Cingulate cortex of the rhesus monkey: I. Cytoarchitecture and thalamic afferents

Authors

  • Brent A. Vogt,

    1. Departments of Anatomy and Physiology, Boston University School of Medicine, Boston, Massachusetts 02118
    2. Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Massachusetts 01730
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  • Deepak N. Pandya,

    1. Departments of Anatomy and Physiology, Boston University School of Medicine, Boston, Massachusetts 02118
    2. Edith Nourse Rogers Memorial Veterans Hospital, Bedford, Massachusetts 01730
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  • Douglas L. Rosene

    1. Departments of Anatomy and Physiology, Boston University School of Medicine, Boston, Massachusetts 02118
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Abstract

The cytoarchitecture and thalamic afferents of cingulate cortex were evaluated in the rhesus monkey (Macaca mulatto). Area 24 has three divisions of which area 24a is adjacent to the callosal sulcus and has the least laminar differentiation. Area 24b has more clearly defined layers II, III, and Va, and area 24c, which forms the lower bank of the anterior cingulate sulcus, has a particularly dense layer III. Area 23 also has three divisions, each of which has a distinct layer IV. Area 23a is adjacent to the callosal sulcus and has the thinnest layers II–IV, which have the same cell density as layers V and VI. Area 23b has the largest pyramids in layers IIIc and Va, and area 23c, in the depths of the posterior cingulate sulcus, has the broadest external and thinnest internal pyramidal layers. Finally, areas 29 and 30 are located in the posterior depths of the callosal sulcus. Two divisions of area 29 are apparent: one with a granular layer directly adjacent to layer I (area 29a–c) and another with differentiation of layers III and IV (area 29d). Area 30 has a dysgranular layer IV.

Injections of the retrograde tracer horseradish peroxidase (HRP) were made into subdivisions of cingulate cortex in the monkey. Area 25 received thalamic input mainly from the midline parataenial (Pt), central densocellular (Cdc), and reuniens nuclei as well as from the dorsal parvicellular division of the mediodorsal nucleus (MDpc). A less dense projection also originated in the intralaminar parafascicular (Pf), central superior, and limitans (Li) nuclei as well as the medial division of the anterior nuclei (AM).

Areas 24a and 24b received most thalamic afferents from fusiform and multipolar cells in the Cdc and Pf nuclei with fewer from the ventral anterior (VA) and MDpc and MD densocellular (MDdc) nuclei and only minor input from AM. Most input to premotor cingulate area 24c appeared to originate in VA, MDdc, and Li.

Area 29 received the most dense input from nuclei traditionally associated with limbic cortex including the anteroventral (AV), anterodorsal (AD), and laterodorsal (LD) nuclei. Areas 23a and 23b, in contrast, did not receive AV, AD, or LD input, but the greatest proportion of their thalamic afferents arose in AM. Less-pronounced input also came from the lateroposterior (LP), medial pulvinar, and MDdc nuclei. This latter nucleus projected more to area 23b than to areas 30 or 23a.

Anterior medial nucleus efferents to cingulate cortex were of particular note for two reasons. First, AM projected primarily to posterior cingulate areas with area 23 receiving its principal thalamic input from AM. Second, projections to areas 30, 23a, and 23b were topographically organized with ventral areas 30 and 23a receiving from the central core of AM. While the more dorsally located area 23b received input from peripheral and medial.

In light of the extensive projections of Cds, Csl, and Pf to anterior cingulate cortex, it is proposed that the midline and intralaminar thalamic nuclie be classified as part of limbic thalamus along with the anterior, LD, and MD nuclei. Furthermore, although AM projects mainly to posterior cingulate cortex, it also has light projections to area 25 and minor input to area 24. As suhc, AM is the only limbic thalamic nucleus that has such widespread projections to cingulate cortex. Finally, visually evoked activity in area 23 may be the result of projections from the LP and medial pulvinar.

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