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Brain Evolution and Human Neuropsychology: The Inferential Brain Hypothesis

Published online by Cambridge University Press:  30 March 2012

Timothy R. Koscik  and
Daniel Tranel
Timothy R. Koscik*
Affiliation:
Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa Department of Psychology, University of Toronto, Toronto, Ontario
Daniel Tranel
Affiliation:
Department of Neurology, Division of Behavioral Neurology and Cognitive Neuroscience, University of Iowa College of Medicine, Iowa City, Iowa Department of Psychology, University of Iowa, Iowa City, Iowa
*
Correspondence and reprint requests to: Timothy R. Koscik, Department of Psychology, University of Toronto, 100 St. George Street, Toronto, Ontario, M5S 3G3. E-mail: [email protected]
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Abstract

Collaboration between human neuropsychology and comparative neuroscience has generated invaluable contributions to our understanding of human brain evolution and function. Further cross-talk between these disciplines has the potential to continue to revolutionize these fields. Modern neuroimaging methods could be applied in a comparative context, yielding exciting new data with the potential of providing insight into brain evolution. Conversely, incorporating an evolutionary base into the theoretical perspectives from which we approach human neuropsychology could lead to novel hypotheses and testable predictions. In the spirit of these objectives, we present here a new theoretical proposal, the Inferential Brain Hypothesis, whereby the human brain is thought to be characterized by a shift from perceptual processing to inferential computation, particularly within the social realm. This shift is believed to be a driving force for the evolution of the large human cortex. (JINS, 2012, 18, 394–401)

Keywords

Brain evolutionNeuropsychologyInferenceOlfactionComparative neuroanatomyPrimates
Type
Short Review
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 3 , May 2012 , pp. 394 - 401
Copyright
Copyright © The International Neuropsychological Society 2012

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References

Adolphs, R. (1999). Social cognition and the human brain. Trends in Cognitive Sciences, 3(12), 469–479.CrossRefGoogle ScholarPubMed
Adolphs, R. (2003). Cognitive neuroscience of human social behaviour. Nature Reviews Neuroscience, 4(3), 165–178.CrossRefGoogle ScholarPubMed
Anderson, A.K., Christoff, K., Stappen, I., Panitz, D., Ghahremani, D.G., Glover, G., Sobel, N. (2003). Dissociated neural representations of intensity and valence in human olfaction. Nature Neuroscience, 6(2), 196–202.CrossRefGoogle ScholarPubMed
Anderson, S.W., Bechara, A., Damasio, H., Tranel, D., Damasio, A.R. (1999). Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nature Neuroscience, 2(11), 1032–1037.CrossRefGoogle ScholarPubMed
Baron, G., Frahm, H.D., Bhatnagar, K.P., Stephan, H. (1983). Comparison of brain structure volumes in Insectivora and Primates. III. Main olfactory bulb (MOB). Journal für Hirnforschung, 24(5), 551–568.Google ScholarPubMed
Baron, G., Stephan, H., Frahm, H.D. (1987). Comparison of brain structure volumes in Insectivora and primates. VI. Paleocortical components. Journal für Hirnforschung, 28(4), 463–477.Google ScholarPubMed
Barton, R.A. (1998). Visual specialization and brain evolution in primates. Proceedings of the Royal Society B: Biological Sciences, 265(1409), 1933–1937. doi:10.1098/rspb.1998.0523CrossRefGoogle ScholarPubMed
Barton, R.A. (2006). Olfactory evolution and behavioral ecology in primates. American Journal of Primatology, 68(6), 545–558.CrossRefGoogle ScholarPubMed
Bhatnagar, K.P., Kallen, F.C. (1974). Cribriform plate of ethmoid, olfactory bulb and olfactory acuity in forty species of bats. Journal of Morphology, 142(1), 71–89.CrossRefGoogle ScholarPubMed
Bilder, R.M. (2011). Neuropsychology 3.0: Evidence-based science and practice. Journal of the International Neuropsychological Society, 17(01), 7–13.CrossRefGoogle ScholarPubMed
Bond, A.B., Kamil, A.C., Balda, R.P. (2003). Social complexity and transitive inference in corvids. Animal Behaviour, 65(3), 479–487.CrossRefGoogle Scholar
Brennan, P.A., Keverne, E.B. (2004). Something in the air? New insights into mammalian pheromones. Current Biology, 14(2), R81–R89.CrossRefGoogle ScholarPubMed
Buschhuter, D., Smitka, M., Puschmann, S., Gerber, J.C., Witt, M., Abolmaali, N.D., Hummel, T. (2008). Correlation between olfactory bulb volume and olfactory function. Neuroimage, 42(2), 498–502.CrossRefGoogle ScholarPubMed
Byrne, R.W. (1996). Machiavellian intelligence. Evolutionary Anthropology, 5(5), 172–180.3.0.CO;2-H>CrossRefGoogle Scholar
Courchesne, E., Carper, R., Akshoomoff, N. (2003). Evidence of brain overgrowth in the first year of life in autism. JAMA, 290(3), 337–340. doi:10.1001/jama.290.3.337CrossRefGoogle ScholarPubMed
Damasio, A.R. (1994). Descartes’ error: Emotion, reason, and the human brain. New York: Putnam.Google Scholar
Damasio, A.R., Tranel, D., Damasio, H. (1990). Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social-stimuli. Behavioural Brain Research, 41(2), 81–94.CrossRefGoogle ScholarPubMed
Damasio, H., Damasio, A.R. (1980). The anatomical basis of conduction aphasia. Brain, 103(2), 337–350.CrossRefGoogle ScholarPubMed
Davis, H. (1992). Transitive inference in rats. (Rattus norvegicus) Journal of Comparative Psychology, 106(4), 342–349. doi:10.1037/0735-7036.106.4.342CrossRefGoogle ScholarPubMed
DeVito, L.M., Kanter, B.R., Eichenbaum, H. (2010). The hippocampus contributes to memory expression during transitive inference in mice. Hippocampus, 20(1), 208–217.CrossRefGoogle ScholarPubMed
Dunbar, R.I.M. (1998). The social brain hypothesis. Evolutionary Anthropology, 6(5), 178–190.3.0.CO;2-8>CrossRefGoogle Scholar
Frahm, H.D., Stephan, H., Stephan, M. (1982). Comparison of brain structure volumes in Insectivora and Primates. I. Neocortex. Journal für Hirnforschung, 23(4), 375–389.Google ScholarPubMed
Gilad, Y., Wiebe, V., Przeworski, M., Lancet, D., Pääbo, S. (2004). Loss of olfactory receptor genes coincides with the acquisition of full trichromatic vision in primates. PLoS Biol, 2(1), e5.CrossRefGoogle ScholarPubMed
Gillan, D.J. (1981). Reasoning in the chimpanzee: II. Transitive inference. Journal of Experimental Psychology: Animal Behavior Processes, 7(2), 150–164.Google Scholar
Gittleman, J.L. (1991). Carnivore olfactory bulb size: Allometry, phylogeny and ecology. Journal of Zoology, 225(2), 253–272.CrossRefGoogle Scholar
Gottfried, J.A., Zald, D.H. (2005). On the scent of human olfactory orbitofrontal cortex: Meta-analysis and comparison to non-human primates. Brain Research Reviews, 50(2), 287–304.CrossRefGoogle ScholarPubMed
Grosenick, L., Clement, T.S., Fernald, R.D. (2007). Fish can infer social rank by observation alone. Nature, 445(7126), 429–432.CrossRefGoogle ScholarPubMed
Halpern, M., Martinez-Marcos, A. (2003). Structure and function of the vomeronasal system: An update. Progress in Neurobiology, 70(3), 245–318.CrossRefGoogle ScholarPubMed
Harvey, P.H., Clutton-Brock, T.H. (1985). Life history variation in primates. Evolution, 39(3), 559–581.CrossRefGoogle ScholarPubMed
Haselton, M.G., Gildersleeve, K. (2011). Can men detect ovulation? Current Directions in Psychological Science, 20(2), 87–92. doi:10.1177/0963721411402668CrossRefGoogle Scholar
Jernigan, T.L., Trauner, D.A., Hesselink, J.R., Tallal, P.A. (1991). Maturation of human cerebrum observed in vivo during adolescence. Brain, 114(5), 2037–2049. doi:10.1093/brain/114.5.2037CrossRefGoogle ScholarPubMed
Kennedy, D.P., Gläscher, J., Tyszka, J.M., Adolphs, R. (2009). Personal space regulation by the human amygdala. Nature Neuroscience, 12(10), 1226–1227.CrossRefGoogle ScholarPubMed
Kiviniemi, V.J., Haanpää, H., Kantola, J.-H., Jauhiainen, J., Vainionpää, V., Alahuhta, S., Tervonen, O. (2005). Midazolam sedation increases fluctuation and synchrony of the resting brain BOLD signal. Magnetic Resonance Imaging, 23(4), 531–537. doi:10.1016/j.mri.2005.02.009CrossRefGoogle ScholarPubMed
Koenigs, M., Young, L., Adolphs, R., Tranel, D., Cushman, F., Hauser, M., Damasio, A. (2007). Damage to the prefrontal cortex increases utilitarian moral judgements. Nature, 446(7138), 908–911. doi:10.1038/nature05631CrossRefGoogle Scholar
Koscik, T.R., Tranel, D. (2011). The human amygdala is necessary for developing and expressing normal interpersonal trust. Neuropsychologia, 49(4), 602–611.CrossRefGoogle ScholarPubMed
Kuze, N., Malim, T.P., Kohshima, S. (2005). Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): Possible signals in visual communication. American Journal of Primatology, 65(4), 353–376.CrossRefGoogle ScholarPubMed
Lévy, F., Locatelli, A., Piketty, V., Tillet, Y., Poindron, P. (1995). Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiology & Behavior, 57(1), 97–104. doi:10.1016/0031-9384(94)00200-oCrossRefGoogle Scholar
Levy, R., Goldman-Rakic, P.S. (2000). Segregation of working memory functions within the dorsolateral prefrontal cortex. Experimental Brain Research, 133(1), 23–32.CrossRefGoogle ScholarPubMed
Liman, E.R., Innan, H. (2003). Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proceedings of the National Academy of Sciences of the United States of America, 100(6), 3328–3332.CrossRefGoogle Scholar
Luders, E., Steinmetz, H., Jäncke, L. (2002). Brain size and grey matter in the healthy human brain. Neuroreport, 13(17), 2371–2374.CrossRefGoogle ScholarPubMed
MacLean, E.L., Merritt, D.J., Brannon, E.M. (2008). Social complexity predicts transitive reasoning in prosimian primates. Animal Behaviour, 76(2), 479–486.CrossRefGoogle ScholarPubMed
Margulies, D.S., Vincent, J.L., Kelly, C., Lohmann, G., Uddin, L.Q., Biswal, B.B., Petrides, M. (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proceedings of the National Academy of Sciences of the United States of America, 106(47), 20069–20074.CrossRefGoogle ScholarPubMed
Marsh, H.L., MacDonald, S.E. (2011). Information seeking by orangutans: A generalized search strategy? Animal Cognition, [Epub ahead of print].Google ScholarPubMed
Martuzzi, R., Ramani, R., Qiu, M., Rajeevan, N., Constable, R.T. (2010). Functional connectivity and alterations in baseline brain state in humans. Neuroimage, 49(1), 823–834.CrossRefGoogle ScholarPubMed
Matochik, J.A. (1988). Role of the main olfactory system in recognition between individual spiny mice. Physiology & Behavior, 42(3), 217–222.CrossRefGoogle ScholarPubMed
Mishkin, M., Ungerleider, L.G., Macko, K.A. (1983). Object vision and spatial vision: Two cortical pathways. Trends in Neurosciences, 6(0), 414–417. doi:10.1016/0166-2236(83)90190-xCrossRefGoogle Scholar
Peltier, S.J., Kerssens, C., Hamann, S.B., Sebel, P.S., Byas-Smith, M., Hu, X. (2005). Functional connectivity changes with concentration of sevoflurane anesthesia. Neuroreport, 16(3), 285–288.CrossRefGoogle ScholarPubMed
Preuss, T.M. (2007). Primate brain evolution in phylogenetic context. In J. Kaas (Ed.), Evolution of nervous systems: A comprehensive review (Vol. 4). New York: Elsevier.Google Scholar
Preuss, T.M. (2010). Reinventing primate neuroscience for the twenty-first century. Primate Neuroethology, 1(9), 422–454.CrossRefGoogle Scholar
Preuss, T.M. (2011). The human brain: Rewired and running hot. Annals of the New York Academy of Sciences, 1225, E182–E191.CrossRefGoogle ScholarPubMed
Rilling, J.K., Glasser, M.F., Preuss, T.M., Ma, X., Zhao, T., Hu, X., Behrens, T.E.J. (2008). The evolution of the arcuate fasciculus revealed with comparative DTI. Nature Neuroscience, 11(4), 426–428.CrossRefGoogle ScholarPubMed
Rizzolatti, G., Arbib, M.A. (1998). Language within our grasp. Trends in Neurosciences, 21(5), 188–194. doi:10.1016/s0166-2236(98)01260-0CrossRefGoogle ScholarPubMed
Rizzolatti, G., Luppino, G., Matelli, M. (1998). The organization of the cortical motor system: New concepts. Electroencephalography and Clinical Neurophysiology, 106, 283–296.CrossRefGoogle ScholarPubMed
Sanchez-Andrade, G., Kendrick, K.M. (2009). The main olfactory system and social learning in mammals. Behavioural Brain Research, 200(2), 323–335. doi:10.1016/j.bbr.2008.12.021CrossRefGoogle ScholarPubMed
Semendeferi, K., Damasio, H., Frank, R., Van Hoesen, G.W. (1997). The evolution of the frontal lobes: A volumetric analysis based on three-dimensional reconstructions of magnetic resonance scans of human and ape brains. Journal of Human Evolution, 32(4), 375–388.CrossRefGoogle ScholarPubMed
Sherry, D.F., Jacobs, L.F., Gaulin, S.J.C. (1992). Spatial memory and adaptive specialization of the hippocampus. Trends in Neurosciences, 15(8), 298–303.CrossRefGoogle ScholarPubMed
Squire, L.R., Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science, 253(5026), 1380–1386. doi:10.1126/science.1896849CrossRefGoogle ScholarPubMed
Stephan, H., Frahm, H., Baron, G. (1981). New and revised data on volumes of brain structures in insectivores and primates. Folia Primatologica, 35(1), 1–29.CrossRefGoogle ScholarPubMed
Stephan, H., Frahm, H.D., Baron, G. (1987). Comparison of brain structure volumes in Insectivora and primates. VII. Amygdaloid components. Journal für Hirnforschung, 28(5), 571–584.Google ScholarPubMed
Subiaul, F., Barth, J., Okamoto-Barth, S., Povinelli, D.J. (2007). Human cognitive specializations. In: J. Kaas (Ed.), Evolution of nervous systems: A comprehensive review (Vol. 4). New York: Elsevier.Google Scholar
Treichler, F.R., Van Tilburg, D. (1996). Concurrent conditional discrimination tests of transitive inference by macaque monkeys: List linking. Journal of Experimental Psychology: Animal Behavior Processes, 22(1), 105–117.Google ScholarPubMed
Vincent, J.L., Patel, G.H., Fox, M.D., Snyder, A.Z., Baker, J.T., Van Essen, D.C., Raichle, M.E. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447(7140), 83–86.CrossRefGoogle ScholarPubMed
von Fersen, L., Wynne, C.D., Delius, J.D., Staddon, J.E. (1991). Transitive inference formation in pigeons. Journal of Experimental Psychology: Animal Behavior Processes, 17(3), 334–341.Google Scholar
Weiss, B.M., Kehmeier, S., Schloegl, C. (2010). Transitive inference in free-living greylag geese, Anser anser. Animal Behaviour, 79(6), 1277–1283.CrossRefGoogle Scholar
Young, L., Bechara, A., Tranel, D., Damasio, H., Hauser, M., Damasio, A. (2010). Damage to ventromedial prefrontal cortex impairs judgment of harmful intent. Neuron, 65(6), 845–851.CrossRefGoogle ScholarPubMed
Zhang, J., Webb, D.M. (2003). Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proceedings of the National Academy of Sciences of the United States of America, 100(14), 8337–8341.CrossRefGoogle ScholarPubMed