The connectional organization of neural systems in the cat cerebral cortex

BACKGROUND The mammalian brain consists of the cerebral cortical sheet, which is composed of many distinct areas, the cerebellar cortex, and many non-cortical nuclei. Powerful neuroanatomical techniques have revealed a large number of connections between these structures. The large number of brain structures and the very many connections between them form a strikingly complex network. The complexity of this network has made it difficult to understand how the central nervous system is organized. Recently, however, optimization analysis of an important subset of central nervous connections that occur between the different areas of the cerebral cortex has produced understandable and quantitative representations of the organization of cortical systems of the primate brain. RESULTS Here we briefly report the extension of this approach to the cortical systems of the cat. There were four connectional clusters of cortical areas in the cat. These clusters of areas corresponded to the visual, auditory, and somato-motor systems, and to the frontal and limbic areas, which we call the fronto-limbic complex. All the major sensory systems were hierarchically organized, and their 'higher' stations were more closely associated with the fronto-limbic complex than were their 'lower' stations. CONCLUSIONS Features of the organization of the cat brain, together with earlier primate results, suggest that there may be a common cortical plan in mammals. We suggest that this common plan may involve relatively discrete, hierarchically organized, cortical sensory systems and a topologically central fronto-limbic complex. Specific variations on this wiring plan may relate to evolutionary history and selection for particular ecological niches.

[1]  H. Burton,et al.  Second somatic sensory area in the cerebral cortex of cats: Somatotopic organization and cytoarchitecture , 1982, The Journal of comparative neurology.

[2]  R. Douglas,et al.  Opening the grey box , 1991, Trends in Neurosciences.

[3]  J. Price,et al.  Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat , 1977, The Journal of comparative neurology.

[4]  Yasuhiko Tamai,et al.  Eye movements following cortical stimulation in the ventral bank of the anterior ectosylvian sulcus of the cat , 1989, Neuroscience Research.

[5]  Giancarlo Tassinari,et al.  Visual and somatosensory integration in the anterior ectosylvian cortex of the cat , 1987, Brain Research.

[6]  C. Avendaño,et al.  Organization of the association cortical afferent connections of area 5: A retrograde tracer study in the cat , 1988, The Journal of comparative neurology.

[7]  Philip K. Maini,et al.  Experimental and Theoretical Advances in Biological Pattern Formation , 1993, NATO ASI Series.

[8]  Malcolm P. Young,et al.  Objective analysis of the topological organization of the primate cortical visual system , 1992, Nature.

[9]  C Blakemore,et al.  Stimulus selectivity and functional organization in the lateral suprasylvian visual cortex of the cat. , 1987, The Journal of physiology.

[10]  H. Groenewegen,et al.  Connections of the parahippocampal cortex. I. Cortical afferents , 1986, The Journal of comparative neurology.

[11]  C. Cavada,et al.  Topographical organization of the cortical afferent connections of the prefrontal cortex in the cat , 1985, The Journal of comparative neurology.

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

[13]  J. Price,et al.  Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat , 1977, The Journal of comparative neurology.

[14]  K. Tanaka,et al.  Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[15]  J. Kaas,et al.  Somatotopic organization of the third somatosensory area (SIII) in cats. , 1987, Somatosensory research.

[16]  Malcolm P. Young,et al.  Analysis and Modelling of the Organization of the Mammalian Cerebral Cortex , 1993 .

[17]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[18]  K. Rockland,et al.  Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey , 1979, Brain Research.

[19]  G. Mandl,et al.  Frontal ‘oculomotor’ area in alert cat. I. Eye movements and neck activity evoked by stimulation , 1978, Brain Research.

[20]  R. Dykes,et al.  Organization of primary somatosensory cortex in the cat. , 1980, Journal of neurophysiology.

[21]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. Kaas,et al.  The representation of the body surface in S-I of cats , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  R. Dykes,et al.  What Makes a Map in Somatosensory Cortex , 1986 .

[24]  R N Shepard,et al.  Multidimensional Scaling, Tree-Fitting, and Clustering , 1980, Science.

[25]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[26]  R. Reale,et al.  Patterns of cortico‐cortical connections related to tonotopic maps in cat auditory cortex , 1980, The Journal of comparative neurology.

[27]  S Shipp,et al.  Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physioligical and connectional study , 1991, Visual Neuroscience.

[28]  A. Rosenquist,et al.  Corticocortical connections among visual areas in the cat , 1984, The Journal of comparative neurology.

[29]  P. Goldman-Rakic,et al.  Preface: Cerebral Cortex Has Come of Age , 1991 .

[30]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[31]  L. Palmer,et al.  Retinotopic organization of areas 20 and 21 in the cat , 1980, The Journal of comparative neurology.