Topography, cytoarchitecture, and cellular phenotypes of cortical areas that form the cingulo‐parahippocampal isthmus and adjoining retrocalcarine areas in the monkey

The monkey cingulo‐parahippocampal isthmus was identified recently in the depths and lateral bank of the anterior calcarine fissure but was not characterized fully. Cytoarchitectonic and immunohistochemical results presented here reveal that the isthmus is composed of four cortical areas. These include the presubiculum of the isthmus (PrSi), parasubiculum of the isthmus (PaSi), area 29 of the isthmus (area 29i) and area prostriata (Pro), which has anterior (Pro‐a) and posterior (Pro‐p) divisions. The PrSi, characterized by dense calbindin+ (CB+) neuropil in layer III, merges with area 29i at approximately the middle portion of the isthmus; the latter lacking the CB+ neuropil. The PaSi, characterized by a cell‐free lamina dissecans and light parvalbumin+ labeling, is observed in the ventral isthmus. The Pro, located posterior to area 29i and PaSi, and anterior to area 17, has an incipient layer IV, but the density of granule cells gradually increase toward area 17. Pro‐a has an incipient layer IV, contains few SMI‐32+ neurons, and adjoins area 30 dorsally. The latter also has an incipient layer IV but contains, in contrast, more SMI‐32+ neurons. Pro‐p has a clear but thin layer IV, contains a small number of SMI‐32+ neurons, and adjoins both area 23 and area 18 dorsally and area 18 ventrally. Compared with Pro‐p, area 23 contains many more SMI‐32+ neurons, whereas area 18 contains far more SMI‐32+ neurons. These findings reveal that the isthmus is a key cortical zone connecting both the cingulate and parahippocampal gyri, but also the limbic and visual cortices. Emphasizing the former only, which has been the tendency historically, underestimates the anatomic complexity of the isthmus, and likely, its functional correlates. J. Comp. Neurol. 456:184–201, 2003. © 2002 Wiley‐Liss, Inc.

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

[2]  I N FILIMONOFF,et al.  A rational subdivision of the cerebral cortex. , 1947, Archives of neurology and psychiatry.

[3]  D. Amaral,et al.  The entorhinal cortex of the monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[4]  D. V. van Essen,et al.  The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  E. Schäfer.  The spinal Cord and Brain , 1893 .

[6]  F. Sanides.  7 – Representation in the Cerebral Cortex and Its Areal Lamination Patterns , 1972 .

[7]  B. Vogt,et al.  Cytology of human caudomedial cingulate, retrosplenial, and caudal parahippocampal cortices , 2001, The Journal of comparative neurology.

[8]  K. Rockland,et al.  Parvalbumin immunoreactive Cajal-Retzius and non-Cajal-Retzius neurons in layer I of different cortical regions of human newborn , 2000, Anatomy and Embryology.

[9]  M. Petrides,et al.  Architectonic analysis of the human retrosplenial cortex , 2000, The Journal of comparative neurology.

[10]  Modular organization of the monkey presubiculum , 2001, Experimental Brain Research.

[11]  K. Rockland,et al.  Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas , 2000, The Journal of comparative neurology.

[12]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

[13]  H. Barbas,et al.  Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey , 1995, Hippocampus.

[14]  F Mauguiere,et al.  Anatomical evidence for medial pulvinar connections with the posterior cingulate cortex, the retrosplenial area, and the posterior parahippocampal gyrus in monkeys , 1985, The Journal of comparative neurology.

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

[16]  P. Goldman-Rakic,et al.  Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey , 1984, Neuroscience.

[17]  J. Morrison,et al.  Neurofilament and calcium‐binding proteins in the human cingulate cortex , 1997, The Journal of comparative neurology.

[18]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[19]  D. Pandya,et al.  Parietal, temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study , 1994, The Journal of comparative neurology.

[20]  D L Rosene,et al.  Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents , 1987, The Journal of comparative neurology.

[21]  M Petrides,et al.  Architecture and connections of retrosplenial area 30 in the rhesus monkey (macaca mulatta). , 1999, The European journal of neuroscience.

[22]  Douglas L. Rosene,et al.  The Hippocampal Formation of the Primate Brain , 1987 .

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

[24]  B. Vogt,et al.  Retrosplenial cortex in the rhesus monkey: A cytoarchitectonic and golgi study , 1976, The Journal of comparative neurology.

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

[26]  B. Berger,et al.  Retrosplenial/presubicular continuum in primates: a developmental approach in fetal macaques using neurotensin and parvalbumin as markers. , 1997, Brain research. Developmental brain research.

[27]  K. Rockland,et al.  Localization of area prostriata and its projection to the cingulate motor cortex in the rhesus monkey. , 2000, Cerebral cortex.

[28]  Jelliffe.  Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .