Amygdalocortical Projections Research Articles

Amygdala: Eyes Wide Open

Summary A new study sheds light on how the amygdala contributes to social interactions by providing direct evidence for specialized visual neurons that selectively respond to seeing the eyes of another individual or making eye contact with them.

Differential modes of termination of amygdalothalamic and amygdalocortical projections in the monkey

The amygdala complex participates in multiple systems having to do with affective processes. It has been implicated in human disorders of social and emotional behavior, such as autism. Of the interconnected functional networks, considerable research in rodents and primates has focused on connections between the amygdala and orbitofrontal cortex (OFC). The amygdala projects to OFC by both a direct amygdalocortical (AC) pathway and an indirect pathway through mediodorsal thalamus. In the rat, retrograde tracer experiments indicate that the AC and amygdalothalamic (AT) pathways originate from separate populations, and may therefore convey distinctive information, although the characteristics of these pathways remain unclear. To investigate this issue in monkeys we made anterograde tracer injections in the basolateral amygdala complex (BLC; n = 3). Three distinctive features were found preferentially associated with the AT or AC pathways. First, AT terminations are large (average diameter = 3.5 microm; range = 1.2-7.0 microm) and cluster around proximal dendrites, in contrast with small-bouton AC terminations. Second, AT terminations form small arbors (diameter approximately 0.1 mm), while AC are widely divergent (often >1.0 mm long). The AT terminations features are reminiscent of large bouton, "driver" corticothalamic terminations. Finally, AC but not AT terminations are positive for zinc (Zn), a neuromodulator associated with synaptic plasticity. From these results we suggest that AC and AT terminations originate from distinct populations in monkey as well as in rodent. Further work is necessary to determine the degree and manner of their segregation and how these subsystems interact within a broader connectivity network.

Bihemispheric organization of amygdalo-cortical projections in the rat

Two fluorescent dyes were injected symmetrically into the prefrontal cortices of the left and right hemisphere. A consistent number of amygdaloid neurons was labeled from the injection in the contralateral cortex. Each nucleus of the basolateral amygdaloid complex showed a specific pattern of contralaterality. The highest degree of bihemisphericity was observed in the ventral basolateral nucleus. A significant number of neurons connected with the cortex of both hemispheres by means of axon collaterals was observed in the anterior basolateral nucleus. These anatomical findings indicate that the basolateral amygdaloid complex could act as subcortical link for interhemispheric communication.

Amygdaloid connections with posterior insular and temporal cortical areas in the rat

The connections of the amygdala with the insular and temporal cortices were examined by injecting wheat germ agglutinin conjugated to HRP (WGA-HRP) into the rat cortex. Following injections into the posterior agranular insular area (AIp) or perirhinal cortex (PR), bands of labeled neurons extending across nuclear boundaries were observed in the amygdala. These neuronal bands involved cells in the lateral, basolateral, and basomedial nuclei as well as the periamygdaloid cortex. Other nuclei of the corticomedial amygdala and the ventral endopiriform nucleus also exhibited retrogradely labeled cells. Anterograde label was observed in nuclei containing labeled neurons and in the central nucleus. Injections into gustatory, somatosensory, and auditory neocortical areas located dorsal to AIp and PR labeled small numbers of cells in the lateral and basolateral nuclei. Injections into AIp, PR, and, to a lesser extent, dorsally adjacent neocortical areas produced both retrograde and anterograde labeling in the contralateral amygdala. The main nuclei with contralateral insular and temporal projections are the basomedial nucleus, ventral endopiriform nucleus, and nucleus of the lateral olfactory tract. The contralateral central nucleus and to a lesser extent the lateral nucleus exhibited anterograde labeling. The pattern of retrograde labeling seen with injections at different rostrocaudal levels of the AIp-PR continuum indicates that amygdalocortical projections to these areas exhibit an overlapping topographical organization. Comparison of the results of this study with findings on amygdaloprefrontal cortical efferents suggests that amygdaloid projections to the entire fronto-insulo-temporal mesocortical field are topographically organized.

Amygdalohippocampal and amygdalocortical projections in the primate brain.

Several lines of evidence have supported the view that the amygdaloid complex plays a major role in the initiation and maintenance of temporal lobe or ‘psychomotor’ seizures. Chronic stereotaxic depth recordings in intractable epileptics, for example, have demonstrated striking correlations between amygdaloid epileptic discharges and the behavioral changes associated with seizures (Wieser, 1983). Electrical stimulation of the amygdaloid complex can also elicit experiences, such as illusions of perception or memory and emotions, such as fear, which are common manifestations of temporal lobe epilepsy (Gloor et al., 1982). Recent experimental models of temporal lobe epilepsy, such as the kindling paradigm (Le Gal La Salle, 1982) and the use of excitatory neurotoxins (Tremblay and Ben-Ari, 1984) have provided additional evidence that the amygdaloid complex and the closely associated hippocampal formation are particularly vulnerable to seizure-producing conditions. In fact, the amygdala and hippocampus are among the most commonly damaged structures in epileptic encephalopathy (Ounsted et al., 1966; Corsellis and Bruton, 1983). Given this context,it would be of obvious importance to determine the extent and organization of the interconnectivity of these two structures as well as their connections with cortical regions which are likely to subserve the perceptual and cognitive functions that are disrupted during seizures. It is only in the last several years, however, that these connections have been systematically studied.

Amygdaloid projections to the motor, premotor and prefrontal areas of the cat's cerebral cortex: A topographical study using retrograde transport of horseradish peroxidase

The topographic organization of the projections from the amygdaloid complex to the frontal (motor, premotor and prefrontal) cortex has been investigated in the cat by means of the horseradish peroxidase retrograde transport technique. While most of these projections arise from the magnocellular component of the basal nucleus, some arise also from other nuclei, such as the parvocellular basal nucleus, the corticoamygdaloid transition area and the cortical nucleus. The projections from the latter nuclei are directed to the central portions of the prefrontal cortex, both laterally and medially. No clear-cut topographic segregation appeared to exist in the distribution within the magnocellular basal nucleus of the cells of origin of projections to the motor, premotor and prefrontal cortex. The gross topographic arrangement of the amygdalocortical projections seems to reciprocate, to some extent at least, the organization of corticoamygdaloid projections from high-order sensory and polymodal association areas.

Amygdalo-cortical projections in the monkey (Macaca fascicularis).

Amygdalo-cortical projections were analyzed in the macaque monkey (Macaca fascicularis) in a series of experiments in which 3H-amino acids were injected into each of the major divisions of the amygdaloid complex and the anterogradely transported label was demonstrated autoradiographically. Projections to widespread regions of frontal, insular, temporal, and occipital cortices have been observed. The heaviest projections to frontal cortex terminated in medial and orbital regions which included areas 24, 25, and 32 on the medial surface and areas 14, 13a, and 12 on the orbital surface. Lighter projections were also seen in areas 45, 46, 6, 9, and 10. The heaviest projection to the insula terminated in the agranular insular cortex with a decreasing gradient of innervation to the more caudally placed dysgranular and granular insular areas. The projection to this region continues around the dorsal limiting sulcus to terminate in the somatosensory fields 3, 1-2, and SII. Essentially all major divisions of the temporal neocortex receive a projection from the amygdaloid complex with the most prominent projections ending in the cortex of the temporal pole (area TG) and the perirhinal cortex. The entire rostrocaudal extent of the inferotemporal cortex (areas TE and TEO) is also in receipt of an amygdaloid projection. While the rostral superior temporal gyrus (area TA) is heavily labeled in several of the experiments (with light labeling continuing into AI and adjacent auditory association regions) there was little indication of labeling in the caudal reaches of area TA. There was a surprisingly strong projection to prestriate regions of the occipital lobe and, in at least one case, clear-cut labeling in areas OB and 17. Labeling in the parietal cortex was primarily observed in the depths of the intraparietal sulcus. In all cortical fields, label was heaviest at the border between layers I and II and in some regions layers V and VI also had above background levels of silver grains.

Cortical substrates of taste aversion learning: Direct amygdalocortical projections to the gustatory neocortex do not mediate conditioned taste aversion learning

The gustatory neocortex (GN) receives direct projections from the lateral and basolateral amygdaloid nuclei. Amygdalocortical afferents ascend to the GN via the external capsule and the claustrum. The involvement of these amygdalocortical projections in conditioned taste aversion (CTA) learning was examined by producing lesions within the GN, the amygdaloid complex, or the external capsule and claustrum caudal to the GN. The complete destruction of amygdalocortical projections by lesions of the external capsule was verified following behavioral testing both by anterograde degeneration histology and by retrograde fluorescent transport experiments. Elimination of amygdalocortical input to the GN failed to significantly disrupt CTA acquisition, whereas lesions of the GN or amygdaloid complex produced reliable CTA learning impairments. These results are inconsistent with a current hypothesis which suggests that ascending amygdalocortical projections to the GN may mediate CTA learning.

The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat.

The mediodorsal nucleus of the rat thalamus has been divided into medial, central and lateral segments on the basis of its structure and axonal connections, and these segments have been shown by experiments using the autoradiographic method of demonstrating axonal connections to project to seven distinct cortical areas covering most of the frontal pole of the hemisphere. The position and cytoarchitectonic characteristics of these areas are described. The medial segment of the nucleus projects to the prelimbic area (32) on the medial surface of the hemisphere, and to the dorsal agranular insular area, dorsal to the rhinal sulcus on the lateral surface. The lateral segment projects to the anterior cingulate area (area 24) and the medial precentral area on the dorsomedial shoulder of the hemisphere, while the central segment projects to the ventral agranular insular area in the dorsal bank of the rhinal sulcus, and to a lateral part of the orbital cortex further rostrally. (The term "orbital" is used to refer to the cortex on the ventral surface of the frontal pole of the hemisphere.) A ventral part of this orbital cortex also receives fibers from the mediodorsal nucleus, possibly its lateral segment, but the medial part of the orbital cortex, and the ventrolateral orbital area in the fundus of the rhinal sulcus receive projections from the paratenial nucleus and the submedial nucleus, respectively. All of these thalamocortical projections end in layer III, and in the outer part of layer I. The basal nucleus of the ventromedial complex (the thalamic taste relay) has been shown to have a similar laminar projection (layer I and layers III/IV) to the granular insular area immediately dorsal to, but not overlapping, the mediodorsal projection field. However, the principal nucleus of the ventromedial complex appears to project to layer I, and possibly layer VI, of the entire frontal pole of the hemisphere. The anteromedial nucleus does not appear to project to layer III of the projection field of the mediodorsal nucleus, although it may project to layers I and VI, especially in the anterior cingulate and medial precentral areas. A thalamoamygdaloid projection from the medial segment of the mediodorsal nucleus to the basolateral nucleus of the amygdala has also been demonstrated, which reciprocates an amygdalothalamic projection from the basolateral nucleus to the medial segment. The habenular nuclei also appear to project to the central nucleus of the amygdala. These results are discussed in relation to the delineation and subdivision of the prefrontal cortex in the rat, and to amygdalothalamic and amygdalocortical projections which are described in a subsequent paper (Krettek and Price, '77).