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. 2013 Aug;23(8):1901-22.
doi: 10.1093/cercor/bhs177. Epub 2012 Jun 26.

Contrasting Patterns of Cortical Input to Architectural Subdivisions of the Area 8 Complex: A Retrograde Tracing Study in Marmoset Monkeys

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Contrasting Patterns of Cortical Input to Architectural Subdivisions of the Area 8 Complex: A Retrograde Tracing Study in Marmoset Monkeys

David H Reser et al. Cereb Cortex. .
Free PMC article

Abstract

Contemporary studies recognize 3 distinct cytoarchitectural and functional areas within the Brodmann area 8 complex, in the caudal prefrontal cortex: 8b, 8aD, and 8aV. Here, we report on the quantitative characteristics of the cortical projections to these areas, using injections of fluorescent tracers in marmoset monkeys. Area 8b was distinct from both 8aD and 8aV due to its connections with medial prefrontal, anterior cingulate, superior temporal polysensory, and ventral midline/retrosplenial areas. In contrast, areas 8aD and 8aV received the bulk of the projections from posterior parietal cortex and dorsal midline areas. In the frontal lobe, area 8aV received projections primarily from ventrolateral areas, while both 8aD and 8b received dense inputs from areas on the dorsolateral surface. Whereas area 8aD received the most significant auditory projections, these were relatively sparse, in comparison with those previously reported in macaques. Finally, area 8aV was distinct from both 8aD and 8b by virtue of its widespread input from the extrastriate visual areas. These results are compatible with a homologous organization of the prefrontal cortex in New and Old World monkeys, and suggest significant parallels between the present pathways, revealed by tract-tracing, and networks revealed by functional connectivity analysis in Old World monkeys and humans.

Keywords: connections; frontal eye field; parietal cortex; prefrontal cortex; primate.

Figures

Figure 1.
Figure 1.
Examples of injection sites. Whereas examination of a single section only reveals part of the trajectory, these series of photomicrographs demonstrate the restricted lateral spread of the injection sites, and confirm that the white matter was not involved. (Left) Injection site in area 8b in case CJ83-DY. The photographs of the injection site (top two panels) were obtained in sections counterstained for myelin. The bottom panel illustrates a Nissl-stained section adjacent to the section where the injection site made the closest approach to the interface between cortex and white matter (A + 14.8). (Middle) Injection sites in area 8aD in case CJ108-FR. In this case, tracer was released along two parallel tracks, both of which were confined to area 8aD. Again, the Nissl-stained section (A + 14.6) corresponds to the level where the injection site was deemed closest to the white matter. (Right) Injection site in area 8aV in case CJ108-FE. This series of sections demonstrates that the injection site reached at least to layer 5 in this case; unfortunately, the section where the injection site was deemed deepest (A + 15.3) was damaged subsequent to plotting. Scale bars: 1 mm.
Figure 2.
Figure 2.
Two-dimensional reconstruction of the marmoset cortex, showing the areas defined by Paxinos et al. (2012) grouped into 15 anatomical and functional sectors (colors). This map, representing a right hemisphere (rostral to the right, ventral downwards), was prepared using the software suite CARET (Van Essen et al. 2001). To reduce the amount of distortion, discontinuities were introduced along the frontal pole and ventromedial convexity of the frontal lobe (thus separating portions of areas 10, 14, and 25), the temporal pole, and the fundus of the calcarine sulcus (thus separating portions of the primary visual area, V1 and area prostriata, ProSt). The red and green pairs of asterisks each indicate 2 adjacent points which became separated in the maps due to such discontinuities. Whereas this type of representation allows a global appreciation of the topological relationship between cortical areas, there are significant residual distortions (typically, areal expansion along the edges of the map). Thus, the scale bar (5 mm) is approximate. The abbreviations of areas containing labeled neurons following injections in areas 8aD, 8aV, and 8b are given in Table 2; for other abbreviations, see Paxinos et al. (2012).
Figure 3.
Figure 3.
Histological characteristics of areas 8b, 8aD, and 8aV in the marmoset. (Top) Section stained for myelin, using the Gallyas technique. (Bottom) Section stained for Nissl substance, using cresyl violet. The approximate locations of the boundaries are indicated by the arrowheads. The insert (upper right) indicates the level of these sections (approximately A + 15.5 mm). Scale bar (bottom left) = 500 µm.
Figure 4.
Figure 4.
Summary maps showing the distribution of labeled neurons following 4 injections of tracers in subdivisions of BA8. Each panel illustrates a 2-dimensional reconstruction prepared using CARET (Van Essen et al. 2001), using the same conventions as in Figure 2, including orientation (rostral to the right, ventral downwards) and the locations of the discontinuities used to reduce distortions. The gray shading represents curvature: Convex (outward-projecting) surfaces such as dorsal midline and the lips of the lateral fissure (lf) appear lighter than the gray background, whereas concave (inward-projecting) surfaces such as the banks of the lateral fissure appear darker than the background. Colored points represent individual neurons labeled with DY (yellow), FR (red), and FE (green), and the centers of the injection sites are indicated by black circles. For orientation, the locations of several areas containing labeled neurons are indicated (compare with the full reconstruction shown in Fig. 2). Other abbreviations: cal, calcarine sulcus; cc, corpus callosum; ips, intraparietal sulcus; sts, superior temporal sulcus. Scale bar = 5 mm.
Figure 6.
Figure 6.
(AO) Coronal sections illustrating the locations of labeled neurons (yellow–green points) relative to architectural boundaries of cortical areas, following a tracer injection in area 8b (case CJ83-DY). The injection site is indicated in black in (E). The gray lines indicate the boundaries of areas containing labeled neurons, with the approximate stereotaxic A–P levels shown in italicized numbers at the bottom left of each section. Abbreviations for subcortical labeled neurons (according to Paxinos et al. 2012): AM, anteromedial nucleus; APT/PLi, anterior pretectal nucleus and posterior limitans nucleus; AV, anteroventral nucleus; Cl, claustrum; CL, central lateral nucleus; CM, central medal nucleus; IAM, interanteromedial nucleus; MD, mediodorsal nucleus; MDC, caudal mediodorsal nucleus; MDL, lateral mediodorsal nucleus; MDM, medial mediodorsal nucleus; NBM, nucleus Basalis of Meynert; RT, reticular nucleus; ZIR, rostral zona incerta. The insert indicates the section levels in a lateral view of the right hemisphere. Scale bar (adjacent to O) = 2 mm.
Figure 5.
Figure 5.
Percentages of neurons labeled in different cortical sectors, following injections of retrograde tracers in areas 8b (top), 8aD (middle), and 8aV (bottom). Black, white, or gray bars label the data from different cases, and only extrinsic connections are shown. The abbreviations of the cortical sectors are: dlp, dorsolateral prefrontal cortex; vlp, ventrolateral prefrontal cortex; ofc, orbitofrontal cortex; mpc, medial prefrontal cortex; prm, premotor/motor cortex; acc, anterior cingulate cortex; ssc, somatosensory cortex; ins, insular cortex; aud, auditory cortex; lit, lateral/inferior temporal cortex; vtc, ventral temporal cortex; ppc, posterior parietal cortex; pcr, posterior cingulate/retrosplenial cortex; vis, visual cortex. Because no tracer-filled cells were observed in the olfactory cortex in any case, this sector is not represented in the graphs. See Figure 2 for the areas included in each sector.
Figure 7.
Figure 7.
(AC) Coronal sections illustrating the locations of labeled neurons (black squares) in the retrosplenial and calcarine cortices following a tracer injection in area 8b (case CJ74-FB). The approximate A–P levels are shown in italicized numbers to the right of each section. The insert indicates the section levels in a lateral view of the right hemisphere. Scale bar (adjacent to A) = 1 mm.
Figure 8.
Figure 8.
(AJ): Coronal sections illustrating the locations of labeled neurons (red circles) relative to architectural boundaries of cortical areas, following a tracer injection in area 8aD (case CJ108-FR). The injection site (formed by 2 parallel syringe tracks, see Fig. 1) is indicated in black in D. The gray lines indicate the boundaries of areas containing labeled neurons, with the approximate stereotaxic A–P levels shown in italicized numbers at the bottom left of each section. The insert indicates the section levels in a lateral view of the right hemisphere. Scale bar (below J) = 2 mm.
Figure 9.
Figure 9.
(AM) Coronal sections illustrating the locations of labeled neurons (green circles) relative to architectural boundaries of cortical areas, following a tracer injection in area 8aV (case CJ108-FE). The injection site is indicated in black in B and C. The gray lines indicate the boundaries of areas containing labeled neurons, with the approximate stereotaxic A–P levels shown in italicized numbers at the bottom left of each section. The insert indicates the section levels in a lateral view of the right hemisphere. Scale bar (adjacent to M) = 2 mm.
Figure 10.
Figure 10.
(AF) Coronal sections illustrating the locations of labeled neurons (yellow–green circles) relative to architectural boundaries of cortical areas, following a tracer injection in the area 8aV (case CJ75-DY). The injection site is indicated in black in the A. The gray lines indicate the boundaries of areas containing labeled neurons, with the approximate stereotaxic A–P levels shown in italicized numbers at the bottom left of each section. The insert indicates the section levels in a lateral view of the right hemisphere. Scale bar (adjacent to F) = 2 mm.
Figure 11.
Figure 11.
Summary of the afferent connections of the 3 areas comprising the BA8 complex in the marmoset. (Top) Medial, lateral, and ventral views of the brain, showing the cortical areas that send the principal projections to areas 8b, 8aD, and 8aV. The areas are coded according to the same color scale used in the bottom diagram, but only projections formed by >0.5% of the labeled neurons are represented. The assigned colors reflect the densest value of the 2 results for a projection from a given area (the results of case CJ94-DY, with an injection that invaded area 45, were not considered for this purpose). (Bottom) Results from individual cases, color-coded according to the percentage of labeled neurons, observed in the different areas (see scale on the far right). This format highlights the similarities between observations in 2 cases of injections in the same area, as well as differences between injections in the different areas (for abbreviations, see Tables 2 and 3). For ease of comparison, the boxes along each row (each corresponding to 1 area) are arranged in the same sequence as the areas are listed in Table 3.

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