Pyramidal Cells, Patches, and Cortical Columns: a Comparative Study of Infragranular Neurons in TEO, TE, and the Superior Temporal Polysensory Area of the Macaque Monkey

The basal dendritic arbors of layer III pyramidal neurons are known to vary systematically among primate visual areas. Generally, those in areas associated with "higher" level cortical processing have larger and more spinous dendritic arbors, which may be an important factor for determining function within these areas. Moreover, the tangential area of their arbors are proportional to those of the periodic supragranular patches of intrinsic connections in many different areas. The morphological parameters of both dendritic and axon arbors may be important for the sampling strategies of cells in different cortical areas. However, in visual cortex, intrinsic patches are a feature of supragranular cortex, and are weaker or nonexistent in infragranular cortex. Thus, the systematic variation in the dendritic arbors of pyramidal cells in supragranular cortex may reflect intrinsic axon projections, rather than differences in columnar organization. The present study was aimed at establishing whether cells in the infragranular layers also vary in terms of dendritic morphology among different cortical areas, and whether these variations mirror the ones demonstrated in supragranular cortex. Layer V pyramidal neurons were injected with Lucifer yellow in flat-mounted cortical slices taken from cytoarchitectonic areas TEO and TE and the superior polysensory area (STP) of the macaque monkey. The results demonstrate that cells in STP were larger, had more bifurcations, and were more spinous than those in TE, which in turn were larger, had more bifurcations and were more spinous than those in TEO. These results parallel morphological variation seen in layer III pyramidal neurons, suggesting that increasing complexity of basal dendritic arbors of cells, with progression through higher areas of the temporal lobe, is a general organizational principle. It is proposed that the differences in microcircuitry may contribute to the determination of the functional signatures of neurons in different cortical areas. Furthermore, these results provide evidence that intrinsic circuitry differs across cortical areas, which may be important for theories of columnar processing.

[1]  G. J. Romanes,et al.  The Neocortex of Macaca mulatta , 1948 .

[2]  D. Sholl.  Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953, Journal of anatomy.

[3]  Sholl Da.  Dendritic organization in the neurons of the visual and motor cortices of the cat. , 1953 .

[4]  V. Mountcastle,et al.  Neural mechanisms subserving cutaneous sensibility, with special reference to the role of afferent inhibition in sensory perception and discrimination. , 1959, Bulletin of the Johns Hopkins Hospital.

[5]  T. Powell,et al.  Morphological variations in the dendritic spines of the neocortex. , 1969, Journal of cell science.

[6]  D. B. Bender,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 1969, Science.

[7]  M. Carpenter.  The cerebral cortex , 1976 .

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

[9]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[10]  J. Szentágothai.  The modular architectonic principle of neural centers. , 1983, Reviews of physiology, biochemistry and pharmacology.

[11]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[12]  E. G. Jones.  Cerebral Cortex , 1987, Cerebral Cortex.

[13]  Keiji Tanaka,et al.  Polysensory properties of neurons in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. , 1988, Journal of neurophysiology.

[14]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  A. Larkman,et al.  Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. I. Establishment of cell classes , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[17]  A. Larkman.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: I. Branching patterns , 1991, The Journal of comparative neurology.

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

[19]  A. Larkman,et al.  Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions , 1991, The Journal of comparative neurology.

[20]  R. Porter,et al.  A fractal analysis of pyramidal neurons in mammalian motor cortex , 1991, Neuroscience Letters.

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

[22]  J. DeFelipe,et al.  The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs , 1992, Progress in Neurobiology.

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

[24]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[25]  K. Rockland,et al.  Specific and columnar projection from area TEO to TE in the macaque inferotemporal cortex. , 1993, Cerebral cortex.

[26]  M. Young.  The organization of neural systems in the primate cerebral cortex , 1993, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  R. Malach.  Cortical columns as devices for maximizing neuronal diversity , 1994, Trends in Neurosciences.

[28]  B. Seltzer,et al.  Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex , 1995, The Journal of comparative neurology.

[29]  Keiji Tanaka,et al.  Optical Imaging of Functional Organization in the Monkey Inferotemporal Cortex , 1996, Science.

[30]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[31]  R. Chase,et al.  Comparative morphology of three types of projection‐identified pyramidal neurons in the superficial layers of cat visual cortex , 1996, The Journal of comparative neurology.

[32]  E. Callaway,et al.  Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex , 1996, Nature.

[33]  Keiji Tanaka,et al.  Columnar Organization in the Inferotemporal Cortex , 1997 .

[34]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

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

[36]  I. Fujita,et al.  Contrasting forms of synaptic plasticity in monkey inferotemporal and primary visual cortices , 1997, Neuroreport.

[37]  Christof Koch,et al.  Biophysics of Computation: Information Processing in Single Neurons (Computational Neuroscience Series) , 1998 .

[38]  G. Elston,et al.  Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. , 1998, Cerebral cortex.

[39]  G. Elston,et al.  Complex dendritic fields of pyramidal cells in the frontal eye field of the macaque monkey: comparison with parietal areas 7a and LIP , 1998, Neuroreport.

[40]  Feedback cells in marmoset visual cortex: Laminar position, morphology and topography of V1-projecting pyramidal neurones , 1999 .

[41]  M G Rosa,et al.  Supragranular pyramidal neurones in the medial posterior parietal cortex of the macaque monkey: morphological heterogeneity in subdivisions of area 7. , 1999, Neuroreport.

[42]  G. Elston,et al.  Variation in the spatial relationship between parvalbumin immunoreactive interneurones and pyramidal neurones in rat somatosensory cortex. , 1999, NeuroReport.

[43]  G. Elston,et al.  Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[44]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[45]  Vivien A. Casagrande,et al.  Biophysics of Computation: Information Processing in Single Neurons , 1999 .

[46]  Morphological variation of MT-projecting cortical neurones in the marmoset monkey , 1999 .

[47]  G. Elston.  Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[48]  H. Barbas,et al.  The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. , 2000, Cerebral cortex.