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Brain phylogeny, ontogeny and dysfunction: integrating evolutionary, developmental and clinical perspectives in cognitive neuroscience

Published online by Cambridge University Press:  24 June 2014

Anthony J. Hannan
Anthony J. Hannan*
Affiliation:
Howard Florey Institute, University of Melbourne, Parkville, Victoria, Australia
*
Dr Anthony J. Hannan, Howard Florey Institute, University of Melbourne, Parkville, VIC 3010, Australia. Tel: +61 3 8344 7316; Fax: +61 3 9348 1707; E-mail: [email protected]
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Abstract

Objective:

One of the most popular approaches in cognitive neuroscience has been to study the normal adult human brain. However, there are likely to be limits to the knowledge that can be obtained from such studies. If we assume that no single approach can ever provide us with knowledge of causative processes whereby the mind emerges from the brain, then we need to consider how to combine more disparate approaches. I aim to illustrate here how the parallel study of brain phylogeny, ontogeny and dysfunction may bring us towards an integrative understanding of fundamental aspects of cognitive neuroscience.

Methods:

A review of published literature in these research areas was carried out and representative articles selected.

Results:

Comparative approaches, utilizing the extraordinary behavioural abilities as well as the structural and functional variants that evolution has thrown up across diverse groups of species, can inform the core neural systems that may be necessary and sufficient to support specific cognitive processes. Similarly, detailed studies of human brain development, focusing on structural and functional maturation correlated with temporal mapping of cognitive processes as they come ‘on-line’, may provide unique mechanistic insights. Finally, the study of brain dysfunction in neurological and psychiatric disorders such as Huntington’s disease, Alzheimer’s disease, schizophrenia and depression, may have the beneficial side-effect of greatly enhancing our understanding of healthy brain function.

Conclusion:

Each approach has its own epistemological advantages and disadvantages, but combined they may lead to more sophisticated, and empirically testable, models. In this review, I outline evidence for their utility, illustrate the approaches using specific examples and suggest how new advances in fields such as genomics, neurophysiology and neuroimaging may provide unprecedented opportunities in cognitive neuroscience.

Keywords

Alzheimer’s diseasedepressionschizophreniacognitionmemoryperceptionHuntington’s disease
Type
Review article
Information
Acta Neuropsychiatrica , Volume 19 , Issue 3 , June 2007 , pp. 149 - 158
Copyright
Copyright © 2007 Blackwell Munksgaard

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References

Gazzaniga, MS. (ed.) The cognitive neurosciences III. Cambridge, MA: MIT Press, 2004.Google Scholar
Chalmers, DJ. The conscious mind: in search of a fundamental theory. New York: Oxford University Press, 1996.Google Scholar
Vidyasagar, TR. A neuronal model of attentional spotlight: parietal guiding the temporal. Brain Res Brain Res Rev 1999;30:66–76.CrossRefGoogle ScholarPubMed
Crick, F, Koch, C. A framework for consciousness. Nat Neurosci 2003;6:119–126.CrossRefGoogle ScholarPubMed
Miller, SM. On the correlation/constitution distinction problem (and other hard problems) in the scientific study of consciousness. Acta Neuropsychiatr 2007;19:159–176.CrossRefGoogle Scholar
Logothetis, NK, Pauls, J, Augath, M, Trinath, T, Oeltermann, A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001;412:150–157.CrossRefGoogle ScholarPubMed
Logothetis, NK. The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 2002;357:1003–1037.CrossRefGoogle ScholarPubMed
Kirkcaldie, MTK, Kitchener, PD. When brains expand: mind and the evolution of cortex. Acta Neuropsychiatr 2007;19:139–148.CrossRefGoogle ScholarPubMed
Darwin, C. The descent of man, and selection in relation to sex. London: Murray, 1871.Google Scholar
Eccles, JC. Evolution of the brain: creation of the self. London: Routledge, 1989.Google Scholar
Duchaine, B, Cosmides, L, Tooby, J. Evolutionary psychology and the brain. Curr Opin Neurobiol 2001;11:225–230.CrossRefGoogle Scholar
Creely, H, Khaitovich, P. Human brain evolution. Prog Brain Res 2006;158:295–309.CrossRefGoogle ScholarPubMed
Iriki, A. The neural origins and implications of imitation, mirror neurons and tool use. Curr Opin Neurobiol 2006;16:660–667.CrossRefGoogle ScholarPubMed
Karlen, SJ, Krubitzer, L. The evolution of the neocortex in mammals: intrinsic and extrinsic contributions to the cortical phenotype. Novartis Found Symp 2006;270:146–159.CrossRefGoogle ScholarPubMed
Khaitovich, P, Enard, W, Lachmann, M, Paabo, S. Evolution of primate gene expression. Nat Rev Genet 2006;7:693–702.CrossRefGoogle ScholarPubMed
Kriegstein, A, Noctor, S, Martinez-Cerdeno, V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006;7:883–890.CrossRefGoogle ScholarPubMed
Molnar, Z, Metin, C, Stoykova, Aet al. Comparative aspects of cerebral cortical development. Eur J Neurosci 2006;23:921–934.CrossRefGoogle ScholarPubMed
Blake, R, Logothetis, NK. Visual competition. Nat Rev Neurosci 2002;3:13–21.CrossRefGoogle ScholarPubMed
Rosa, MG, 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;360:665–691.CrossRefGoogle ScholarPubMed
Martin, SJ, Grimwood, PD, Morris, RG. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 2000;23:649–711.CrossRefGoogle ScholarPubMed
Han, CJ, O’Tuathaigh, CM, Van Trigt, Let al. Trace but not delay fear conditioning requires attention and the anterior cingulate cortex. Proc Natl Acad Sci USA 2003;100:13087–13092.CrossRefGoogle Scholar
Kentros, CG, Agnihotri, NT, Streater, S, Hawkins, RD, Kandel, ER. Increased attention to spatial context increases both place field stability and spatial memory. Neuron 2004;42:283–295.CrossRefGoogle ScholarPubMed
Callaway, EM, Sanes, JR. New technologies. Curr Opin Neurobiol 2006;16:540–542.CrossRefGoogle ScholarPubMed
Vickery, RM. Mind the neuron! Acta Neuropsychiatr 2007;19:177–182.CrossRefGoogle ScholarPubMed
Cohen, MR, Newsome, WT. What electrical microstimulation has revealed about the neural basis of cognition. Curr Opin Neurobiol 2004;14:169–177.CrossRefGoogle ScholarPubMed
Tehovnik, EJ, Tolias, AS, Sultan, F, Slocum, WM, Logothetis, NK. Direct and indirect activation of cortical neurons by electrical microstimulation. J Neurophysiol 2006;96:512–521.CrossRefGoogle ScholarPubMed
Bliss, TV, Collingridge, GL. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 1993;361:31–39.CrossRefGoogle ScholarPubMed
Wilbrecht, L, Nottebohm, F. Vocal learning in birds and humans. Ment Retard Dev Disabil Res Rev 2003;9:135–148.CrossRefGoogle ScholarPubMed
Emery, NJ, Clayton, NS. The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 2004;306:1903–1907.CrossRefGoogle ScholarPubMed
Clayton, NS, Hen, R. Neural circuits and behaviour: developmental and evolutionary perspectives. Curr Opin Neurobiol 2005;15:683–685.CrossRefGoogle ScholarPubMed
Raby, CR, Alexis, DM, Dickinson, A, Clayton, NS. Planning for the future by western scrub-jays. Nature 2007;445:919–921.CrossRefGoogle ScholarPubMed
Long, A, Platt, M. Decision making: the virtue of patience in primates. Curr Biol 2005;15:R874–R876.CrossRefGoogle ScholarPubMed
Emery, NJ, Clayton, NS. Evolution of the avian brain and intelligence. Curr Biol 2005;15:R946–R950.CrossRefGoogle ScholarPubMed
Srinivasan, MV, Zhang, S. Visual motor computations in insects. Annu Rev Neurosci 2004;27:679–696.CrossRefGoogle ScholarPubMed
Laureys, S, Giacino, JT, Schiff, ND, Schabus, M, Owen, AM. How should functional imaging of patients with disorders of consciousness contribute to their clinical rehabilitation needs? Curr Opin Neurol 2006;19:520–527.CrossRefGoogle ScholarPubMed
Dunbar, RI, Shultz, S. Understanding primate brain evolution. Philos Trans R Soc Lond B Biol Sci 2007;362:649–658.CrossRefGoogle ScholarPubMed
Butler, AB, Manger, PR, Lindahl, BI, Arhem, P. Evolution of the neural basis of consciousness: a bird-mammal comparison. Bioessays 2005;27:923–936.CrossRefGoogle ScholarPubMed
Blakemore, C. In celebration of cerebration. Lancet 2005;366:2035–2057.CrossRefGoogle ScholarPubMed
Nithianantharajah, J, Hannan, AJ. Dynamic mutations as digital genetic modulators of brain development, function and dysfunction. Bioessays 2007;29:525–535.CrossRefGoogle ScholarPubMed
Johnson, MH, Munakata, Y. Processes of change in brain and cognitive development. Trends Cogn Sci 2005;9:152–158.CrossRefGoogle ScholarPubMed
Khazipov, R, Luhmann, HJ. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci 2006;29:414–418.CrossRefGoogle ScholarPubMed
Lamme, VA. Towards a true neural stance on consciousness. Trends Cogn Sci 2006;10:494–501.CrossRefGoogle ScholarPubMed
Malhi, GS, Sachdev, P. Novel physical treatments for the management of neuropsychiatric disorders. J Psychosom Res 2002;53:709–719.CrossRefGoogle ScholarPubMed
Kobayashi, M, Pascual-Leone, A. Transcranial magnetic stimulation in neurology. Lancet Neurol 2003;2:145–156.CrossRefGoogle ScholarPubMed
Loo, CK, Mitchell, PB. A review of the efficacy of transcranial magnetic stimulation (TMS) treatment for depression, and current and future strategies to optimize efficacy. J Affect Disord 2005;88:255–267.CrossRefGoogle ScholarPubMed
Miller, SM, Ngo, TT. Studies of caloric vestibular stimulation: implications for the cognitive neurosciences, clinical neurosciences and neurophilosophy. Acta Neuropsychiatr 2007;19:183–203.CrossRefGoogle ScholarPubMed
Huntington’s Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell 1993;72:971–983.CrossRefGoogle ScholarPubMed
Bates, GP, Harper, PS, Jones, L. (eds.) Huntington’s disease, 3rd edn. Oxford: Oxford University Press, 2002.Google ScholarPubMed
Van Dellen, A, Grote, HE, Hannan, AJ. Gene-environment interactions, neuronal dysfunction and pathological plasticity in Huntington’s disease. Clin Exp Pharmacol Physiol 2005;32:1007–1019.CrossRefGoogle ScholarPubMed
Rosas, HD, Koroshetz, WJ, Chen, YIet al. Evidence for more widespread cerebral pathology in early HD: an MRI-based morphometric analysis. Neurology 2003;60:1615–1620.CrossRefGoogle ScholarPubMed
Georgiou-Karistianis, N, Smith, E, Bradshaw, JLet al. Future directions in research with presymptomatic individuals carrying the gene for Huntington’s disease. Brain Res Bull 2003;59:331–338.CrossRefGoogle ScholarPubMed
Georgiou-Karistianis, N, Sritharan, A, Farrow, Met al. Increased cortical recruitment in Huntington’s disease using a Simon task. Neuropsychologia 2007;45:1791–1800.CrossRefGoogle ScholarPubMed
Thiruvady, DR, Georgiou-Karistianis, N, Egan, GFet al. Functional connectivity of the prefrontal cortex in Huntington’s disease. J Neurol Neurosurg Psychiatry 2007;78:127–133.CrossRefGoogle ScholarPubMed
Mangiarini, L, Sathasivam, K, Seller, Met al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 1996;87:493–506.CrossRefGoogle Scholar
Murphy, KP, Carter, RJ, Lione, LAet al. Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human Huntington’s disease mutation. J Neurosci 2000;20:5115–5123.Google ScholarPubMed
Mazarakis, NK, Cybulska-Klosowicz, A, Grote, Het al. Deficits in experience-dependent cortical plasticity and sensory-discrimination learning in presymptomatic Huntington’s disease mice. J Neurosci 2005;25:3059–3066.CrossRefGoogle ScholarPubMed
van Dellen, A, Blakemore, C, Deacon, R, York, D, Hannan, AJ. Delaying the onset of Huntington’s in mice. Nature 2000;404:721–722.CrossRefGoogle ScholarPubMed
Spires, TL, Grote, HE, Varshney, NKet al. Environmental enrichment rescues protein deficits in a mouse model of Huntington’s disease, indicating a possible disease mechanism. J Neurosci 2004;24:2270–2276.CrossRefGoogle Scholar
Nithianantharajah, J, Hannan, AJ. Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat Rev Neurosci 2006;7:697–709.CrossRefGoogle ScholarPubMed
Wexler, NS, Lorimer, J, Porter, Jet al.; U.S.-Venezuela Collaborative Research Project. Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington’s disease age of onset. Proc Natl Acad Sci USA 2004;101:3498–3503.Google ScholarPubMed
Spires, TL, Hyman, BT. Neuronal structure is altered by amyloid plaques. Rev Neurosci 2004;15:267–278.CrossRefGoogle ScholarPubMed
Masters, CL, Cappai, R, Barnham, KJ, Villemagne, VL. Molecular mechanisms for Alzheimer’s disease: implications for neuroimaging and therapeutics. J Neurochem 2006;97:1700–1725.CrossRefGoogle ScholarPubMed
Valenzuela, MJ, Sachdev, P. Brain reserve and dementia: a systematic review. Psychol Med 2006;36:441–454.CrossRefGoogle ScholarPubMed
Spires, TL, Hannan, AJ. Molecular mechanisms mediating pathological plasticity in Huntington’s disease and Alzheimer’s disease. J Neurochem 2007;100:874–882.CrossRefGoogle ScholarPubMed
Villemagne, VL, Rowe, CC, Macfarlane, S, Novakovic, KE, Masters, CL. Imaginem oblivionis: the prospects of neuroimaging for early detection of Alzheimer’s disease. J Clin Neurosci 2005;12:221–230.CrossRefGoogle ScholarPubMed
Pantelis, C, Yucel, M, Wood, SJet al. Structural brain imaging evidence for multiple pathological processes at different stages of brain development in schizophrenia. Schizophr Bull 2005;31:672–696.CrossRefGoogle Scholar
Gray, L, Hannan, AJ. Dissecting cause and effect in the pathogenesis of psychiatric disorders: genes, environment and behaviour. Curr Mol Med 2007 (in press).Google Scholar
Harrison, PJ, Weinberger, DR. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005;10:40–68.CrossRefGoogle ScholarPubMed
Rickards, H. Depression in neurological disorders: an update. Curr Opin Psychiatry 2006;19:294–298.CrossRefGoogle ScholarPubMed
Nestler, EJ, Gould, E, Manji, Het al. Preclinical models: status of basic research in depression. Biol Psychiatry 2002;52:503–528.CrossRefGoogle ScholarPubMed
Dranovsky, A, Hen, R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry 2006;59:1136–1143.CrossRefGoogle ScholarPubMed
Grote, HE, Hannan, AJ. Regulators of adult neurogenesis in the healthy and diseased brain. Clin Exp Pharmacol Physiol 2007;34:533–545.CrossRefGoogle ScholarPubMed
Grote, HE, Bull, ND, Howard, MLet al. Cognitive disorders and neurogenesis deficits in Huntington’s disease mice are rescued by fluoxetine. Eur J Neurosci 2005;22:2081–2088.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Belmonte, MK. Autism: a window onto the development of the social and the analytic brain. Annu Rev Neurosci 2005;28:109–126.CrossRefGoogle ScholarPubMed
Amodio, DM, Frith, CD. Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 2006;7:268–277.CrossRefGoogle ScholarPubMed
Meyer-Lindenberg, A, Mervis, CB, Berman, KF. Neural mechanisms in Williams syndrome: a unique window to genetic influences on cognition and behaviour. Nat Rev Neurosci 2006;7:380–393.CrossRefGoogle ScholarPubMed
Skuse, D. Genetic influences on the neural basis of social cognition. Philos Trans R Soc Lond B Biol Sci 2006;361:2129–2141.CrossRefGoogle ScholarPubMed
Stevens, A, Price, J. Evolutionary psychiatry: a new beginning. New York: Routledge, 1996.Google Scholar
Keller, MC, Miller, G. Resolving the paradox of common, harmful, heritable mental disorders: which evolutionary genetic models work best? Behav Brain Sci 2006;29:385–404.CrossRefGoogle ScholarPubMed
Panksepp, J. Emotional endophenotypes in evolutionary psychiatry. Prog Neuropsychopharmacol Biol Psychiatry 2006;30:774–784.CrossRefGoogle ScholarPubMed