Brain maps, great and small: lessons from comparative studies of primate visual cortical organization

In this paper, we review evidence from comparative studies of primate cortical organization, highlighting recent findings and hypotheses that may help us to understand the rules governing evolutionary changes of the cortical map and the process of formation of areas during development. We argue that clear unequivocal views of cortical areas and their homologies are more likely to emerge for ‘core’ fields, including the primary sensory areas, which are specified early in development by precise molecular identification steps. In primates, the middle temporal area is probably one of these primordial cortical fields. Areas that form at progressively later stages of development correspond to progressively more recent evolutionary events, their development being less firmly anchored in molecular specification. The certainty with which areal boundaries can be delimited, and likely homologies can be assigned, becomes increasingly blurred in parallel with this evolutionary/developmental sequence. For example, while current concepts for the definition of cortical areas have been vindicated in allowing a clarification of the organization of the New World monkey ‘third tier’ visual cortex (the third and dorsomedial areas, V3 and DM), our analyses suggest that more flexible mapping criteria may be needed to unravel the organization of higher-order visual association and polysensory areas.

[1]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[2]  Giorgio M Innocenti,et al.  Immature cortex lesions alter retinotopic maps and interhemispheric connections , 2003, Annals of neurology.

[3]  R Gattass,et al.  Cortical afferents of visual area MT in the Cebus monkey: Possible homologies between New and old World monkeys , 1993, Visual Neuroscience.

[4]  G. Glazko,et al.  Estimation of divergence times for major lineages of primate species. , 2003, Molecular biology and evolution.

[5]  Burke,et al.  Selective block of conduction in Y optic nerve fibres: significance for the concept of parallel processing , 1998, The European journal of neuroscience.

[6]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[7]  H. Kennedy,et al.  The timetable of laminar neurogenesis contributes to the specification of cortical areas in mouse isocortex , 1997, The Journal of comparative neurology.

[8]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[9]  L Weiskrantz,et al.  Pattern of neuronal activity associated with conscious and unconscious processing of visual signals. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[11]  A. Cowey,et al.  The regional cortical basis of achromatopsia: a study on macaque monkeys and an achromatopsic patient , 2001, The European journal of neuroscience.

[12]  M G Rosa,et al.  The dorsomedial visual areas in New World and Old World monkeys: homology and function , 2001, The European journal of neuroscience.

[13]  M. Paolini,et al.  Direction selectivity in the middle lateral and lateral (ML and L) visual areas in the California ground squirrel. , 1998, Cerebral cortex.

[14]  H. Sherk,et al.  A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex , 1993, Visual Neuroscience.

[15]  W. Maguire,et al.  Visuotopic organization of the prelunate gyrus in rhesus monkey , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  Aina Puce,et al.  Electrophysiology and brain imaging of biological motion. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[17]  R E Weller,et al.  Cortical connections of striate cortex in the owl monkey , 1982, The Journal of comparative neurology.

[18]  Annie C. Hsueh,et al.  Pattern motion integration in infants. , 2004, Journal of vision.

[19]  S. Zeki,et al.  The Riddoch syndrome: insights into the neurobiology of conscious vision. , 1998, Brain : a journal of neurology.

[20]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[21]  W. B. Spatz,et al.  Transient molecular visualization of ocular dominance columns (ODCs) in normal adult marmosets despite the desegregated termination of the retino‐geniculo‐cortical pathways , 1998, The Journal of comparative neurology.

[22]  O. Creutzfeldt,et al.  Extrageniculo-striate visual mechanisms: compartmentalization of visual functions. , 1988, Progress in brain research.

[23]  M. Eadie Alfred Walter Campbell (1868–1937) , 2003, Journal of Neurology.

[24]  Keiji Tanaka,et al.  Neuronal selectivities to complex object features in the ventral visual pathway of the macaque cerebral cortex. , 1994, Journal of neurophysiology.

[25]  J. Kaas,et al.  Distinctive compartmental organization of human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Levitt,et al.  A monoclonal antibody to limbic system neurons. , 1984, Science.

[27]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[28]  W. Newsome,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[29]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  G. Elston,et al.  Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area, middle temporal crescent, and surrounding cortex , 1998, The Journal of comparative neurology.

[31]  B. Finlay,et al.  Developmental structure in brain evolution , 2001, Behavioral and Brain Sciences.

[32]  Ricardo Gattass,et al.  Third tier ventral extrastriate cortex in the New World monkey, Cebus apella , 2000, Experimental Brain Research.

[33]  H. Dinse,et al.  Contribution of area 19 to the foreground-background-interaction of the cat: an analysis based on single cell recordings and behavioural experiments , 2004, Experimental Brain Research.

[34]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

[35]  L. Krubitzer,et al.  The evolution of visual cortex: where is V2? , 1999, Trends in Neurosciences.

[36]  M M Cohen,et al.  Speechreading in the akinetopsic patient, L.M. , 1997, Brain : a journal of neurology.

[37]  N. Rubin,et al.  fMRI Activation in Response to Illusory Contours and Salient Regions in the Human Lateral Occipital Complex , 2003, Neuron.

[38]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J. Kaas,et al.  Connections of primary auditory cortex in the new world monkey, Saguinus , 1989, The Journal of comparative neurology.

[40]  G. Orban,et al.  Selectivity for 3D shape that reveals distinct areas within macaque inferior temporal cortex. , 2000, Science.

[41]  W. Burke,et al.  LIMITS OF PARALLEL PROCESSING: EXCITATORY CONVERGENCE OF DIFFERENT INFORMATION CHANNELS ON SINGLE NEURONS IN STRIATE AND EXTRASTRIATE VISUAL CORTICES , 1996, Clinical and experimental pharmacology & physiology.

[42]  Michela Gamberini,et al.  The Most Direct Visual Pathway to the Frontal Cortex , 2004, Cortex.

[43]  J. Kaas,et al.  Topographic patterns of V2 cortical connections in macaque monkeys , 1996, The Journal of comparative neurology.

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

[45]  M. Rosa Visual maps in the adult primate cerebral cortex: some implications for brain development and evolution. , 2002, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[46]  Keiji Tanaka,et al.  Divergent backward projections from the anterior part of the inferotemporal cortex (area TE) in the macaque , 2000, The Journal of comparative neurology.

[47]  Rafael Yuste,et al.  Gap junctions in developing neocortex: a review , 2004, Brain Research Reviews.

[48]  C. N. Guy,et al.  The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. , 1995, Brain : a journal of neurology.

[49]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[50]  Wendy A Suzuki,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cytoarchitectonic and chemoarchitectonic organization , 2003, The Journal of comparative neurology.

[51]  Doris Y. Tsao,et al.  Neuroimaging Weighs In: Humans Meet Macaques in “Primate” Visual Cortex , 2003, The Journal of Neuroscience.

[52]  D. Pandya,et al.  Intrinsic connections and architectonics of the superior temporal sulcus in the rhesus monkey , 1989, The Journal of comparative neurology.

[53]  A. Mikami,et al.  Projections from the cytochrome oxidase modules of visual area V2 to the ventral posterior area in the macaque , 2004, Experimental Brain Research.

[54]  Xiangmin Xu,et al.  Optical imaging of visually evoked responses in prosimian primates reveals conserved features of the middle temporal visual area. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[55]  P. Rakić,et al.  Changes in cell-cycle kinetics during the development and evolution of primate neocortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  L. Palmer,et al.  The retinotopic organization of lateral suprasylvian visual areas in the cat , 1978, The Journal of comparative neurology.

[57]  C. Oxnard,et al.  Evolutionary radiations and convergences in the structural organization of mammalian brains , 2001, Nature.

[58]  R Gattass,et al.  Area V4 in Cebus monkey: extent and visuotopic organization. , 1998, Cerebral cortex.

[59]  D. Pandya,et al.  Dorsolateral prefrontal cortex: comparative cytoarchitectonic analysis in the human and the macaque brain and corticocortical connection patterns , 1999, The European journal of neuroscience.

[60]  Giorgio M Innocenti,et al.  Areal organization of the posterior parietal cortex of the ferret (Mustela putorius). , 2002, Cerebral cortex.

[61]  L. Krubitzer,et al.  Organization of somatosensory cortex in three species of marsupials, Dasyurus hallucatus, Dactylopsila trivirgata, and Monodelphis domestica: Neural correlates of morphological specializations , 1999, The Journal of comparative neurology.

[62]  Lawrence C. Sincich,et al.  Complete flatmounting of the macaque cerebral cortex , 2003, Visual Neuroscience.

[63]  M. Rosa Visuotopic Organization of Primate Extrastriate Cortex , 1997 .

[64]  D. Pandya,et al.  Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey , 2002, The European journal of neuroscience.

[65]  M. Mishkin,et al.  Pattern discrimination thresholds after partial inferior temporal or lateral striate lesions in monkeys , 1977, Brain Research.

[66]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[67]  G. Striedter Stepping into the Same River Twice: Homologues as Recurring Attractors in Epigenetic Landscapes , 1998, Brain, Behavior and Evolution.

[68]  M G Rosa,et al.  Retinotopic orgarnzation of the primary visual cortex of flying foxes (Pteropus poliocephalus and pteropus scapulatus) , 1993, The Journal of comparative neurology.

[69]  B. Fischer,et al.  Visual field representations and locations of visual areas V1/2/3 in human visual cortex. , 2003, Journal of vision.

[70]  R. Reale,et al.  Tonotopic organization in auditory cortex of the cat , 1980, The Journal of comparative neurology.

[71]  M. Rosa,et al.  CLARIFYING HOMOLOGIES IN THE MAMMALIAN CEREBRAL CORTEX: THE CASE OF THE THIRD VISUAL AREA (V3) , 2005, Clinical and experimental pharmacology & physiology.

[72]  P S Goldman-Rakic,et al.  Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[73]  T. Hashikawa,et al.  Retinol-binding protein gene is highly expressed in higher-order association areas of the primate neocortex. , 2004, Cerebral cortex.

[74]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[75]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[76]  P. Levitt,et al.  Expression of the mRNAs encoding the limbic system‐associated membrane protein (LAMP): I. Adult rat brain , 1996, The Journal of comparative neurology.

[77]  Alex R. Wade,et al.  Long-term deprivation affects visual perception and cortex , 2003, Nature Neuroscience.

[78]  I. Fujita,et al.  Distribution of α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionate‐type glutamate receptor subunits (GluR2/3) along the ventral visual pathway in the monkey , 2003, The Journal of comparative neurology.

[79]  W T Newsome,et al.  Ventral posterior visual area of the macaque: Visual topography and areal boundaries , 1986, The Journal of comparative neurology.

[80]  J. T. Weber,et al.  Chemoarchitectonic subdivisions of the visual pulvinar in monkeys and their connectional relations with the middle temporal and rostral dorsolateral visual areas, MT and DLr , 1993, The Journal of comparative neurology.

[81]  C. Malsburg,et al.  How patterned neural connections can be set up by self-organization , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[82]  J. Kaas,et al.  Connectional and Architectonic Evidence for Dorsal and Ventral V3, and Dorsomedial Area in Marmoset Monkeys , 2001, The Journal of Neuroscience.

[83]  R B Tootell,et al.  Topography of cytochrome oxidase activity in owl monkey cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[84]  S. Eggan,et al.  Postnatal development of pre‐ and postsynaptic GABA markers at chandelier cell connections with pyramidal neurons in monkey prefrontal cortex , 2003, The Journal of comparative neurology.

[85]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  A. Romer The vertebrate body , 1971 .

[87]  E. Rolls,et al.  Functional subdivisions of the temporal lobe neocortex , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  S. Zeki The distribution of wavelength and orientation selective cells in different areas of monkey visual cortex , 1983, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[89]  M G Rosa,et al.  Visual areas in the dorsal and medial extrastriate cortices of the marmoset , 1995, The Journal of comparative neurology.

[90]  R. Weller,et al.  Cortical connections of dorsal cortex rostral to V II in squirrel monkeys , 1991, The Journal of comparative neurology.

[91]  J. Kaas,et al.  The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). , 1975 .

[92]  M. L. Pucak,et al.  Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex , 1997, Neuroscience.

[93]  G. Elston,et al.  The second visual area in the marmoset monkey: Visuotopic organisation, magnification factors, architectonical boundaries, and modularity , 1997, The Journal of comparative neurology.

[94]  Paul A Yates,et al.  Molecular Development of Sensory Maps Representing Sights and Smells in the Brain , 1999, Cell.

[95]  M G Rosa,et al.  Visual field representation in striate and prestriate cortices of a prosimian primate (Galago garnetti). , 1997, Journal of neurophysiology.

[96]  R. Gattass,et al.  Complete pattern of ocular dominance stripes in V1 of a New World monkey, Cebus apella , 2004, Experimental Brain Research.

[97]  T. Hendler,et al.  Convergence of visual and tactile shape processing in the human lateral occipital complex. , 2002, Cerebral cortex.

[98]  J. Allman,et al.  The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (aotus trivirgatus) , 1975, Brain Research.

[99]  R. Weller,et al.  Cortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1992, The Journal of comparative neurology.

[100]  B. Seltzer,et al.  Architectonics and cortical connections of the upper bank of the superior temporal sulcus in the rhesus monkey: An analysis in the tangential plane , 2003, The Journal of comparative neurology.

[101]  M G Rosa,et al.  Visuotopic organisation of striate cortex in the marmoset monkey (Callithrix jacchus) , 1996, The Journal of comparative neurology.

[102]  P. Rakić,et al.  Molecular gradients and compartments in the embryonic primate cerebral cortex. , 1999, Cerebral cortex.

[103]  E G Jones,et al.  Neurochemical gradient along the monkey occipito-temporal cortical pathway. , 1994, Neuroreport.

[104]  J.H. Kaas,et al.  How do features of sensory representations develop? , 2002, Proceedings 2nd International Conference on Development and Learning. ICDL 2002.

[105]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[106]  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.

[107]  J. Zihl,et al.  Speechreading in the akinetopsic patient , 1997 .

[108]  L Krubitzer,et al.  Area 3a: topographic organization and cortical connections in marmoset monkeys. , 2001, Cerebral cortex.

[109]  D. Pandya,et al.  Comparison of prefrontal architecture and connections. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[110]  T Tarui,et al.  Cell output, cell cycle duration and neuronal specification: a model of integrated mechanisms of the neocortical proliferative process. , 2003, Cerebral cortex.

[111]  R. Weller,et al.  Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys , 1993, Visual Neuroscience.

[112]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[113]  Mazyar Fallah,et al.  Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions , 2003, Neuropsychologia.

[114]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[115]  R. Gattass,et al.  Laminar, columnar and topographic aspects of ocular dominance in the primary visual cortex ofCebus monkeys , 1992, Experimental Brain Research.

[116]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

[117]  G. Bonin,et al.  The neocortex of Macaca mulatta , 1947 .

[118]  D. B. Bender,et al.  Vertical meridian representation on the prelunate gyrus in area V4 of macaque , 2001, Brain Research Bulletin.

[119]  H. Bülthoff,et al.  Representation of the perceived 3-D object shape in the human lateral occipital complex. , 2003, Cerebral cortex.

[120]  W. Burke,et al.  Laminar differences in plasticity in area 17 following retinal lesions in kittens or adult cats , 2003, The European journal of neuroscience.

[121]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[122]  Neurosciences,et al.  Organization of Visual Areas in Macaque and Human Cerebral Cortex , 2002 .

[123]  P. D. Lewis,et al.  The Founders of Neurology , 1972, Medical History.

[124]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: II. Cortical afferents , 2003, The Journal of comparative neurology.

[125]  J. Kaas,et al.  Convergences in the Modular and Areal Organization of the Forebrain of Mammals: Implications for the Reconstruction of Forebrain Evolution , 2002, Brain, Behavior and Evolution.

[126]  Claire E Warner,et al.  Topographic and laminar maturation of striate cortex in early postnatal marmoset monkeys, as revealed by neurofilament immunohistochemistry. , 2005, Cerebral cortex.

[127]  S. Zeki Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[128]  M I Sereno,et al.  Analysis of retinotopic maps in extrastriate cortex. , 1994, Cerebral cortex.

[129]  P. Flechsig Anatomie des menschlichen Gehirns und Rückenmarks : auf myelogenetischer Grundlage , 1920 .

[130]  D. J. Price,et al.  Patterns of cytochrome oxidase activity in areas 17, 18 and 19 of the visual cortex of cats and kittens , 2004, Experimental Brain Research.

[131]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[132]  D. J. Felleman,et al.  Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex , 1997, The Journal of comparative neurology.

[133]  Tutis Vilis,et al.  The lateral occipital complex subserves the perceptual persistence of motion-defined groupings. , 2003, Cerebral cortex.

[134]  J. Kaas,et al.  Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans , 2001, The Journal of comparative neurology.

[135]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[136]  L A Krubitzer,et al.  The organization and connections of somatosensory cortex in marmosets , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[137]  H. Kennedy,et al.  Laminar Distribution of Neurons in Extrastriate Areas Projecting to Visual Areas V1 and V4 Correlates with the Hierarchical Rank and Indicates the Operation of a Distance Rule , 2000, The Journal of Neuroscience.

[138]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[139]  K. Brodmann,et al.  Über den allgemeinen Bauplan des Cortex pallii bei den Mammaliern und zwei homologe Rindenfelder im besonderen , 1906 .

[140]  S. Zeki,et al.  The third visual complex of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[141]  C. Gross,et al.  Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: A dual tracer study , 1988, The Journal of comparative neurology.

[142]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[143]  Brendan J. O'Brien,et al.  The retinal input to calbindin-D28k-defined subdivisions in macaque inferior pulvinar , 2001, Neuroscience Letters.

[144]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[145]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[146]  Todd M. Preuss,et al.  Specializations of the Human Visual System: The Monkey Model Meets Human Reality , 2003 .

[147]  I. Ohzawa,et al.  Receptive field properties of cells in area 19 of the cat , 2004, Experimental Brain Research.

[148]  B R Payne,et al.  Evidence for visual cortical area homologs in cat and macaque monkey. , 1993, Cerebral cortex.

[149]  G. Elston,et al.  Visual Responses of Neurons in the Middle Temporal Area of New World Monkeys after Lesions of Striate Cortex , 2000, The Journal of Neuroscience.

[150]  Kazuo Hikosaka,et al.  Representation of foveal visual fields in the ventral bank of the superior temporal sulcus in the posterior inferotemporal cortex of the macaque monkey , 1998, Behavioural Brain Research.

[151]  Y. Sugita,et al.  Auditory-visual speech perception examined by fMRI and PET , 2003, Neuroscience Research.

[152]  J. Lund,et al.  The hierarchical development of monkey visual cortical regions as revealed by the maturation of parvalbumin-immunoreactive neurons. , 1996, Brain research. Developmental brain research.

[153]  A. Dale,et al.  The representation of the ipsilateral visual field in human cerebral cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[154]  Martin I Sereno,et al.  Brain mapping in animals and humans , 1998, Current Opinion in Neurobiology.

[155]  S. Zeki,et al.  A visuo‐somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A , 1998, The European journal of neuroscience.

[156]  C Blakemore,et al.  Mechanisms Underlying the Early Establishment of Thalamocortical Connections in the Rat , 1998, The Journal of Neuroscience.

[157]  D. R. Kornack Neurogenesis and the Evolution of Cortical Diversity: Mode, Tempo, and Partitioning during Development and Persistence in Adulthood , 2000, Brain, Behavior and Evolution.

[158]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[159]  N. Logothetis,et al.  Visual Areas in Macaque Cortex Measured Using Functional Magnetic Resonance Imaging , 2002, The Journal of Neuroscience.

[160]  G. Orban,et al.  Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. , 1999, Journal of neurophysiology.

[161]  W. Howells The Antecedents of Man. An Introduction to the Evolution of the Primates. , 1961 .

[162]  H. Tamura,et al.  Visual response properties of cells in the ventral and dorsal parts of the macaque inferotemporal cortex. , 2001, Cerebral cortex.

[163]  Henry Kennedy,et al.  Quantitative Analysis of Connectivity in the Visual Cortex: Extracting Function from Structure , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[164]  J. Kaas,et al.  Cortical connections of the dorsomedial visual area in Old World macaque monkeys , 1999, The Journal of comparative neurology.

[165]  D. Amaral,et al.  Macaque monkey retrosplenial cortex: I. Three‐dimensional and cytoarchitectonic organization , 2000, The Journal of comparative neurology.

[166]  Henry Kennedy,et al.  Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. , 2002, Cerebral cortex.

[167]  M. Wassef,et al.  Role of thalamic axons in the expression of H-2Z1, a mouse somatosensory cortex specific marker. , 1999, Cerebral cortex.

[168]  J. Kaas,et al.  Subdivisions of auditory cortex and ipsilateral cortical connections of the parabelt auditory cortex in macaque monkeys , 1998, The Journal of comparative neurology.

[169]  M. Mishkin,et al.  OCCIPITOTEMPORAL CORTICOCORTICAL CONNECTIONS IN THE RHESUS MONKEY. , 1965, Experimental neurology.

[170]  B. Finlay,et al.  Linked regularities in the development and evolution of mammalian brains. , 1995, Science.

[171]  Ron D. Frostig,et al.  A mapping label required for normal scale of body representation in the cortex , 2000, Nature Neuroscience.

[172]  Arnold R. Kriegstein,et al.  Evolutionary radiations and convergences in the structural organization of mammalian brains , 2022 .

[173]  R Gattass,et al.  Visual area MT in the Cebus monkey: Location, visuotopic organization, and variability , 1989, The Journal of comparative neurology.

[174]  M. Gamberini,et al.  Resolving the organization of the New World monkey third visual complex: The dorsal extrastriate cortex of the marmoset (Callithrix jacchus) , 2005, The Journal of comparative neurology.

[175]  J. Bolton,et al.  Anatomie des menschlichen Gehirns und Ruckenmarks auf myelogenetischer Gründlage , 1921 .

[176]  C. Russo,et al.  Timing the origin of New World monkeys. , 2003, Molecular biology and evolution.

[177]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[178]  D. L. Adams,et al.  Capricious expression of cortical columns in the primate brain , 2003, Nature Neuroscience.

[179]  M. Rosa,et al.  Maps of the visual field in the cerebral cortex of primates: Functional organisation and significance , 2004 .

[180]  M. Rosa Topographic organisation of extrastriate areas in the flying fox: Implications for the evolution of mammalian visual cortex , 1999, The Journal of comparative neurology.

[181]  W. B. Spatz,et al.  Morphology and connections of neurons in area 17 projecting to the extrastriate areas mt and 19DM and to the superior colliculus in the monkey Callithrix jacchus , 1995, The Journal of comparative neurology.

[182]  B. Finlay,et al.  Neural development in metatherian and eutherian mammals: Variation and constraint , 1999, The Journal of comparative neurology.

[183]  K. Willecke,et al.  Spatiotemporal transcription of connexin45 during brain development results in neuronal expression in adult mice , 2003, Neuroscience.

[184]  M. Rosa,et al.  Visual areas in lateral and ventral extrastriate cortices of the marmoset monkey , 2000, The Journal of comparative neurology.

[185]  J. Kaas,et al.  Evidence from V1 connections for both dorsal and ventral subdivisions of V3 in three species of new world monkeys , 2002, The Journal of comparative neurology.

[186]  C. Galletti,et al.  The cortical connections of area V6: an occipito‐parietal network processing visual information , 2001, The European journal of neuroscience.

[187]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[188]  Muge M. Bakircioglu,et al.  Mapping visual cortex in monkeys and humans using surface-based atlases , 2001, Vision Research.

[189]  L A Krubitzer,et al.  The dorsomedial visual area of owl monkeys: Connections, myeloarchitecture, and homologies in other primates , 1993, The Journal of comparative neurology.