The Theory of Localist Representation and of a Purely Abstract Cognitive System: The Evidence from Cortical Columns, Category Cells, and Multisensory Neurons

The debate about representation in the brain and the nature of the cognitive system has been going on for decades now. This paper examines the neurophysiological evidence, primarily from single cell recordings, to get a better perspective on both the issues. After an initial review of some basic concepts, the paper reviews the data from single cell recordings – in cortical columns and of category-selective and multisensory neurons. In neuroscience, columns in the neocortex (cortical columns) are understood to be a basic functional/computational unit. The paper reviews the fundamental discoveries about the columnar organization and finds that it reveals a massively parallel search mechanism. This columnar organization could be the most extensive neurophysiological evidence for the widespread use of localist representation in the brain. The paper also reviews studies of category-selective cells. The evidence for category-selective cells reveals that localist representation is also used to encode complex abstract concepts at the highest levels of processing in the brain. A third major issue is the nature of the cognitive system in the brain and whether there is a form that is purely abstract and encoded by single cells. To provide evidence for a single-cell based purely abstract cognitive system, the paper reviews some of the findings related to multisensory cells. It appears that there is widespread usage of multisensory cells in the brain in the same areas where sensory processing takes place. Plus there is evidence for abstract modality invariant cells at higher levels of cortical processing. Overall, that reveals the existence of a purely abstract cognitive system in the brain. The paper also argues that since there is no evidence for dense distributed representation and since sparse representation is actually used to encode memories, there is actually no evidence for distributed representation in the brain. Overall, it appears that, at an abstract level, the brain is a massively parallel, distributed computing system that is symbolic. The paper also explains how grounded cognition and other theories of the brain are fully compatible with localist representation and a purely abstract cognitive system.

[1]  R. Desimone,et al.  Stimulus-selective properties of inferior temporal neurons in the macaque , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  K. Doya,et al.  Representation of Action-Specific Reward Values in the Striatum , 2005, Science.

[3]  T. Hromádka,et al.  Sparse Representation of Sounds in the Unanesthetized Auditory Cortex , 2008, PLoS biology.

[4]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[5]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[6]  David C Earle,et al.  On the differences between cognitive and noncognitive systems , 1987, Behavioral and Brain Sciences.

[7]  C. Koch,et al.  Category-specific visual responses of single neurons in the human medial temporal lobe , 2000, Nature Neuroscience.

[8]  D. Perrett,et al.  Visual neurones responsive to faces in the monkey temporal cortex , 2004, Experimental Brain Research.

[9]  H. Barlow The neuron doctrine in perception. , 1995 .

[10]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[11]  Paul C. Bressloff,et al.  Laminar Neural Field Model of Laterally Propagating Waves of Orientation Selectivity , 2015, PLoS Comput. Biol..

[12]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[13]  Charles G. Gross,et al.  Coding for visual categories in the human brain , 2000, Nature Neuroscience.

[14]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  M. Ross Quillian,et al.  Retrieval time from semantic memory , 1969 .

[16]  Robin A. A. Ince,et al.  Neural Codes Formed by Small and Temporally Precise Populations in Auditory Cortex , 2013, The Journal of Neuroscience.

[17]  T. Albright,et al.  Two-dimensional map of direction selectivity in cortical visual area MT of Cebus monkey. , 2002, Anais da Academia Brasileira de Ciencias.

[18]  Kathleen S. Rockland,et al.  Five Points on Columns , 2010, Front. Neuroanat..

[19]  Chris I. Baker,et al.  Integration of Visual and Auditory Information by Superior Temporal Sulcus Neurons Responsive to the Sight of Actions , 2005, Journal of Cognitive Neuroscience.

[20]  P. Goldman-Rakic,et al.  Dissociation of object and spatial processing domains in primate prefrontal cortex. , 1993, Science.

[21]  Asim Roy,et al.  A theory of the brain: localist representation is used widely in the brain , 2012, Front. Psychology.

[22]  Zenon W. Pylyshyn,et al.  Connectionism and cognitive architecture: A critical analysis , 1988, Cognition.

[23]  M. Tarr,et al.  Visual Object Recognition , 1996, ISTCS.

[24]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: part 1.: an account of basic findings , 1988 .

[25]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[26]  Mauro Ursino,et al.  A model of contextual interactions and contour detection in primary visual cortex , 2004, Neural Networks.

[27]  J. Maunsell,et al.  Sensory modality specificity of neural activity related to memory in visual cortex. , 1997, Journal of neurophysiology.

[28]  David J. Field,et al.  Sparse coding with an overcomplete basis set: A strategy employed by V1? , 1997, Vision Research.

[29]  Alex Martin,et al.  Representation of Manipulable Man-Made Objects in the Dorsal Stream , 2000, NeuroImage.

[30]  P. Smolensky THE CONSTITUENT STRUCTURE OF CONNECTIONIST MENTAL STATES: A REPLY TO FODOR AND PYLYSHYN , 2010 .

[31]  FRANK MORRELL,et al.  Visual System's View of Acoustic Space , 1972, Nature.

[32]  David J. Freedman,et al.  Neural mechanisms of visual categorization: Insights from neurophysiology , 2008, Neuroscience & Biobehavioral Reviews.

[33]  Tomaso Poggio,et al.  Generalization in vision and motor control , 2004, Nature.

[34]  T. Gelder,et al.  Mind as Motion: Explorations in the Dynamics of Cognition , 1995 .

[35]  Lizabeth M Romanski,et al.  Representation and integration of auditory and visual stimuli in the primate ventral lateral prefrontal cortex. , 2007, Cerebral cortex.

[36]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[37]  Rolls Et Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. , 1984 .

[38]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[39]  J. Assad,et al.  Direction selectivity of neurons in the macaque lateral intraparietal area. , 2009, Journal of neurophysiology.

[40]  Henry Markram,et al.  The Neocortical Column , 2012, Front. Neuroanat..

[41]  C. Gross Genealogy of the “Grandmother Cell” , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[42]  M. Sakagami,et al.  Category representation and generalization in the prefrontal cortex , 2012, The European journal of neuroscience.

[43]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[44]  M. Carandini,et al.  Integration of visual motion and locomotion in mouse visual cortex , 2013, Nature Neuroscience.

[45]  G. DeAngelis,et al.  Organization of Disparity-Selective Neurons in Macaque Area MT , 1999, The Journal of Neuroscience.

[46]  Joe Z Tsien,et al.  Neural encoding of the concept of nest in the mouse brain , 2007, Proceedings of the National Academy of Sciences.

[47]  P. Smolensky On the proper treatment of connectionism , 1988, Behavioral and Brain Sciences.

[48]  R. Quiroga Concept cells: the building blocks of declarative memory functions , 2012, Nature Reviews Neuroscience.

[49]  I. Fried,et al.  Percepts to recollections: insights from single neuron recordings in the human brain , 2012, Trends in Cognitive Sciences.

[50]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[51]  P. Földiák,et al.  Forming sparse representations by local anti-Hebbian learning , 1990, Biological Cybernetics.

[52]  Alison L. Barth,et al.  Experimental evidence for sparse firing in the neocortex , 2012, Trends in Neurosciences.

[53]  M. Page,et al.  Connectionist modelling in psychology: A localist manifesto , 2000, Behavioral and Brain Sciences.

[54]  N. Logothetis,et al.  Shape representation in the inferior temporal cortex of monkeys , 1995, Current Biology.

[55]  Keiji Tanaka Columns for complex visual object features in the inferotemporal cortex: clustering of cells with similar but slightly different stimulus selectivities. , 2003, Cerebral cortex.

[56]  Allen Newell,et al.  Computer science as empirical inquiry: symbols and search , 1976, CACM.

[57]  A. M. Schrier,et al.  Categorization of natural stimuli by monkeys (Macaca mulatta): effects of stimulus set size and modification of exemplars. , 1987, Journal of experimental psychology. Animal behavior processes.

[58]  J. Panksepp,et al.  Sleep as a fundamental property of neuronal assemblies , 2008, Nature Reviews Neuroscience.

[59]  Emilio Kropff,et al.  Place cells, grid cells, and the brain's spatial representation system. , 2008, Annual review of neuroscience.

[60]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[61]  E. Rolls,et al.  Spatial View Cells in the Primate Hippocampus , 1997, The European journal of neuroscience.

[62]  R. Desimone Face-Selective Cells in the Temporal Cortex of Monkeys , 1991, Journal of Cognitive Neuroscience.

[63]  M. Hasselmo,et al.  Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[64]  Michael L. Hines,et al.  Sparse Distributed Representation of Odors in a Large-scale Olfactory Bulb Circuit , 2013, PLoS Comput. Biol..

[65]  V. Mountcastle The columnar organization of the neocortex. , 1997, Brain : a journal of neurology.

[66]  R. Wyttenbach,et al.  Categorical Perception of Sound Frequency by Crickets , 1996, Science.

[67]  Walter J. Freeman,et al.  Representations: Who Needs Them? , 1990 .

[68]  W. Freeman Second Commentary: On the proper treatment of connectionism by Paul Smolensky (1988) - Neuromachismo Rekindled , 1989 .

[69]  Allen Newell,et al.  Physical Symbol Systems , 1980, Cogn. Sci..

[70]  B. A. Baldwin,et al.  Cells in temporal cortex of conscious sheep can respond preferentially to the sight of faces. , 1987, Science.

[71]  C. Gross,et al.  A neuronal representation of the location of nearby sounds , 1999, Nature.

[72]  Daniel L Adams,et al.  The cortical column: a structure without a function , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[73]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[74]  C. Koch,et al.  Sparse but not ‘Grandmother-cell’ coding in the medial temporal lobe , 2008, Trends in Cognitive Sciences.

[75]  Diane Pecher,et al.  Introduction to the Special Topic Embodied and Grounded Cognition , 2011, Front. Psychology.

[76]  P S Goldman-Rakic,et al.  Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. , 1999, Cerebral cortex.

[77]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[78]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[79]  J. Tanji,et al.  Neuronal activity in the primate prefrontal cortex in the process of motor selection based on two behavioral rules. , 2000, Journal of neurophysiology.

[80]  Asim Roy An extension of the localist representation theory: grandmother cells are also widely used in the brain , 2013, Front. Psychol..

[81]  M. R. D'Amato,et al.  The person concept in monkeys (Cebus apella) , 1988 .

[82]  E. Rolls,et al.  Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey , 2004, Experimental Brain Research.

[83]  M. A. Carreira-Perpiñán,et al.  Cortical Columns , 2002 .

[84]  James L. McClelland,et al.  Précis of Semantic Cognition: A Parallel Distributed Processing Approach , 2008, Behavioral and Brain Sciences.

[85]  Peter M. Todd,et al.  Learning and connectionist representations , 1993 .

[86]  Lawrence W. Barsalou,et al.  Grounded Cognition: Past, Present, and Future , 2010, Top. Cogn. Sci..

[87]  T. Rogers,et al.  Where do you know what you know? The representation of semantic knowledge in the human brain , 2007, Nature Reviews Neuroscience.

[88]  John J. Foxe,et al.  The timing and laminar profile of converging inputs to multisensory areas of the macaque neocortex. , 2002, Brain research. Cognitive brain research.

[89]  Christopher D. Chambers,et al.  Current perspectives and methods in studying neural mechanisms of multisensory interactions , 2012, Neuroscience & Biobehavioral Reviews.

[90]  S. Thorpe Localized versus distributed representations , 1998 .

[91]  E. Rolls Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. , 1984, Human neurobiology.

[92]  Robert L. Goldstone,et al.  Categorical perception. , 2010, Wiley interdisciplinary reviews. Cognitive science.

[93]  Jeffrey S Bowers,et al.  On the biological plausibility of grandmother cells: implications for neural network theories in psychology and neuroscience. , 2009, Psychological review.

[94]  K M Gothard,et al.  Neural responses to facial expression and face identity in the monkey amygdala. , 2007, Journal of neurophysiology.

[95]  Asif A Ghazanfar,et al.  Multisensory Integration of Looming Signals by Rhesus Monkeys , 2004, Neuron.

[96]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[97]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[98]  M. Papas Shape Representation , 2019 .

[99]  H. Karten,et al.  Laminar and columnar auditory cortex in avian brain , 2010, Proceedings of the National Academy of Sciences.

[100]  R. Desimone,et al.  Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[101]  A. Nieder,et al.  Cross-Modal Associative Mnemonic Signals in Crow Endbrain Neurons , 2015, Current Biology.

[102]  James L. McClelland,et al.  An interactive activation model of context effects in letter perception: I. An account of basic findings. , 1981 .

[103]  James K. Kroger,et al.  Cross-modal and cross-temporal association in neurons of frontal cortex , 2000, Nature.

[104]  V. Mountcastle Modality and topographic properties of single neurons of cat's somatic sensory cortex. , 1957, Journal of neurophysiology.

[105]  P. Goldman-Rakic,et al.  An auditory domain in primate prefrontal cortex , 2002, Nature Neuroscience.

[106]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study , 1999, The European journal of neuroscience.

[107]  S. Thorpe,et al.  Rapid categorization of natural images by rhesus monkeys , 1998, Neuroreport.

[108]  L. Barsalou Grounded cognition. , 2008, Annual review of psychology.

[109]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[110]  B. Mesquita,et al.  Adjustment to Chronic Diseases and Terminal Illness Health Psychology : Psychological Adjustment to Chronic Disease , 2006 .

[111]  Geoffrey E. Hinton,et al.  Distributed Representations , 1986, The Philosophy of Artificial Intelligence.

[112]  Jeffrey L. Elman,et al.  Language as a dynamical system , 1996 .

[113]  James L. McClelland,et al.  Semantic Cognition: A Parallel Distributed Processing Approach , 2004 .

[114]  J. Macke,et al.  Neural population coding: combining insights from microscopic and mass signals , 2015, Trends in Cognitive Sciences.

[115]  Amy Coplan Simulating Minds: The Philosophy, Psychology, and Neuroscience of Mindreading by goldman, alvin , 2008 .

[116]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[117]  W. Roberts,et al.  Concept learning at different levels of abstraction by pigeons, monkeys, and people. , 1988 .

[118]  E. Rolls,et al.  Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey , 1985, Brain Research.

[119]  C. Koch,et al.  Explicit Encoding of Multimodal Percepts by Single Neurons in the Human Brain , 2009, Current Biology.

[120]  Ankoor S. Shah,et al.  Auditory Cortical Neurons Respond to Somatosensory Stimulation , 2003, The Journal of Neuroscience.

[121]  M. Brecht,et al.  Behavioural report of single neuron stimulation in somatosensory cortex , 2008, Nature.

[122]  Kristin Scott,et al.  Taste Representations in the Drosophila Brain , 2004, Cell.

[123]  Henning Scheich,et al.  Anatomical connections suitable for the direct processing of neuronal information of different modalities via the rodent primary auditory cortex , 2009, Hearing Research.

[124]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[125]  A. J. Mistlin,et al.  Specialized face processing and hemispheric asymmetry in man and monkey: Evidence from single unit and reaction time studies , 1988, Behavioural Brain Research.

[126]  A. Pouget,et al.  Neural correlations, population coding and computation , 2006, Nature Reviews Neuroscience.

[127]  Michael J. Spivey,et al.  Computational Grounded Cognition: a new alliance between grounded cognition and computational modeling , 2013, Front. Psychology.

[128]  C. Koch,et al.  A category-specific response to animals in the right human amygdala , 2011, Nature Neuroscience.

[129]  Andreas Nieder,et al.  Active encoding of decisions about stimulus absence in primate prefrontal cortex neurons , 2012, Proceedings of the National Academy of Sciences.

[130]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 1: behavioural study , 1999, The European journal of neuroscience.

[131]  Anne Kuefer,et al.  The Case For Mental Imagery , 2016 .

[132]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[133]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

[134]  Andreas Nieder,et al.  Coding of abstract quantity by ‘number neurons’ of the primate brain , 2012, Journal of Comparative Physiology A.