

We have focused on aimed throwing by chimpan-zees in this paper, but some discussion of theprevalence of throwing in other species seems war-ranted within the context of the underlying cognitiveprocesses that appear to accompany this ability inapes. In particular, capuchin monkeys have beenreported to engage in aimed throwing [14] and theyhave well-documented tool-using abilities both in thewild and in captivity [50–56]. On the basis of ourresults in chimpanzees, this leads to the suggestionthat capuchin monkeys might also engage in someforms of gestural communication during intraspeciesinteractions; however, this has not been frequentlyreported in the literature [57]. Thus, the

Phil. Trans. R. Soc. B (2012)

interconnection in social cognitive abilities betweenthrowing and gestural communication may not bewell developed in the capuchin monkey. We wouldalso point out that, though the capuchin monkeys inthe studies by Westergaard & Suomi [15] did learnto throw, their behaviour was explicitly shaped by theinvestigators by initially having the subjects throw anobject into a bucket containing peanut butter (a pre-ferred food). The peanut-butter-covered object wasthen handed to the subject and thereby the monkeyswere reinforced with food for throwing. Thus, theacquisition of throwing by capuchin monkeys (atleast in this study) appears to be mediated by a differ-ent type of reward when compared with thechimpanzees we have described in this paper.

There are limitations to the present study that war-rant some discussion. First, it could be argued that theassociations we found between throwing and WMreflect inherent differences in cortical organizationrather than developing as a consequence of learningto throw. In other words, it may be the case that chim-panzees that learn to throw have inherently higherlevels of WM within the KNOB and IFG regionsand that this enabled them to learn to throw (ratherthan the increased WM emerging as a consequenceof their experience). Similarly, though we found anassociation between throwing ability and communi-cation skills on the PCTB tasks, it is not clearwhether increased communication abilities are a con-sequence of learning to throw or vice versa. Neitherof these alternative explanations can be ruled outbased on the findings reported here.

One approach to address this issue would be toidentify THROW2 apes that differ with respectto WM volumes or asymmetries and then train themto throw. If inherent differences in WM explain theresults reported here, then the prediction would bethat individuals with larger WM volumes wouldacquire throwing abilities much faster than individualswith smaller volumes. In terms of communication, asimilar approach could be used by performing a pre–post-test of communication abilities in two groups ofapes, where one group is taught to throw and theother group is not. If learning to throw enhances com-munication abilities, then apes taught to throw shouldperform significantly better on the communicationtasks in the post-test compared with apes that arenot taught to throw.

Second, we examined the proportion of GM andWM within gyri comprising the regions of interest inthis study (IFG and KNOB). This is a relativelycrude measure of WM organization. Ideally, studiescomparing THROWþ and THROW2 apes usingmore sensitive measures of WM connectivity, such asDTI, would be more informative of the possiblechanges in cortical connectivity between the IFG andKNOB in these cohorts of apes [58,59].

In summary, we believe that this is the first evidencelinking throwing with aspects of cortical organizationand asymmetries in non-human primates as well aswith differences in communicative abilities. The brainareas distinguishing right- and left-handed throwingchimpanzees show considerable overlap with corticalregions involved in language processing by humans.

46 W. D. Hopkins et al. Throwing in chimpanzees

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Our findings that (i) chimpanzees are predominantlyright-handed for throwing [4], and (ii) relative WMvolumes within two frontal lobe regions distinguishright- from left-handed throwers suggest that the lefthemisphere was specialized for the planning of complexmotor actions prior to the split between the lines leadingto humans and chimpanzees. Increasing selection foraimed throwing in a context of hunting or predatordefence in hominins may have refined the neural archi-tecture of the left hemisphere so as to eventually supportother complex motor sequencing actions, includinglanguage and speech.

All procedures used with the chimpanzees were approved bythe Institutional Animal Care and Use Committee of EmoryUniversity.

This research was supported in part by NIH grants NS-42867, HD-60563 and HD-56232. The Yerkes Centre isfully accredited by the American Association forAccreditation of Laboratory Animal Care. AmericanPsychological Association guidelines for the ethicaltreatment of animals were adhered to during all aspects ofthis study. We are grateful for the helpful assistance of theentire veterinary staff at the Yerkes Centre in collection ofthe MRI scans.

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