We used the autoradiographic tract-tracing method to define the amygdaloid projection fields after injecting 3H-amino acids into individual thalamic nuclei in the rat. The parvicellular division of the ventroposterior nucleus, the thalamic taste relay, projected lightly to the central and lateral amygdaloid nuclei. The central medial, interanteromedial, and paraventricular thalamic nuclei, viscerosensory relays of the thorax and abdomen, projected heavily to the amygdala. All projected to the basolateral amygdaloid nucleus, the paraventricular nucleus in addition having terminations in the central nucleus, the amygdaloid portion of the nucleus of the stria terminalis, and the amygdalohippocampal transition area. The magnocellular division of the medial geniculate, a thalamic auditory (and, to a moderate degree, a spinothalamic) relay, sent heavy projections to the central, accessory basal, lateral, and anterior cortical nuclei, and to the anterior amygdaloid area and the nucleus of the accessory olfactory tract. Other thalamic nuclei projecting to the amygdala, for which functions could not be associated, were the paratenial and subparafascicular nuclei. The former projected to the lateral, basal, and posterolateral cortical nuclei; the latter projected very lightly to the central, medial, and basal accessory nuclei. These results show that, like the cortical amygdaloid nuclei, which are sensory (olfactory) in nature, the subcortical amygdaloid nuclei must have major sensory functions. These thalamic afferents, when correlated with cortical and brainstem data from the literature, suggested that the amygdala is in receipt of sensory information from many modalities. To uncover the manner by which such information is processed by the amygdala and relayed to effector areas of the brain, six hypothetical mechanisms relating to modality specificity and convergence were posited. By charting sensory-related afferents to all subdivisions of the amygdala, each nucleus was characterized as to its mechanism of information processing. Four proposed amygdaloid systems emerged from this analysis. A unimodal corticomedial amygdaloid system relays pheromonal information from the accessory olfactory bulb to medial basal forebrain and hypothalamic areas. A second system--the lateral-basomedial--collects and combines input from a number of sensory modalities and distributes it to the same basal forebrain and hypothalamic areas as the corticomedial. The central system appears to concentrate the effect of viscerosensory information arriving from multiple brainstem, thalamic, cortical, and amygdaloid sources; this information is combined with significant auditory and spinothalamic inputs from the thalamus and cortex. The central system projects to lateral nuclei in the basal forebrain, hypothalamus, and brainstem.(ABSTRACT TRUNCATED AT 400 WORDS)

As part of an attempt to understand how sensory stimuli influence emotional processes we examined all of the telencephalic sensory systems of the rhesus monkey for efferents to the amygdala and immediately surrounding structures, using primarily the Fink-Heimer technique. The results support the following conclusions.1. All sensory systems contain areas that project to the amygdaloid complex (the somatosensory system, tentatively so), but not to more central limbic structures in the basal forebrain and hypothalamus. Consequently, whatever influence the sensory systems have on emotional processes mediated by these more central limbic structures is likely to depend largely on relays through the amygdala.2. Except for the olfactory system, the amygdalopetal projections arise only from the later stages of cortical processing within each sensory system, i.e., from the modality-specific association areas one or more steps removed from the primary sensory areas. Thus, the modality-specific cortical sources of the amygdalopetal projections, like their amygdaloid targets, are important links in the sensory-limbic pathways. These sources are: for vision, areas TE and ventral TG; for audition, anterior TA and dorsal TG; for taste, area IA; and for somesthesis, possibly areas IA or IB. The amygdalopetal sources thus occupy a limited territory that begins dorsally in the anterior insula and extends ventrally across the anterior temporal neocortex as far as the rhinal fissure.3. Within the visual system, progressively heavier and more widespread efferents arise from successively later stages of the amygdalopetal sources. The posterior half of TE sends a moderate projection to the dorsal part of the lateral nucleus, the anterior half of TE sends a heavy projection to the dorsal parts of both the lateral and basal nuclei, and the ventral part of TG sends a heavy projection to the dorsal and medial parts of the lateral and basal nuclei and to the dorsal part of the basal accessory nucleus. This pattern of progressive intensification and spread of the amygdalopetal projections applies also to the auditory system and probably to the other cortical sensory systems as well. The pattern suggests that a progressively greater influence on amygdaloid activity is exerted by successively more highly processed sensory information.4. The efferents to the amygdaloid complex from the different sensory systems terminate in a dovetailed pattern. The major amygdaloid targets are: for vision, the anterodorsal parts of the lateral, basal, and basal accessory nuclei; for audition, the posterior parts of the lateral and basal accessory nuclei; for taste, the medial parts of the lateral and basal nuclei; and for olfaction, the cortical and medial nuclei. This pattern implies that each part of the amygdala is under the major influence of a particular sensory system.Requests for reprints should be sent to Dr. Blair H. Wer.

Unilateral lateral hypothalamlic lesions in rats produce deficits in orientation to contralateral visucal, olfactory, whisker-toluch, and somatosetnsory stimuli. This syndrome of sensory neglect appears to be involved in some of the deficits in feedinig and attack which follow bilateral lateral hypothalamic lesions.

A study was made of the normal and experimental anatomy of the olfactory system of the young adult male rhesus monkey. The cytoarchitecture of the central olfactory areas was studied with cell and fiber stains, while the extent and pattern of the projections of the olfactory bulb were determined by the Fink-Heimer and autoradiographic methods. The brain of one animal that had sustained damage to the olfactory bulb two days prior to sacrifice, and of one that had a transection of the olfactory tract ten days prior to sacrifice, were processed with the Fink-Heimer technique. The first of these and four others received injections of 3H-proline or 3H-leucine into the olfactory bulb, and following a survival period of 18 hours, or 2, 4, 12, or 20 days, their brains were processed with the autoradiographic technique. The results were the same for both experimental methods and for all survival periods. The projections of the olfactory bulb in this microsmatic animal are entirely ipsilateral. All of the structures that receive direct olfactory afferents have a laminar organization except for the anterior olfactory nucleus, which is laminated only in its anterior, peduncular, portion. While the olfactory bulb projects to the entire extent and depth of the anterior olfactory nucleus, the olfactory afferents of all other structures are confined to layer IA of the plexiform layer. These structures are: all divisions of the olfactory tubercle; the frontal and temporal prepiriform cortices; the oral, medial, and dorsal divisions of the superficial amygdaloid nucleus; and polar and anterior entorhinal cortex. The rhesus monkey does not have a recognizable accessory olfactory bulb, and no projections were seen to one of its targets, the nucleus of the stria terminalis. Also, no projections were seen to the taenia tecta or the ventral division of the superficial amygdaloid nucleus. With these exceptions, the projections of the olfactory bulb in the rhesus monkey are similar to those in macrosmatic species.

The connections between the cerebral cortex and amygdala were studied in the rat by means of silver degeneration techniques. To help define the sites of origin and termination of cortico-amygdaloid connections, the architecture of the cortex and the amygdala was studied in sections from normal brains stained for cells, fibers, acetylcholinesterase activity, and heavy metals (Timm staining). The amygdalopetal cortex on the dorsal and lateral surfaces of the rat brain is limited to a narrow strip of periallocortex that forms the dorsal wall and lip of the rhinal sulcus. Histochemical stains indicate that this cortex comprises several stages of cortical differentiation that are intermediate between the ventrally adjacent allocortices and the dorsally adjacent neocortices. The lateral periallocortex consists of two major divisions, the agranular insula (area 13) anteriorly, and a temporal agranular cortex (areas 35 and 36) posteriorly. The principal amygdaloid target for this cortex is the lateral nucleus. Anterior area 13 and posterior area 35 project to the anterior and posterior halves, respectively, of the medial division of this nucleus, while posterior area 13 and anterior area 35 projects to the lateral division of this nucleus. All divisions of periallocortex also send projections to a part of the putamen that surrounds the lateral half of the central nucleus. All of area 13 also sends efferents to the anterior part of the basal nucleus, while the anterior half of area 13 sends an additional projection to the central nucleus. Comparison of these data with those obtained in the cat and monkey suggests that a constant feature of eutherian brains is the existence of a subset of efferents from each of the four neocortical sensory systems that is routed so as to provide subcortical limbic structures with modality-specific information. The initial sequence in this sensorilimbic system consists of one or more modality-specific corticocortical relays that originate in the primary sensory cortices and terminate in one of four topographically adjacent, modality-specific areas of the insular and temporal cortices. These insular and temporal areas then each establish modality-specific connections within the amygdaloid complex. The final set of relays presumably comprises the connection that each of these amygdaloid areas makes with the autonomic and endocrine nuclei of the brain.