Organization of corticostriatal and corticoamygdalar projections arising from the anterior inferotemporal area TE of the macaque monkey: a Phaseolus vulgaris leucoagglutinin study

Abstract

Corticostriatal and corticoamygdalar projections arising from area TE of the macaque monkey were studied by focal injections of the anterograde tracer Phaseolus vulgaris leucoagglutinin into the dorsolateral and ventromedial subdivisions of the anterior TE (TEad and TEav, respectively). This approach yielded several new results. First, the global distributions of labeled terminals revealed that both TEad and TEav projected to the ventrocaudal striatum, including the tail of the caudate nucleus and the adjacent ventral putamen, and the dorsolateral aspect of the deep amygdaloid nuclei. TEav also projected to the medial basal nucleus of the amygdala and the ventral striatum. Second, the reconstructed single axons (n = 18) demonstrated that some axons originating from TEav or TEad projected simultaneously to the ventrocaudal striatum and the dorsolateral aspect of the deep amygdaloid nuclei by giving off collaterals. TEav axons projected to the medial basal nucleus of the amygdala also had collaterals projecting to the perirhinal cortex or area TG. And third, it was revealed that the axons originating from a focal TEav or TEad projected to a restricted territory (3.4-3.6 mm rostrocaudally) in the ventrocaudal striatum with four to six dispersed, rostrocaudally elongated, rod-like modules. Individual axons with multiple arbors innervated many of these modules. These findings add the evidence that the anterior part of TE is anatomically heterogeneous and suggest that the deep amygdaloid nuclei may be functionally dissociated, with the dorsolateral aspect more closely related to the ventrocaudal striatum and the medial basal nucleus more closely related to the perirhinal cortex.

Fig. 1.

PHA-L injection sites and labeling of axonal fibers in the white matter. A, Schematic brain diagrams illustrating PHA-L injection sites (filled circles) in the two TEad cases (Case 1 andCase 2, lateral view) and the two TEav cases (Case 3 and Case 4, bottom view).B, C, Photomicrographs showing PHA-L injection sites in coronal sections in a TEad case (B, case 1) and a TEav case (C, case 3). The two sections were counterstained for Nissl to identify the cortical layers.D, Camera-lucida drawing of a coronal section from case 4. PHA-L-labeled axonal fibers in the white matter circumscribed by theshaded rectangle are shown at higher magnification by a photomicrograph (bottom panel). The twoarrows indicate an axonal trunk that courses dorsally and terminates in the ventral putamen. The complete reconstruction of this axon (axon 4-1) is shown in Figure 15. The bundles of fibers on the right run dorsally and rostrally toward more rostrally located subcortical structures or cortical areas. amt, Anterior middle temporal sulcus; ot, occipitotemporal sulcus;pmt, posterior middle temporal sulcus;st, superior temporal sulcus; rh, rhinal sulcus; Amy, amygdala; Cd, caudate nucleus; Cl, claustrum; H, hippocampus;LV, lateral ventricle; Put, putamen. The same abbreviations for sulci are used in all figures unless otherwise stated. Scale bars: B, C, 1 mm;D, 0.2 mm.

Fig. 8.

Photomicrographs showing axonal fibers and terminals labeled after PHA-L injection into TEav (case 4). Four sections (113, 131, 147, 191) are illustrated at both low (left column) and high (right column) magnifications. Arrows in each pair of photomicrographs indicate identical locations. A, B, Proximal axonal trunk and an emerging branch (arrow) of axon 4-2 in the ventral putamen (for complete details, see Figs. 7, ar3, 9B). Note the differences in thickness and morphology between the smooth proximal axonal and the beaded branch with terminal swellings and varicosities (arrowheads inB). C, D, Distinctive terminal cluster in the ventral putamen, in which two arbors of two different axons were reconstructed (axon 4-2, Figs. 7, 9E,ar8; axon 4-1, Fig. 15, ar6). Thearrows indicate an emerging branch (of axon 4-1) coursing toward the densest part of the cluster. E, F, Arbor ar7 of axon 4-2 (Figs. 7, 9D) in the ventral putamen. G, H, Circumscribed terminal cluster within the lateral nucleus (L) of the amygdala. Arbor 10 of axon 4-2 (Figs. 7, 9F) was completely reconstructed in this cluster. L, Lateral nucleus of the amygdala; Put, putamen; WM, white matter. Scale bars: A, C, E, G, 100 μm; B, D, F, H, 50 μm.

Fig. 2.

Camera-lucida drawings of 13 coronal section outlines showing the distribution of PHA-L-labeled terminals in the ventrocaudal striatum (composed of the tail of the caudate nucleus and adjacent ventral putamen), the ventral striatum (composed of the nucleus accumbens, olfactory tubercle, and adjacent ventral part of the head of the caudate nucleus and ventral putamen), and the remaining parts of the striatum after TEav injection (case 3).Numbers indicate serial numbers of individual sections (40 μm thick); bottom section numbers indicate posterior sections. Section outlines are illustrated caudorostrally (A–N) at equal intervals (1.2 mm). Note the absence of labeled terminals at the level of the anterior commissure (E, F). AC, Anterior commissure; Cd, caudate nucleus; IC, internal capsule; NA, nucleus accumbens;OT, olfactory tubercle; Put, putamen.

Fig. 3.

Camera-lucida drawings of 7 coronal section outlines showing the distribution of PHA-L-labeled terminals in the ventrocaudal striatum after TEad injection (case 1).Numbers indicate serial numbers of individual sections (30 μm thick); bottom section numbers indicate posterior sections. Section outlines are illustrated caudorostrally (A–G) at equal intervals (0.6 mm). Abbreviations are the same as in Figure 2.

Fig. 11.

Camera-lucida reconstruction of axon 2-1 labeled by PHA-L anterogradely transported from TEad (case 2) to the ventrocaudal striatum and the dorsolateral aspect of the deep amygdaloid nuclei. This axon was serially reconstructed through 79 sections (section thickness, 35 μm). Abbreviations and conventions are the same as in Figure 7.

Fig. 4.

Camera-lucida drawings of 8 coronal section outlines showing the distribution of PHA-L-labeled terminals in the amygdala after TEav injection (case 3). Numbers indicate serial numbers of individual sections (40 μm thick); bottom section numbers indicate posterior sections. Section outlines are illustrated caudorostrally (A–H) at equal intervals (0.6 mm). AAA, Anterior amygdaloid area;AB, accessory basal nucleus; CE, central nucleus; COa, anterior cortical nucleus;En, endopiriform nucleus; L, lateral nucleus; LB, lateral basal nucleus; M, medial nucleus; MB, medial basal nucleus;NLOT, nucleus of the lateral olfactory tract;PAC, periamygdaloid cortex; Pir, piriform cortex; DAN, deep amygdaloid nuclei; Cd, caudate nucleus; Cl, claustrum; EC, entorhinal cortex; H, hippocampus; LV, lateral ventricle; Put, putamen; rh, rhinal sulcus.

Fig. 10.

Camera-lucida reconstruction of axon 4-3 labeled by PHA-L anterogradely transported from TEav (case 4) to the ventrocaudal striatum and the dorsolateral aspect of the deep amygdaloid nuclei. This axon was serially reconstructed through 177 sections (section thickness, 40 μm). AC, Anterior commissure. Other abbreviations and conventions are the same as in Figure 7.

Fig. 12.

Camera-lucida reconstruction of axon 4-4 labeled by PHA-L anterogradely transported from TEav (case 4) to the medial basal nucleus (MB) of the amygdala and the perirhinal cortex (area 36). This axon was serially reconstructed through 92 sections (section thickness, 40 μm). Note that the branch terminating in the medial basal nucleus does not encroach into other deep amygdaloid nuclei. 35, Area 35; 36r, rostral division of area 36; amt, anterior middle temporal sulcus. Other abbreviations and conventions are the same as in Figure 7.

Fig. 5.

Camera-lucida drawings of 6 coronal section outlines showing the distribution of PHA-L-labeled terminals in the amygdala after TEad injection (case 2). Numbers indicate serial numbers of individual sections (35 μm thick); bottom section numbers indicate posterior sections. Section outlines are illustrated caudorostrally (A–F) at equal intervals (0.7 mm). Note the absence of labeled terminals in the medial basal nucleus (MB). AC, Anterior commissure; BNM, basal nucleus of Meynert. Other abbreviations are the same as in Figure 4.

Fig. 6.

Schematic diagrams showing the projections of single axons from TEav (A) and TEad (B) to the striatum and amygdala. Theshaded areas in the amygdala indicate the relative locations of the projections to the lateral nucleus, lateral basal nucleus, and accessory basal nucleus, which are regarded as single projection zones (dorsolateral aspect of the deep amygdaloid nuclei) and are distinguished from the medial basal nucleus (see Results).Arrows with bifurcating branches indicate axons with collaterals that terminate in two or more subcortical structures or cortical areas. Other arrows show axons that arborize within a single subcortical structure or cortical area.Shaded arrows show the projections from TEav and TEad to the perirhinal cortex (areas 35 and 36) and area TG, which have been described in detail in another paper (Saleem and Tanaka, 1996). Those axon collaterals that project further to other structures are not shown (see Results). AB, Accessory basal nucleus;CE, central nucleus; L, lateral nucleus;LB, lateral basal nucleus; MB, medial basal nucleus; 35/36, areas 35 and 36 of the perirhinal cortex; TG, area TG.

Fig. 7.

Camera-lucida reconstruction of axon 4-2 labeled by PHA-L anterogradely transported from TEav (case 4) to the ventrocaudal striatum and the dorsolateral aspect of the deep amygdaloid nuclei. Thick lines represent the main axonal trunk and collaterals, and thin lines represent terminal arbors. Numbers indicate serial numbers of individual sections; smaller numbers are posterior. This axon was serially reconstructed through 103 sections (section thickness, 40 μm). Ten terminal arbors (ar1–ar10) were drawn; each arbor is presented with a range of sections (numbers inparentheses), from which the arbor was completely reconstructed. Sections in which the axon gives off major collaterals are indicated by section numbers andarrows. Dashed lines (with sectionnumbers) indicate borders between different structures. The global locations of terminal arbors are illustrated in low-magnification camera-lucida drawings of selected sections, where terminal clusters containing individual arbors are circumscribed byshaded ellipses or circles. Double lines indicate the incomplete portion of the axon. The main axonal trunk in the white matter was followed to the injection site.AB, Accessory basal nucleus; CE, central nucleus; L, lateral nucleus; LB, lateral basal nucleus; MB, medial basal nucleus;Amy, amygdala; Cd, caudate nucleus;Cl, claustrum; GPe, external globus pallidus; H, hippocampus; LV, lateral ventricle; Put, putamen; WM, white matter; rh, rhinal sulcus. Orientation:M, medial; L, lateral; D, dorsal; V, ventral. The same conventions and abbreviations are used for illustrating other reconstructed axons unless otherwise noted.

Fig. 9.

Six completely reconstructed arbors of axon 4-2 (A–F; see Fig. 7 for their global locations). Note the morphological details of varicosities and terminal swellings, presumably synaptic boutons.

Fig. 13.

Camera-lucida reconstruction of axon 4-5 labeled by PHA-L anterogradely transported from TEav (case 4) to the medial basal nucleus (MB) of the amygdala, the perirhinal cortex (area 36), and area TG. This axon was serially reconstructed through 166 sections (section thickness, 40 μm). Double lines show incomplete portions of the axon. 36p, Polar division of area 36; 36r, rostral division of area 36; TG, area TG; st, superior temporal sulcus. Other abbreviations and conventions are the same as in Figure7.

Fig. 14.

Camera-lucida reconstruction of axon 1-1 labeled by PHA-L anterogradely transported from TEad (case 1) to the ventrocaudal striatum. This axon was serially reconstructed through 112 sections (section thickness, 30 μm). Double linesindicate the incomplete portion of the axon. Abbreviations and conventions are the same as in Figure 7.

Fig. 15.

Camera-lucida reconstruction of axon 4-1 labeled by PHA-L anterogradely transported from TEav (case 4) to the ventrocaudal striatum. This axon was serially reconstructed through 58 sections (section thickness, 40 μm). Abbreviations and conventions are the same as in Figure 7.

Fig. 16.

Camera-lucida reconstruction of axon 3-7 labeled by PHA-L anterogradely transported from TEav (case 3) to the dorsolateral aspect of the deep amygdaloid nuclei. This axon was serially reconstructed through 101 sections (section thickness, 40 μm). Note that although this axon innervates most of the dorsolateral aspect of the deep amygdaloid nuclei, it avoids encroaching into the medial basal nucleus (MB). Abbreviations and conventions are the same as in Figure 7.

Fig. 17.

Camera-lucida reconstruction of axon 2-2 labeled by PHA-L anterogradely transported from TEad (case 2) to the dorsolateral aspect of the deep amygdaloid nuclei and the basal nucleus of Meynert. This axon was serially reconstructed through 38 sections (section thickness, 35 μm). BNM, Basal nucleus of Meynert. Other abbreviations and conventions are the same as in Figure7.

Fig. 18.

Camera-lucida reconstruction of axon 3-2 labeled by PHA-L anterogradely transported from TEav (case 3) to the ventral striatum. This axon was serially reconstructed through 197 sections (section thickness, 40 μm). Cd, Caudate nucleus;IC, internal capsule; NA, nucleus accumbens; OT, olfactory tubercle; Put, putamen. Other abbreviations and conventions are the same as in Figure7.

Fig. 19.

Multiple rod-like modules of the terminal field and the distribution of terminal arbors of 3 completely reconstructed axons in the ventrocaudal striatum after PHA-L injection into TEav (case 4). Numbers indicate serial numbers of individual sections (40 μm thick); bottom section numbersindicate posterior sections. A, Camera-lucida drawings of 11 coronal section outlines showing axonal terminals in the ventrocaudal striatum. Each rostrocaudally elongated rod-like module is illustrated in a different color. Six rods were observed in this case.B, Distribution of terminal arbors of 3 reconstructed axons [axon 4-1 (red), axon 4-2 (green), and axon 4-3 (yellow); see Figs. 7, 10, 15 for details of the 3 axons) in the terminal fields identical to those shown inA. Note that the arbors of the 3 axons innervated 5 of 6 rods, sparing only 1 rod (shown in brown inA). Cd, Caudate nucleus;Cl, claustrum; Put, putamen.