Macaque monkey retrosplenial cortex: I. Three‐dimensional and cytoarchitectonic organization

This is the first in a series of reports on the neuroanatomic organization and connectivity of the macaque monkey retrosplenial cortex, i.e., areas 29 and 30. To elucidate the topographic configuration of the retrosplenial cortex and adjacent structures, we have made three‐dimensional computer reconstructions of the posterior cingulate region that includes the retrosplenial cortex. The largest portion of the posterior cingulate gyrus is located dorsal to the corpus callosum. At the caudal limit of the corpus callosum, the gyrus curves around the splenium, turns laterally and forms a region called the isthmus that links the cingulate and parahippocampal gyri. The isthmus contains the caudomedial lobule, which is a rostrally oriented bulge that is made up, in part, of portions of the retrosplenial cortex. To delineate the subdivisions of the retrosplenial and adjacent cortices, we conducted a cytoarchitectonic analysis by using cerebral hemispheres that were cut at oblique angles and stained with a variety of techniques, including immunohistochemistry for nonphosphorylated neurofilament protein. The dorsal bank of the callosal sulcus and the rostral surface of the isthmus are covered by the retrosplenial cortical areas 29l, 29m, and 30, whereas most of the medial surface of the posterior cingulate gyrus and the ventral bank of the posterior cingulate sulcus consist of areas 23i and 23e. The most caudoventral portion of the cingulate gyrus is composed of an area (area 23v) that resembles the retrosplenial and posterior cingulate cortices but has a much more prominent layer IV. On the dorsal bank of the calcarine sulcus, we also defined a transitional zone, area 30v, located between the retrosplenial cortex and the prestriate visual cortex. J. Comp. Neurol. 426:339–365, 2000. © 2000 Wiley‐Liss, Inc.

[1]  G. Smith,et al.  Die Cytoarchitektonik der Hirnrinde des erwachsenen Menschen. , 1927 .

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

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

[4]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[5]  D. Pandya,et al.  Cortico-cortical connections in the rhesus monkey. , 1969, Brain research.

[6]  D. Pandya,et al.  Efferent cortico-cortical projections of the prefrontal cortex in the rhesus monkey. , 1971, Brain research.

[7]  D. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents , 1975, Brain Research.

[8]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

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

[10]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[11]  L. Swanson The hippocampus — new anatomical insights , 1979, Trends in Neurosciences.

[12]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

[13]  B. Merker,et al.  Technical modifications of gallyas' silver stain for myelin , 1983, Journal of Neuroscience Methods.

[14]  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.

[15]  W. Cowan,et al.  A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[16]  D. Amaral,et al.  The distribution of acetylcholinesterase in the hippocampal formation of the monkey , 1984, The Journal of comparative neurology.

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

[18]  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.

[19]  D. Price,et al.  A modified histochemical technique to visualize acetylcholinesterase-containing axons. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[20]  K Zilles,et al.  Quantitative cytoarchitectonics of the posterior cingulate cortex in primates , 1986, The Journal of comparative neurology.

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

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

[23]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[24]  E Valenstein,et al.  Retrosplenial amnesia. , 1987, Brain : a journal of neurology.

[25]  P. Goldman-Rakic Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[26]  Mieke Verfaellie,et al.  Impaired acquisition of temporal information in retrosplenial amnesia , 1988, Brain and Cognition.

[27]  D. Amaral,et al.  Cholinergic innervation of the monkey amygdala: An immunohistochemical analysis with antisera to choline acetyltransferase , 1989, The Journal of comparative neurology.

[28]  E K Warrington,et al.  Selective impairment of memory and visual perception in splenial tumours. , 1991, Brain : a journal of neurology.

[29]  Karl J. Friston,et al.  Willed action and the prefrontal cortex in man: a study with PET , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[30]  I Akiguchi,et al.  [A case of retrosplenial amnesia]. , 1991, Rinsho shinkeigaku = Clinical neurology.

[31]  R. Pearson,et al.  The Human Nervous System. Basic Elements of Structure and Function , 1967, The Yale Journal of Biology and Medicine.

[32]  N Yanagisawa,et al.  [A case of cerebral infarction presenting as retrosplenial amnesia]. , 1992, Rinsho shinkeigaku = Clinical neurology.

[33]  [A case of topographical disturbance following a left medial parieto-occipital lobe infarction]. , 1992, Rinsho shinkeigaku = Clinical neurology.

[34]  D. Amaral,et al.  Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Alan C. Evans,et al.  Functional activation of the human frontal cortex during the performance of verbal working memory tasks. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Karl J. Friston,et al.  Functional mapping of brain areas implicated in auditory--verbal memory function. , 1993, Brain : a journal of neurology.

[37]  A case of verbal amnesia due to left retrosplenial lesion. , 1994 .

[38]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[39]  M. Mishkin,et al.  Stimulus recognition , 1994, Current Opinion in Neurobiology.

[40]  Richard S. J. Frackowiak,et al.  Brain regions associated with acquisition and retrieval of verbal episodic memory , 1994, Nature.

[41]  P M Grasby,et al.  Brain systems for encoding and retrieval of auditory-verbal memory. An in vivo study in humans. , 1995, Brain : a journal of neurology.

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

[43]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

[44]  B. Vogt,et al.  Chapter VIII Primate cingulate cortex chemoarchitecture and its disruption in Alzheimer's disease , 1997 .

[45]  N. Takahashi,et al.  Pure topographic disorientation due to right retrosplenial lesion , 1997, Neurology.

[46]  M. Buonocore,et al.  Activation of left posterior cingulate gyrus by the auditory presentation ofthreat-related words: an fMRI study , 1997, Psychiatry Research: Neuroimaging.

[47]  Anna Maria Di Betta,et al.  Retrograde amnesia in a patient with retrosplenial tumour , 1998 .

[48]  E. Kandel,et al.  Cognitive Neuroscience and the Study of Memory , 1998, Neuron.

[49]  L. Squire,et al.  Episodic memory, semantic memory, and amnesia , 1998, Hippocampus.

[50]  R. Maddock The retrosplenial cortex and emotion: new insights from functional neuroimaging of the human brain , 1999, Trends in Neurosciences.

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

[52]  N. Takahashi,et al.  Pure Topographical Disorientation Due to Right Posterior Cingulate Lesion , 1999, Cortex.