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When brains expand: mind and the evolution of cortex

Published online by Cambridge University Press:  24 June 2014

Matthew T. K. Kirkcaldie*
Affiliation:
Department of Physiology, School of Medical Sciences, The University of New South Wales, Randwick, New South Wales, Australia
Peter D. Kitchener
Affiliation:
Department of Anatomy and Cell Biology, The University of Melbourne, Melbourne Victoria, Australia
*
Dr Matthew T. K. Kirkcaldie, Department of Physiology, School of Medical Sciences, Rm 308a1, Wallace Wurth Building, The University of New South Wales, Randwick, NSW 2052, Australia. Tel: +61 2 9385 2560; Fax: +61 2 9385 1059; E-mail: m.kirkcaldie@unsw.edu.au

Abstract

Objective:

To critically examine the relationship between evolutionary and developmental influences on human neocortex and the properties of the conscious mind it creates.

Methods:

Using PubMed searches and the bibliographies of several monographs, we selected 50 key works, which offer empirical support for a novel understanding of the organization of the neocortex.

Results:

The cognitive gulf between humans and our closest primate relatives has usually been taken as evidence that our brains evolved crucial new mechanisms somehow conferring advanced capacities, particularly in association areas of the neocortex. In this overview of neocortical development and comparative brain morphometry, we propose an alternative view: that an increase in neocortical size, alone, could account for novel and powerful cognitive capabilities. Other than humans’ very large brain in relation to the body weight, the morphometric relations between neocortex and all other brain regions show remarkably consistent exponential ratios across the range of primate species, including humans. For an increase in neocortical size to produce new abilities, the developmental mechanisms of neocortex would need to be able to generate an interarchy of functionally diverse cortical domains in the absence of explicit specification, and in this respect, the mammalian neocortex is unique: its relationship to the rest of the nervous system is unusually plastic, allowing great changes in cortical organization to occur in relatively short periods of evolution. The fact that even advanced abilities like self-recognition have arisen in species from different mammalian orders suggests that expansion of the neocortex quite naturally generates new levels of cognitive sophistication. Our cognitive and behavioural sophistication may, therefore, be attributable to these intrinsic mechanisms’ ability to generate complex interarchies when the neocortex reaches a sufficient size.

Conclusion:

Our analysis offers a parsimonious explanation for key properties of the human mind based on evolutionary influences and developmental processes. This view is perhaps surprising in its simplicity, but offers a fresh perspective on the evolutionary basis of mental complexity.

Type
Review article
Copyright
Copyright © 2007 Blackwell Munksgaard

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References

Arshavsky, YI. “Scientific roots” of dualism in neuroscience. Prog Neurobiol 2006;79:190204.CrossRefGoogle ScholarPubMed
Kelly, K. Out of control: the new biology of machines. London: 4th Estate, 1994.Google Scholar
Campbell, K. Body and mind. London: Macmillan Press, 1971.Google Scholar
Miller, SM, Ngo, T. Studies of caloric vestibular stimulation: implications for the cognitive neurosciences, the clinical neurosciences and neurophilosophy. Acta Neuropsychiatr 2007;19:183203.CrossRefGoogle ScholarPubMed
Keenan, JP. The face in the mirror: the search for the origins of consciousness. New York: HarperCollins Press, 2003.Google Scholar
Plotnik, JM, De Waal, FB, Reiss, D. Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 2006;103:1705317057.CrossRefGoogle Scholar
Reiss, D, Marino, L. Mirror self-recognition in the bottlenose dolphin: a case of cognitive convergence. Proc Natl Acad Sci USA 2001;98:59375942.CrossRefGoogle ScholarPubMed
Preston, SD, De Waal, FBM. Empathy: its ultimate and proximate bases. Behav Brain Sci 2002;25:172.CrossRefGoogle ScholarPubMed
Griffin, DRAnimal minds. Chicago: University of Chicago Press, 1992.Google Scholar
Chalmers, DJ. Facing up to the problem of consciousness. J Consciousness Studies 1995;2:200219.Google Scholar
Dennett, DC. Sweet dreams: philosophical obstacles to a science of consciousness. Cambridge: MIT Press, 2005.CrossRefGoogle Scholar
Miller, SM. On the correlation/constitution distinction (and other hard problems) in the scientific study of consciousness. Acta Neuropsychiatr 2007;19:159176.CrossRefGoogle ScholarPubMed
Hubel, DH, Wiesel, TN. Brain and visual perception: the story of a 25-year collaboration. Oxford: Oxford University Press, 2004.CrossRefGoogle Scholar
Olshausen, BA, Fields, DJ. How close are we to understanding V1? Neural Comput 2005;17:16651699.CrossRefGoogle ScholarPubMed
Arciszewski, MB, Akins, K. “The Race for Consciousness” by John Taylor (book review). Trends Neurosci 2000;23:648649.CrossRefGoogle Scholar
Hodgkin, AL, Huxley, AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952;117:500544.CrossRefGoogle ScholarPubMed
Vickery, RM. Mind the neuron. Acta Neuropsychiatr 2007;19:177182.CrossRefGoogle ScholarPubMed
König, P, Engel, AK, Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci 1996;19:130137.CrossRefGoogle ScholarPubMed
Stuart, G, Spruston, N, Sakmann, B, Häusser, M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 1997;20:125131.CrossRefGoogle ScholarPubMed
Freeman, WJ. The wave packet: an action potential for the 21st century’. J Integ Neurosci 2003;2:330.CrossRefGoogle Scholar
Quiroga, QR, Reddy, L, Kreiman, G, Koch, C, Fried, I. Invariant visual representation by single neurons in the human brain. Nature 2005;435:11021107.CrossRefGoogle ScholarPubMed
Wilson, MA, McNaughton, BL. Dynamics of the hippocampal ensemble code for space. Science 1993;261:10551058.CrossRefGoogle ScholarPubMed
Rizzolatti, G, Craighero, L. The mirror-neuron system. Ann Rev Neurosci 2004;27:169192.CrossRefGoogle ScholarPubMed
Oberman, LM, Hubbard, EM, McCleery, JP, Altschuler, EL, Ramachandran, VS, Pineda, JA. EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Res Cogn Brain Res 2005;24:190198.CrossRefGoogle ScholarPubMed
Stephan, H, Frahm, H, Baron, G. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol 1981;5:129.CrossRefGoogle Scholar
Striedter, GF. Principles of brain evolution. Massachusetts: Sinauer Press, 2005.Google Scholar
Schoenemann, PT, Sheehan, MJ, Glotzer, LD. Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nature Neurosci 2005;8:242252.CrossRefGoogle ScholarPubMed
Sikela, JM. The jewels of our genome: the search for the genomic changes underlying the evolutionarily unique capacities of the human brain. PLoS Genet 2006;2:e80.CrossRefGoogle ScholarPubMed
Uddin, M, Wildman, DE, Liu, Get al. Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles. Proc Natl Acad Sci USA 2004;101:29572962.CrossRefGoogle ScholarPubMed
Nimchinsky, EA, Gilissen, E, Allman, JM, Perl, DP, Erwin, JM, Hof, PR. A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 1999;96:52685273.CrossRefGoogle ScholarPubMed
Hof, PR, Van Der Gucht, E. Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 2007;290:131.CrossRefGoogle ScholarPubMed
Ogden, JA. Visual object agnosia, prosopagnosia, achromatopsia, loss of visual imagery, and autobiographical amnesia following recovery from cortical blindness: case M.H. Neuropsychologia 1993;31:571589.CrossRefGoogle ScholarPubMed
Aboitiz, F, Montiel, J, López, J. Critical steps in the early evolution of the isocortex: insights from developmental biology. Braz J Med Biol Res 2002;35:14551472.CrossRefGoogle ScholarPubMed
Reiner, AJ. A hypothesis as to the organization of cerebral cortex in the common amniote ancestor of modern reptiles and mammals. Novartis Found Symp 2000;228:83102.CrossRefGoogle Scholar
Allman, JM. Evolving brains. New York: W. H. Freeman & Company, 1999.Google Scholar
Iwaniuk, AN, Pellis, SM, Whishaw, IQ. Is digital dexterity really related to corticospinal projections?: a re-analysis of the Heffner and Masterton data set using modern comparative statistics. Behav Brain Res 1999;101:173187.CrossRefGoogle ScholarPubMed
Rosa, MGP, Tweedale, R. Brain maps, great and small: lessons from comparative studies of primate visual cortical organization. Philos Trans R Soc Lond B Biol Sci 2005;360:665691.CrossRefGoogle ScholarPubMed
O’Leary, DD, Nakagawa, Y. Patterning centers, regulatory genes and extrinsic mechanisms controlling arealization of the neocortex. Curr Opin Neurobiol 2002;12:1425.CrossRefGoogle ScholarPubMed
Molnar, Z, Blakemore, C. How do thalamic axons find their way to the cortex? Trends Neurosci 1995;8:389397.CrossRefGoogle Scholar
Hevner, RF, Miyashita-Lin, E, Rubenstein, JL. Cortical and thalamic axon pathfinding defects in Tbr1, Gbx2, and Pax6 mutant mice: evidence that cortical and thalamic axons interact and guide each other. J Comp Neurol 2002 May;447:817.CrossRefGoogle ScholarPubMed
Leamey, CA, Kang, N, Croisier, Eet al. Ten_m3 is expressed in the developing visual pathway. Program No. 567.19. Washington D.C.: Society for Neuroscience, 2003.Google Scholar
Ince-Dunn, G, Hall, BJ, Hu, SCet al. Regulation of thalamocortical patterning and synaptic maturation by NeuroD2. Neuron 2006;49:683695.CrossRefGoogle ScholarPubMed
Sur, M, Leamey, CA. Development and plasticity of cortical areas and networks. Nat Rev Neurosci 2001;2:251262.CrossRefGoogle ScholarPubMed
Bishop, KM, Goudreau, G, O’Leary, DDM. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 2000;288:344349.CrossRefGoogle ScholarPubMed
Jacobs, GH, Williams, GA, Cahill, H, Nathans, J. Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 2007;315:17231725.CrossRefGoogle ScholarPubMed
Rakic, P. Less is more: progenitor death and cortical size. Nat Neurosci 2005;8:981982.CrossRefGoogle ScholarPubMed
Razak, KA, Shen, W, Zumsteg, T, Fuzessery, ZM. Parallel thalamocortical pathways for echolocation and passive sound localization in a gleaning bat, Antrozous pallidus. J Comp Neurol 2007;500:322338.CrossRefGoogle Scholar
Barrett, L, Henzi, P. The social nature of primate cognition. Proc Biol Sci 2005;272:18651875.Google ScholarPubMed
De Waal, FB, Dindo, M, Freeman, CA, Hall, MJ. The monkey in the mirror: hardly a stranger. Proc Natl Acad Sci USA 2005;102:1114011147.CrossRefGoogle ScholarPubMed
De Renzi, E. Disorders of visual recognition. Semin Neurol 2000;20:479485.CrossRefGoogle ScholarPubMed
Meares, R. The contribution of Hughlings Jackson to an understanding of dissociation. Am J Psychiatry 1999;156:18501855.CrossRefGoogle Scholar
Dorus, S, Vallender, EJ, Evans, PDet al. Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 2004;119:10271040.CrossRefGoogle ScholarPubMed
Fisher, SE, Lai, CSL, Monaco, AP. Deciphering the genetic basis of speech and language disorders. Ann Rev Neurosci 2003;26:5780.CrossRefGoogle ScholarPubMed
Ponting, C, Jackson, AP. Evolution of primary microcephaly genes and the enlargement of primate brains. Curr Opin Genet Dev 2005;15:241248.CrossRefGoogle ScholarPubMed
Pollard, KS, Salama, SR, Lambert, Net al. An RNA gene expressed during cortical development evolved rapidly in humans. Nature 2006;443:167172.CrossRefGoogle ScholarPubMed
Hannan, AJ. Brain phylogeny, ontogeny and dysfunction: integrating evolutionary, developmental and clinical perspectives in cognitive neuroscience. Acta Neuropsychiatr 2007;19:149158.CrossRefGoogle ScholarPubMed