Thalamoamygdaloid projections in the rat: A test of the amygdala's role in sensory processing

Abstract

We used the autoradiographic tract‐tracing method to define the amygdaloid projection fields after injecting 3 H‐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. The final system—the basolateral—is a unimodal relay of viscerosensory information from the thalamus to the central nucleus of the amygdala and to the lateral basal forebrain. We argue that all sensory information sorted and restructured by the amygdala to form these systems is distributed directly or indirectly (via a synapse in the basal forebrain or hypothalamus) to diverse brainstem effector mechanisms, an expansion of Nauta's ('58) limbic midbrain concept. The final relays of the first two systems are to motor mechanisms in the medial midbrain and brainstem tegmentum; those of the second two systems project more laterally in the midbrain and brainstem tegmentum. The functional properties of the lateral and medial brainstem areas are quite different. Functional evidence suggests that the four amygdaloid circuits may act in concert as channels by which social communications or other stimuli of behavioral significance initiate sequences of species‐typical consummatory behaviors. Together, they appear to form an integrated neural system of emotion, which can operate independent of the corticobulbar/ corticospinal system.