Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-04T21:57:05.326Z Has data issue: false hasContentIssue false

3 - Genetic and Environmental Influences on Chimpanzee Brain and Cognition

Published online by Cambridge University Press:  28 July 2022

By
William D. Hopkins  and
Chet C. Sherwood
Edited by
Bennett L. Schwartz  and
Michael J. Beran
Bennett L. Schwartz
Affiliation:
Florida International University
Michael J. Beran
Affiliation:
Georgia State University
Get access

Summary

The seminal work on mirror self-recognition, theory of mind, and ape-language abilities beginning in the 1960s has stimulated a recent, significant body research on the cognitive abilities of animals. Because of their greater genetic, morphological, and neuroanatomical similarities with humans, research on cognition in nonhuman primates has held a particular fascination from scientific and public perspective. In this chapter, we present a summary of recent studies by our research group on the general intelligence of chimpanzees. We further present data on (1) the contribution of genetic and non-genetic factors in explaining individual variation in cognitive performance in the chimpanzees and (2) phenotypic, genetic, and environmental associations found between chimpanzee cognition and neuroanatomical organization. We end by discussing limitations in the study of cognition and emphasize the need to include individual as well as grouped data in the reporting of results. We also offer some suggestions for future research that would provide new insight into the evolution of human unique cognitive abilities.

Keywords

chimpanzeecognitionprimate cognition test batteryheritabilityneuroanatomybrain–behavior associations
Type
Chapter
Information
Primate Cognitive Studies , pp. 29 - 56
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adamson, L. R. (1996). Communication development during infancy. Westview.Google Scholar
Altarelli, I., Leroy, F., Monzalvo, K., Fluss, J., Billard, C., Dehaene-Lambertz, G., Galaburda, A. M., & Ramus, F. (2014). Planum temporale asymmetry in developmental dyslexia: Revisiting an old question. Human Brain Mapping, 35, 5717–5735.Google Scholar
Amiez, C., Sallet, J., Hopkins, W. D., Meguerditchian, A., Hadj-Bouziane, F., BenHamed, S., Wilson, C., Procyk, E., & Petrides, M. (2019). Sulcal organization in the medial frontal cortex reveals insights into primate brain evolution. Nature Communications, 10, 3437.Google Scholar
Bailey, P., von Bonin, G., & McCulloch, W. S. (1950). The isocortex of the chimpanzee. University of Illinois Press.Google Scholar
Bard, K. A. (1996). Responsive care: Behavioral intervention for nursery reared chimpanzees. Jane Goodall Institute.Google Scholar
Bard, K. A., & Hopkins, W. D. (2018). Early socioemotional intervention mediates long-term effects of atypical rearing on structural covariation in gray matter in adult chimpanzees. Psychological Science, 29, 594–603.Google Scholar
Bates, E., Camaioni, L., & Volterra, V. (1975). Performatives prior to speech. Merrill-Palmer Quarterly, 21, 205–226.Google Scholar
Bates, E., O’Connell, B., & Shore, C. (1987). Language and communication in infancy. In Osofsky, J. (Ed.), Handbook of infant development (pp. 149–203). Wiley.Google Scholar
Bennett, A. J., Pierre, P. J., Wesley, M. J., Latzman, R., Schapiro, S. J., Mareno, M. C., … & Hopkins, W. D. (2021). Predicting their past: Machine language learning can discriminate the brains of chimpanzees with different early‐life social rearing experiences. Developmental Science, 24, e13114.Google Scholar
Beran, M. J., & Heimbauer, L. A. (2015). A longitudinal assessment of vocabulary retention in symbol-competent chimpanzees (Pan troglodytes). PLoS ONE, 10, e0118408.Google Scholar
Beran, M. J., & Hopkins, W. D. (2018). Self-control in chimpanzees relates to general intelligence. Current Biology, 28, 574–579.CrossRefGoogle ScholarPubMed
Bianchi, S., Reyes, L. D., Hopkins, W. D., Taglialatela, J. P., & Sherwood, C. C. (2016). Neocortical grey matter distribution underlying voluntary, flexible vocalizations in chimpanzee. Scientific Reports, 6, 34733.Google Scholar
Bianchi, S., Stimpson, C. D., Duka, T., Larsen, M., Janssen, W. G. M., Collins, Z., Bauernfield, A. L., Schapiro, S. J., Baze, W. B., McArthur, M. J., Hopkins, W. D., Wildman, D. E., Lipovich, L., Kuzawa, C. W., Jacobs, B., Hof, P. R., & Sherwood, C. C. (2013). Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles human. Proceedings of the National Academcy of Sciences, 111, 10395–10401.Google Scholar
Brakke, K. E., & Savage-Rumbaugh, E. S. (1995). The development of language skills in bonobo and chimpanzee – I. comprehension. Language and Communication, 15, 121–148.Google Scholar
Burkhart, J. M., Schiubiger, M. N., & van Schaik, C. P. (2016). The evolution of general intelligence. Behavioral and Brain Sciences, 28, 1–65.Google Scholar
Buttelmann, D., Carpenter, M., Call, J., & Tomasello, M. (2007). Enculturated chimpanzees imitate rationally. Developmental Science, 10, 31–33.Google Scholar
Call, J., & Tomasello, M. (1994). Production and comprehension of referential pointing by orangutans (Pongo pygmaeus). Journal of Comparative Psychology, 108, 307–317.Google Scholar
Call, J., & Tomasello, M. (1996). The effect of humans on the cognitive development of apes. In Russon, A. E., Bard, K. A., & Parker, S. T. (Eds.), Reaching into thought: The minds of the great apes (pp. 371–403). Cambridge University Press.Google Scholar
Call, J., & Tomasello, M. (2008). Does the chimpanzee have a theory of mind? 30 years later. Trends in Cognitive Sciences, 12, 187–192.CrossRefGoogle ScholarPubMed
Carpenter, M., Nagell, K., Tomasello, M., Butterworth, G., & Moore, C. (1998). Social cognition, joint attention, and communicative competence from 9 to 15 months of age. Monographs of the Society for Research in Child Development, 63, i-174.Google Scholar
Carpenter, M., Tomasello, M., & Savage-Rumbaugh, E. S. (1995). Joint attention and imitative learning in children, chimpanzees and enculturated chimpanzees. Social Development, 4, 218–238.Google Scholar
Clark, H., Elsherif, M. M., & Leavens, D. A. (2019). Ontogeny vs. phylogeny in primate/canid comparisons: A meta-analysis of the object choice task. Neuroscience and Biobehavioral Reviews, 105, 178–189.Google Scholar
Connolly, C. J. (1936). The fissural pattern of the primate brain. American Journal of Physical Anthropology, 11, 31–421.Google Scholar
Darwin, C. (1859). Origin of species. Cambridge University Press.Google Scholar
Davenport, R. K., Rogers, C. M., & Rumbaugh, D. M. (1973). Long-term cognitive deficits in chimpanzees associated with early impoverished rearing. Developmental Psychology, 9, 343–347.Google Scholar
Davis, R. T., McDowell, A. A., & Nissen, H. W. (1957). Solution of bent-wire problems by monkeys and chimpanzees. Journal of Comparative and Physiological Psychology, 50, 441–444.CrossRefGoogle ScholarPubMed
Dawson, G., Munson, J., Estes, A., Osterling, J., McPartland, J., Toth, K., Carver, L., & Abbott, R. (2002). Neurocognitive function and joint attention ability in young children with autism spectrum disorder versus developmental delay. Child Development, 73, 345–358.CrossRefGoogle ScholarPubMed
French, J. A., & Carp, S. B. (2016). Early-life social adversity and developmental processes in nonhuman primates. Current Opinion in Behavioral Science, 7, 40–46.Google Scholar
Gomez-Robles, A., Hopkins, W. D., Schapiro, S. J., & Sherwood, C. C. (2015). Relaxed genetic control of cortical organization in human brains compared with chimpanzees. Proceedings of the National Academy of Sciences USA, 112, 14799–14804.Google Scholar
Greenfield, P. M., & Savage-Rumbaugh, E. S. (1991). Imitation, grammatical development and the invention of a protogrammar by an ape. In Krasnegor, N. A., Rumbaugh, D. M., Schiefelbusch, R. L., & Studdert-Kennedy, M. (Eds.), Biological and behavioral determinants of language development. Erlbaum.Google Scholar
Griffin, A. S. (2016). Innovativeness as an emergent property: A new alignment of comparative and experimental research on animal innovation. Philosophical Transactions of the Royal Society of London B Biological Sciences, 371, 20150544.Google Scholar
Griffiths, T. D., & Warren, J. D. (2002). The planum temporale as a computational hub. Trends in Neurosciences, 25, 349–355.Google Scholar
Harlow, H. F. (1949). The formation of learning sets. Psychological Review, 56, 51–65.CrossRefGoogle ScholarPubMed
Harlow, H. F., & Suomi, S. J. (1971). Social recovery by isolation-reared monkeys. Proceedings of the National Academy of Sciences of the United States of America, 68, 1534–1538.Google Scholar
Hecht, E. E., Gutman, D. A., Bradley, B. A., Preuss, T. M., & Stout, D. (2015). Virtual dissection and comparative connectivity of the superior longitudinal fasciculus in chimpanzees and humans. Neuroimage, 108, 124–137.CrossRefGoogle ScholarPubMed
Herrmann, E., Call, J., Hernandez-Lloreda, M. V., Hare, B., & Tomasello, M. (2007). Humans have evolved specialized skills of social cognition: The cultural intelligence hypothesis Science, 317, 13601366.Google Scholar
Herrmann, E., Hare, B., Call, J., & Tomasello, M. (2010). Differences in the cognitive skills of bonobos and chimpanzees. PLoS ONE, 5, e12438.Google Scholar
Herrmann, E., Hernandez-Lloreda, M. V., Call, J., Hare, B., & Tomasello, M. (2010). The structure of individual differences in the cognitive abilities of children and chimpanzees. Psychological Science, 21, 102–110.CrossRefGoogle ScholarPubMed
Herrnstein, R. J., & Murray, C. (1994). The bell curve. Free Press.Google Scholar
Hopkins, W. D., Coulon, O., Meguerditchian, A., Autrey, M. M., Davidek, K., Mahovetz, L. M., S., P., Mareno, M. C., & Schapiro, S. J. (2017). Genetic factors and oro-facial motor learning selectively influence variability in central sulcus morphology in chimpanzees (Pan troglodytes). Journal of Neuroscience, 37, 5475–5483.Google Scholar
Hopkins, W. D., Keebaugh, A. C., Reamer, L. A., Schaeffer, J., Schapiro, S. J., & Young, L. J. (2014). Genetic influences on receptive joint attention in chimpanzees (Pan troglodytes). Scientific Reports 4, 1–7.Google Scholar
Hopkins, W. D., Latzman, R. D., Mareno, M. C., Schapiro, S. J., Gomez-Robles, A., & Sherwood, C. C. (2018). Heritability of gray matter structural covariation and tool use skills in chimpanzees (Pan troglodytes): A source-based morphometry and quantitative genetic analysis. Cerebral Cortex, 29, 3702–3711.CrossRefGoogle Scholar
Hopkins, W. D., Li, X., & Roberts, N. (2019). More intelligent chimpanzees (Pan troglodytes) have larger brains and increased cortical thickness. Intelligence, 74, 18–24.Google Scholar
Hopkins, W. D., Misiura, M., Pope, S. M., & Latash, E. M. (2015). Behavioral and brain asymmetries in primates: A preliminary evaluation of two evolutionary hypotheses. Yearbook of Cognitive Neuroscience, 1359, 65–83.Google Scholar
Hopkins, W. D., Misiura, M., Reamer, L. A., Schaeffer, J. A., Mareno, M. C., & Schapiro, S. J. (2014). Poor receptive joint attention skills are associated with atypical grey matter asymmetry in the posterior superior temporal gyrus of chimpanzees (Pan troglodytes). Frontiers in Cognition, 5, 7.Google Scholar
Hopkins, W. D., Procyk, E., Petrides, M., Schapiro, S. J., Mareno, M. C., & Amiez, C. (2021). Sulcal morphology in cingulate cortex is associated with voluntary oro-facial motor control and gestural communication in chimpanzees (Pan troglodytes). Cerebral Cortex, 31, 2845–2854.Google Scholar
Hopkins, W. D., Russell, J. L., & Schaeffer, J. (2014). Chimpanzee intelligence is heritable. Current Biology, 24, 1649–1652.Google Scholar
Hopkins, W. D., Taglialatela, J. P., & Leavens, D. A. (2007). Chimpanzees differentially produce novel vocalizations to capture the attention of a human. Animal Behaviour, 73, 281–286.Google Scholar
Hopkins, W. D., Taglialatela, J. P., & Leavens, D. A. (2011). Do chimpanzees have voluntary control of their facial expressions and vocalizations? In Vilain, A., Schwartz, J.-L., Abry, C., & Vauclair, J. (Eds.), Primate communication and human language: Vocalisation, gestures, imitation and deixis in humans and non-humans (pp. 71–90). John Benjamins Publishing Company.Google Scholar
Hostetter, A. B., Cantero, M., & Hopkins, W. D. (2001). Differential use of vocal and gestural communication by chimpanzees (Pan troglodytes) in response to the attentional status of a human (Homo sapiens). Journal of Comparative Psychology, 115, 337–343.Google Scholar
Hostetter, A. B., Russell, J. L., Freeman, H., & Hopkins, W. D. (2007). Now you see me, now you don’t: Evidence that chimpanzees understand the role of the eyes in attention. Animal Cognition, 10, 55–62.CrossRefGoogle Scholar
Ibanez, L. V., Grantz, C. J., & Messinger, D. S. (2012). The develoment of referential communication and autism symptomology in high-risk infants. Infancy, 17, 1–21.Google Scholar
Joly, M., Micheletta, J., De Marco, A., Langermans, J. A., Sterck, E. H., & Waller, B. M. (2017). Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance. Proceedings of the Royal Society B: Biological Sciences, 284, 20162738.CrossRefGoogle ScholarPubMed
Jones, J. H. (2011). Primates and the evolution of long, slow life histories. Current Biology, 21, R708–717.Google Scholar
Josse, G., Mazoyer, B., Crivello, F., & Tzourio-Mazoyer, N. (2003). Left planum temporale: An anatomical marker of left hemispheric specialization for language comprehension. Cognitive Brain Research, 18, 1–14.Google Scholar
Keller, S. S., Deppe, M., Herbin, M., & Gilissen, E. (2012). Variabilty and asymmetry of the sulcal contours defining Broca’s area homologue in the chimpanzee brain. Journal of Comparative Neurology, 520, 1165–1180.Google Scholar
Kohler, W. (1925). The mentality of apes. Harcourt, Brace & World.Google Scholar
Krupenye, C., & Hare, B. (2018). Bonobos prefer individuals that hinder others over those that help. Current Biology, 28, 280–286.Google Scholar
Krupenye, C., Rosati, A. G., & Hare, B. (2015). Bonobos and chimpanzees exhibit human-like framing effects. Biology Letters, 11, 20140527.Google Scholar
Landa, R. J., Holman, K. C., & Garrett-Mayer, E. (2007). Social and communicative development in toddlers with early and later diagnosis of autism spectrum disorders. Archives of General Psychiatry, 64, 853–864.Google Scholar
Leavens, D. A., Hostetter, A. B., Wesley, M. J., & Hopkins, W. D. (2004). Tactical use of unimodal and bimodal communication by chimpanzees, Pan troglodytes. Animal Behaviour, 67, 467–476.Google Scholar
Leavens, D. A., Reamer, L. A., Mareno, M. C., Russell, J. L., Wilson, D. C., Schapiro, S. J., & Hopkins, W. D. (2015). Distal communication by chimpanzees (Pan troglodytes): Evidence for common ground? Child Development, 86, 1623–1638.Google Scholar
Leavens, D. A., Russell, J. L., & Hopkins, W. D. (2010). Multi-modal communication and its social contextual use in captive chimpanzees (Pan troglodytes). Animal Cognition, 13, 33–40.Google Scholar
Leigh, S. R. (2004). Brain growth, life history, and cognition in primate and human evolution. American Journal of Primatology, 62, 139–164.CrossRefGoogle ScholarPubMed
Liebal, K., Pika, S., Call, J., & Tomasello, M. (2004). To move or not to move: How apes adjust to the attentional state of others. Interaction Studies, 5, 199–219.Google Scholar
Loh, K. K., Petrides, M., Hopkins, W. D., Procyk, E., & Amiez, C. (2017). Cognitive control of vocalizations in the primate ventrolateral–dorsomedial frontal (VLF–DMF) brain network. Neuroscience and Biobehavioral Reviews, 82, 32–44.Google Scholar
Loh, K. K., Procyk, E., Neveu, R., Lamberton, F., Hopkins, W. D., Petrides, M., & Amiez, C. (2020). Cognitive control of orofacial motor and vocal responses in the ventrolateral and dorsomedial human frontal cortex. Proceedings of the National Academy of Sciences USA, 117, 4994–5005.Google Scholar
Lyn, H., Russell, J. L., & Hopkins, W. D. (2010). The impact of environment on the comprehension of declarative communication in apes. Psychological Science, 21, 360–365.CrossRefGoogle ScholarPubMed
McDaniel, M. A. (2005). Big-brained peple are smarter: A meta-analysis of the relationship between in vivo brain volume and intelligence. Intelligence, 33, 337–346.Google Scholar
Miller, E. N., Hof, P. R., Sherwood, C. C., & Hopkins, W. D. (2021). The paracingulate sulcus is a unique feature of the medial frontal cortex shared by great apes and humans. Brain, Behavior and Evolution, 96, 26–36.Google Scholar
Miller, J. A., Voorhies, W. I., Li, X., Raghuram, I., Palomero-Gallagher, N., Zilles, K., Sherwood, C. C., Hopkins, W. D., & Weiner, K. S. (2020). Sulcal morphology of ventral temporal cortex is shared between humans and other hominoids. Scientific Reports, 10, 17132.Google Scholar
Mulholland, M. M., Sherwood, C. C., Schapiro, S. J., Raghanti, M. A., & Hopkins, W. D. (2021). Age‐ and cognition‐related differences in the gray matter volume of the chimpanzee brain (Pan troglodytes): A voxel‐based morphometry and conjunction analysis. American Journal of Primatology, e23264.Google Scholar
Mundy, P. (2018). A review of joint attention and social-cognitive brain systems in typical development and autism spectrum disorder. European Journal of Neuroscience, 47, 497–514.Google Scholar
Mundy, P., Block, J., Delgado, C., Pomares, Y., Van Hecke, A. V., & Parlade, M. V. (2007). Individual differences and the development of joint attention in infancy. Child Development, 78, 938–954.Google Scholar
Mundy, P., & Newell, L. (2007). Attention, joint attention, and social cognition. Current Directions in Psychological Science, 16, 269–274.Google Scholar
Nichols, K. E., Fox, N. A., & Mundy, P. (2005). Joint attention, self-recognition and neurocognitive function in toddlers. Infancy, 7, 35–51.Google Scholar
Novak, M. A., & Harlow, H. F. (1975). Social recovery of monkeys isolated for the first year of life: I. Rehabilitation and therapy. Developmental Psychology, 11, 453–465.Google Scholar
Novak, M. A., Meyer, J. S., Lutz, C., & Tiefenbacher, S. (2006). Deprived environments: Developmental insights from primatology. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, 2, 153–189.Google Scholar
Paus, T., Tomaiuolo, F., Otaky, N., MacDonald, D., Petrides, M., Atllas, J., Morris, R., & Evans, A. C. (1996). Human cingulate and paracingulate sulci: Pattern, variability, asymmetry and probabilistic map. Cerebral Cortex, 6, 207–214.Google Scholar
Poss, S. R., Kuhar, C., Stoinski, T. S., & Hopkins, W. D. (2006). Differential use of attentional and visual communicative signaling by orangutans (Pongo pygmaeus) and gorillas (Gorilla gorilla) in response to the attentional status of a human. American Journal of Primatology, 68, 978–992.CrossRefGoogle Scholar
Premack, D. (1976). Intelligence in ape and man. Lawrence Erlbaum and Associates.Google Scholar
Premack, D., & Woodruff, G. (1978). Does the chimpanzee have a theory of mind? Behavioral and Brain Sciences, 1, 515–526.Google Scholar
Presmanes, A. G., Walden, T. A., Stone, W. L., & Yoder, P. J. (2007). Effects of different attentional cues on responding to joint attention in younger siblings of children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37, 133–144.Google Scholar
Reader, S. M., Hager, Y., & Laland, K. N. (2011). The evolution of primate general and cultural intelligence. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 1017–1027.Google Scholar
Reader, S. M., & Laland, K. N. (2002). Social intelligence, innnovation, and enhanced brain size in primates. Proceedings of the National Academy of Sciences, 99, 4436–4441.Google Scholar
Romanes, G. (1892). Animal intelligence. D. Appleton and Company.Google Scholar
Roth, G., & Dicke, U. (2005). Evolution of brain and intelligence. Trends in Cognitive Science, 9, 250–257.Google Scholar
Rumbaugh, D. M. (1977). Language learning by a chimpanzee: The Lana project. Academic Press.Google Scholar
Rumbaugh, D. M., & Pate, J. L. (1984). The evolution of cognition in primates: A comparative perspective. In Roitblat, H. L., Bever, T. G., & Terrace, H. S. (Eds.), Animal cognition (pp. 569–585). Lawrence Erlbaum and Associates.Google Scholar
Russell, J. L., Lyn, H., Schaeffer, J. A., & Hopkins, W. D. (2011). The role of socio‐communicative rearing environments in the development of social and physical cognition in apes. Developmental Science, 14(6), 1459–1470.Google Scholar
Sackett, G. P., Ruppenthal, G. C., & Elias, K. (Eds.). (2006). Nursery rearing of nonhuman primates in the 21st century (Vol. 8). Univerity of Chicago Press.Google Scholar
Savage-Rumbaugh, E. S. (1986). Ape language: From conditioned response to symbol. Columbia University Press.Google Scholar
Savage-Rumbaugh, E. S., Murphy, J., Sevcik, R. A., Brakke, K. E., Williams, S. L., & Rumbaugh, D. M. (1993). Language comprehension in ape and child. Monographs of the Society for Research in Child Development, 58, 1–256.Google Scholar
Savage-Rumbaugh, E. S., Rumbaugh, D. M., & Boysen, S. (1978). Symbolic communication between two chimpanzees (Pan troglodytes). Science, 201, 641–644.Google Scholar
Sclafani, V., Paukner, A., Suomi, S. J., & Ferrari, P. F. (2015). Imitation promotes affiliation in infant macaques at risk for impaired social behaviors. Developmental Science, 18, 614–621.CrossRefGoogle ScholarPubMed
Segerdahl, P., Fields, W., & Savage-Rumbaugh, S. (2006). Kanzi’s primal language: The cultural initiation of primates into language. Palgrave Macmillan.Google Scholar
Shapleske, J., Rossell, S. L., Woodruff, P. W., & David, A. S. (1999). The planum temporale: A systematic, quantitative review of its structural, functional and clinical significance. Brain Research Reviews, 29, 26–49.Google Scholar
Sherwood, C. C., Broadfield, D. C., Holloway, R. L., Gannon, P. J., & Hof, P. R. (2003). Variability of Broca’s area homologue in great apes: Implication for language evolution. The Anatomical Record, 217A, 276–285.Google Scholar
Simpson, E. A., Sclafani, V., Paukner, A., Kaburu, S. S. K., Suomi, S. J., & Ferrari, P. F. (2019). Handling newborn monkeys alters later exploratory, cognitive, and social behaviors. Devolopmental Cognitive Neuroscience, 35, 12–19.Google Scholar
Skinner, B. F. (1974). About behaviorism. Random House.Google Scholar
Smedley, A., & Smedley, B. D. (2005). Race as biology is fiction, racism as a social problem is real: Anthropological and historical perspectives on the social construction of race. American Psychologist, 60, 16–26.CrossRefGoogle ScholarPubMed
Spocter, M. A., Hopkins, W. D., Barks, S. K., Bianchi, S., Hehmeyer, A. E., Anderson, S. M., Stimpson, C. D., Fobbs, A. J., Hof, P. R., & Sherwood, C. C. (2012). Neuropil distribution in the cerebral cortex differs between humans and chimpanzees. The Journal of Comparative Neurology, 520, 2917–2929.Google Scholar
Taglialatela, J. P., Dadda, M., & Hopkins, W. D. (2007). Sex differences in asymmetry of the planum parietale in chimpanzees (Pan troglodytes). Behavioural Brain Research, 184, 185–191.Google Scholar
Taglialatela, J. P., Reamer, L., Schapiro, S. J., & Hopkins, W. D. (2012). Social learning of a communicative signal in captive chimpanzees. Biology Letters, 8, 498–501.Google Scholar
Taglialatela, J. P., Russell, J. L., Schaeffer, J. A., & Hopkins, W. D. (2008). Communicative signaling activates “Broca’s” homologue in chimpanzees. Current Biology, 18, 343–348.Google Scholar
Theall, L. A., & Povinelli, D. J. (1999). Do chimpanzees tailor their gestural signals to fit the attentional state of others? Animal Cognition, 2, 207–214.Google Scholar
Thompson, M. A., Bloomsmith, M. A., & Taylor, L. L. (1991). A canine companion for nursery-reared infant chimpanzee. Laboratory Primate Newsletter, 30, 1–4.Google Scholar
Tolman, E. C. (1924). The inheritance of maze-learning ability in rats. Journal of Comparative Psychology, 4, 1–18.Google Scholar
Tomasello, M. (1995). Joint attention as social cognition. In Moore, C. & Dunham, P. J. (Eds.), Joint attention: Its origins and role in development (pp. 103–130). Erlbaum.Google Scholar
Turner, C. H., Davenport, R. K., & Rogers, C. M. (1969). The effects of early deprivation on the social behavior of adolescent chimpanzees American Journal of Psychiatry, 125, 1531–1536.Google Scholar
Watson, J. B. (1913). Psychology as the behaviorist views it. Psychological Review, 20, 158–177.Google Scholar
Whalen, C., Schreibman, L., & Ingersoll, B. (2006). The collateral effect of joint attention training on social initiations, positive affect, imitation, and spontaneous speech in young children with autism. Journal of Autism and Developmental Disorders, 36, 655–664.Google Scholar
Woodley, M. A., Fernandes, H. B. F., & Hopkins, W. D. (2015). The more g-loaded, the more heritable, evolvable, and phenotypically variable: Homology with humans in chimpanzee cognitive abilities. Intelligence, 50, 159–163.Google Scholar
Yerkes, R. M. (1943). Chimpanzees: A laboratory colony. Yale University Press.Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×