Organization of the amygdalopetal projections from modality‐specific cortical association areas in the monkey

Abstract

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. 5. The same cortical areas that give rise to separate sensory channels to the amygdala send efferents that converge upon the perirhinal and prorhinal cortices, areas known to be a major source of input to the hippocampus. Consequently, both the amygdala and hippocampus can be activated by the same highly processed sensory information, a conclusion that may help to account for a recent finding that these two structures can substitute for each other in a mechanism for recognition memory.