Variations in the structure of the prelunate gyrus in Old World monkeys

Abstract

Anatomical and electrophysiological studies have revealed a complex organization in the macaque prelunate gyrus. We investigated the morphology and architecture of the prelunate gyrus in Old World monkeys. In Macaca nemestrina, we observed a sulcus crossing the prelunate gyrus within 2 mm of the vertical meridian representation. In other macaque species and other cercopithecines, we observed substantial variations in sulcal morphology across the prelunate gyrus. We did not find a sulcus in all species, and the location and depth of that indentation on the gyrus varied among species. A deep sulcus was observed in all species that emerged earlier in evolution than macaques, such as guenons, baboons, and colobines. We analyzed the regional and parcellation features of the prelunate gyrus in three macaque species, M. maura, M. mulatta, and M. radiata, and in Erythrocebus patas, with emphasis on the relation of structure to the distribution of prelunate visual areas. Nonphosphorylated neurofilament protein immunoreactivity permitted the delineation of a novel area in the prelunate gyrus of Old World monkeys, located around the prelunate sulcus. Species-specific patterns were also observed in the prelunate gyrus of the patas monkey compared to macaques. These observations, as well as a cladistic analysis of the data, suggest an expanded and diversified organization of the prelunate gyrus in some cercopithecoids that may reflect adaptation to specific ecological environments. It was, however, progressively lost in most macaques, being retained only in species that diverged early in the evolution of the genus Macaca, such as M. nemestrina and M. maura.

Fig. 1

Location of the prelunate gyrus (arrow) in M. mulatta. All photographs of the parasagittal sections shown on panels A–E were taken from www.brainmaps.org (case RH12). (A) Section 42: 20.9 mm, (B) section 115: 18.0 mm, (C) section 165: 16.0 mm, (D) section 210: 14.2 mm, and (E) section 275: 11.6 mm. Posterior is to the left, anterior to the right. st, superior temporal sulcus; lu, lunate sulcus. Scale bar = 2 cm.

Fig. 2

Variation in the general morphology of the prelunate gyrus and sulcus on lateral views of brain blocks from several monkey species. We refer to a sulcus within 2–3 mm medial to the intersection of the lateral and superior temporal sulci as the "prelunate sulcus" (arrow). Careful examination of the existence and shape of a prelunate sulcus crossing the prelunate gyrus revealed a deep indentation (arrows), a shallow sulcus or only a slight dimple on the surface or footprints of a blood vessel (arrowheads). (A) M. nemestrina, (B, C) M. maura, (D–F) M. mulatta, (G) M. fascicularis, (H, I) M. radiata, (J) P. anubis, (K, L) E. patas. Note that the sulcus is more marked in P. anubis and E. patas compared to the macaques (except in F), which show more variability in its occurrence. Panel A is a superior view of the brain and the other panels show lateral views. st, superior temporal sulcus; lu, lunate sulcus.Scale bar = 1 cm.

Fig. 3

Schematic representation of the prelunate gyrus in M. nemestrina. The insets at the top of each column illustrate dorsal reconstructions of the prelunate gyrus in the left (monkey PO-L) and the right (monkey BR-R shown in Fig. 2A, see also Fig. 4) hemispheres of two animals, with the indication of three parasagittal sections (1–3) through the prelunate sulcus. The line drawings (1–3 or lateral to medial respectively) show the outlines of the cortex throughout the prelunate sulcus with the location of layer IV. The dashed lines represent the course of layer IV in the striate cortex. For case PO-L (left column), the sections are 0.5 mm apart, whereas for case BR-R (right column) sections 1 and 2 are 1.5 mm apart, and sections 2 and 3 are 1 mm apart. lu, lunate sulcus; pl, prelunate sulcus; po, parieto-occipital sulcus; st, superior temporal sulcus. Scale bar = 1 mm.

Fig. 4

The prelunate gyrus in the right hemisphere of M. nemestrina (case BR-R, see also Fig. 3). (A) Dorsal reconstruction of the prelunate gyrus from case BR-R with the indication of four parasagittal sections throughout the prelunate gyrus (B–E). (B–E) Gallyas-stained sections illustrate a differential staining pattern throughout the prelunate gyrus at the different lateral (B) to medial (E) levels shown in A. In panel C the staining pattern is clearly different at the left and right sides of the black arrow that points to the vertical meridian representation (see also panel A, dashed line). Panel C illustrates clearly where the prelunate sulcus is buried in the anterior bank of the superior temporal sulcus. (A) Medial is to the left, lateral to the right, (B–E) Anterior is to the left, posterior to the right. ip, intraparietal sulcus; lu, lunate sulcus; pl, prelunate sulcus; st, superior temporal sulcus; vm, vertical meridian representation. Scale bar = 2 mm.

Fig. 5

The prelunate gyrus in M. mulatta, case JU-L (A–D), case HE-L (E–H) and case KO-R (I–L) illustrating sulcal variations. (A) Photograph of a dorsal view of the prelunate sulcus (arrow) crossing the prelunate gyrus of case JU-L. (B–D) Three consecutive parasagittal Nissl-stained sections through the prelunate gyrus illustrating the presence of a shallow prelunate sulcus (arrow). (E) Parasagittal Nissl-stained section showing the crown of the prelunate gyrus of case HE-L. (F, G) The prelunate sulcus is very deep (arrow). (H) The prelunate sulcus is no longer visible on the cortical surface but still reflected at the level of layer IV. (I–L) Four parasagittal Nissl-stained sections from case KO-R showing a shallow sulcus medially on the prelunate gyrus (arrow). (A) Medial is to right, lateral to the left, (B–L) posterior is to the right, anterior to the left, (B, E, I) top panels showing the most lateral sections from all cases respectively. lu, lunate sulcus; st, superior temporal sulcus. Scale bar = B–D = 2 mm, E–L = 4 mm.

Fig. 6

Cytoarchitecture of the prelunate gyrus in M. maura (A–E) and M. mulatta (F–J). (A) A Nissl-stained section cut parallel to the long axis of the prelunate gyrus of the Moor’s monkey clearly demonstrates the presence of a sulcus (asterisk in A, see also Fig. 2B), and a dimple (star in A). (B–E) High-power photomicrographs of panel A showing the laminar organization pattern along the prelunate gyrus. (F) A Nissl-stained section cut parallel to the long axis of the prelunate gyrus in the rhesus monkey illustrates one deep indentation ventrally in the prelunate gyrus (asterisk in G, see also Fig. 2E). The laminar cytoarchitecture of the prelunate gyrus in the rhesus macaque is outlined in panels G–J. Lateral is to the left, medial to the right. Arrows link the position of higher magnification panels to the overview in A. The scale bar on E = 500 µm (A) and 120 µm (B–E); the scale bar on F = 500 µm; the scale bar on J = 150 µm (G–J).

Fig. 7

Cytoarchitecture of the prelunate gyrus in M. radiata (A–D) and E. patas (E–H). (A) Overview of a Nissl-stained section cut parallel to the long axis of the prelunate gyrus in the bonnet monkey (see Fig. 2H) illustrates a very shallow dimple in the cortical surface due to the imprint of a blood vessel (C). High-power photomicrographs ventral (B) and dorsal (D) to the dimple reveal the laminar architecture along the prelunate gyrus. (E) Overview of a Nissl-stained section cut parallel to the long axis of the prelunate gyrus in the patas monkey (see Fig. 2K) showing a deep indentation corresponding to the prelunate sulcus (G; asterisk in E). Panels F and H differ in cell packing and columnar structure compared to the laminar patterns in the three macaque species (Fig 6A–E, 6F–J, Fig 7A–D). Lateral is to the left, medial to the right. Arrows link the position of higher magnification panels to the overview in A. The scale bar on D = 500 µm (A) and 130 µm (B–D); the scale bar on E = 500 µm; the scale bar on H = 200 µm (F–H).

Fig. 8

Expression of neurofilament protein along the prelunate gyrus in M. maura. (A) Immunoreactive pyramidal neurons are mainly found in layers II, III, and V. Arrowheads indicate the boundary between the intermediate area on the left and area DP on the right side. (B, J) Area V4 is specifically characterized by layer II SMI-32-immunoreactive pyramidal neurons. The ventral sulcus (A, D, asterisk) is located within the intermediate area (IA; A, C–E), which mainly contains SMI-32-immunoreactive neurons in layers II (H, I), III (J) and V (L, M). A star in A and F marks a dorsal indentation in area DP (A, F–G). In area DP, large, intensely labeled neurons are present in layer III (G, K), whereas lightly labeled SMI-32-immunoreactive cells populate layer V and VI (G, N). Lateral is to the left, medial to the right. The higher magnification panels are indicated by arrows, and corresponding letters, pointing to their locations in the overview or at intermediate power; this convention is valid for Figures 8–11. IA, intermediate area. The scale bar on G = 900 µm (A) and 120 µm (B–G); the scale bar on N = 60 µm (H–K) and 30 µm (L–N).

Fig. 9

Regional and laminar distribution profile of SMI-32 immunoreactivity along the prelunate gyrus in M. mulatta. The overview panel (A, arrowheads) illustrates the borders of area V4 (B), the intermediate area (C–E) and area DP (F). The location of the sulcus in area V4 (A, B, asterisk) is more ventral compared to the location of the indentations in other macaque species, and it was more marked anteriorly than posteriorly (see also Fig 2B, 2E, 2H, Fig 8A and Fig 10A). For comparison, the apparent number and staining intensity of neurofilament protein-immunoreactive neurons in layer II drastically changes from area V4 (B, G), towards the intermediate area (C–E, H–I) and into area DP (F). Differences in the staining profile of SMI-32-immunoreactive layer V cells along the prelunate gyrus are illustrated in detail between the intermediate area (J, K) and area DP (L). Lateral is to the left, medial to the right. The scale bar on F = 500 µm (A) and 130 µm (B–F); the scale bar on L = 30 µm (G–L).

Fig. 10

Expression of neurofilament protein in the prelunate gyrus of M. radiata. (A) Low-power photomicrograph of the cortical surface along the axis of the prelunate gyrus showing the SMI-32 immunoreactivity pattern in the intermediate area around a very shallow dimple (see also Fig. 2H). Higher-power photomicrographs of the regional differences for SMI-32 immunoreactivity illustrating the borders between the three visual areas, area V4 (B, G), the intermediate area (C–E, H, K), and area DP (F), which are mainly defined by differences in layer II and V neurofilament protein-immunoreactive pyramidal neurons (see also panel A). Similarly, a differential staining profile of pyramidal cells and their apical dendrites is also clearly visible in layer III of the intermediate area (C–E, I) and area DP (F, J). Note that only layer V of the intermediate area contains darkly labeled large pyramidal neurons with apical dendrites crossing the upper layers (A, C–E, K). Lateral is to the left, medial to the right. The scale bar on F = 500 µm (A) and 130 µm (B–D); the scale bar on K = 500 µm; the scale bar on H = 200 µm (F–H).

Fig. 11

Neurofilament protein immunoreactivity in the prelunate gyrus of E. patas. (A) Generally, layers II, III, and V throughout the prelunate gyrus are moderately populated with SMI-32-immunoreactive pyramidal neurons. SMI-32 labeling shows variation in the laminar and cellular distribution patterns, revealing the borders between area V4 (B), the intermediate area (C–D) and area DP (E; see arrowheads). Immunoreactive neurons are prominent in layer II of area V4 (F), but a gradual decrease in the number of layer II cells occurs in the intermediate area (C–D, G), whereas area DP contains no immunoreactivity in layer II (E). Layer III is quite homogeneously stained for SMI-32 across area V4 (H), the intermediate area (I), and area DP (J). Intensely labeled layer V pyramidal cells with very long apical dendrites penetrating into layer II (N; another such neurons is visible on the right side of panel D), clearly demarcate the intermediate area (M) from abutting areas V4 (K) and DP (L). Asterisks indicate the deep indentation referred to as the prelunate sulcus located in the intermediate area (A, C, see also Fig. 2K). Lateral is to the left, medial to the right. The scale bar on A = 500 µm; the scale bars on B, C, D, E 200 µm; the scale bar on N = 40 µm (F–J, N); the scale bar on M = 40 µm (K–M).

Fig. 12

Overview of the expression profile of neurofilament protein in posterior sections of the prelunate gyrus in M. maura (A–D), M. mulatta (E–G), M. radiata (H–J), E. patas (K–N). SMI-32 immunoreactivity clearly illustrates the differential staining patterns along the prelunate gyrus and the SMI-32-immunoreactive patterns in layers II, III and V resemble the characteristic profiles from the anterior sections in the prelunate gyrus from all species (Fig 8–Fig 11). Arrowheads indicate the borders between abutting areas V4 (A, E, H, K), the intermediate area (B–C, F–G, I, L–M) and area DP (D, G, J, N). An asterisk indicates the location of the prelunate sulcus, and stars indicate shallow dimples. The sulcus was more marked anteriorly than posteriorly in the rhesus monkey depicted here (see also Fig 2E and Fig 9A,B). Lateral is to the left, medial to the right. The scale bar on D = 100 µm (A–D); the scale bar on G = 300 µm (E–G); the scale bar on J = 200 µm (H–J); the scale bar on N = 200 µm (K–N).

Fig. 13

Localization of the prelunate gyrus and prelunate sulcus (arrows) on a superior view of the brain of a M. nemestrina (A). Panels B–E show lateral surface renderings of the common boundaries of areas V4, IA, and DP based on SMI-32 immunohistochemistry in M. maura (B), M. mulatta (C), M. radiata (D), and E. patas (E). Note the location of the prelunate sulcus, when present, in respect to the extent of the intermediate area and its border with area V4. cs, central sulcus; ip, intraparietal sulcus, st, superior temporal sulcus; lu, lunate sulcus. Scale bar = 1 cm for all panels.

Fig. 14

Cladistic analysis of the prelunate sulcus in the available sample. The character states were mapped onto the phylogeny of cercopithecoids provided by Tosi et al. (2003), and a maximum parsimony reconstruction was performed. The most recently diverged macaque species, like M. radiata and M. arctoides in our series lack the trait, and it is equivocal in M. mulatta and M. fascicularis. The nemestrina-Sulawesi clade, however, consistently retains the trait that is seen in all other cercopithecoids investigated. The numbers above some ancestral nodes indicate divergence from present in millions of years (Morales and Melnick, 1998; Tosi et al., 2003). The panels at right show example of the character state in the four species that were analyzed by immunohistochemistry. A true sulcus is indicated by an arrow and a shallower indentation by an arrowhead.