Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat

Although the auditory cortex is believed to be the principal efferent target of the medial geniculate body (MG), our recent behavioral studies indicate that in rats the conditioned coupling of emotional responses to an acoustic stimulus is mediated by subcortical projections of the MG. In the present study we have therefore used WGA-HRP as an anterograde and retrograde axonal marker to (1) define the full range of subcortical efferent projections of the MG; (2) identify the cells of origin within the MG of each projection; and (3) determine whether the subregions of the MG that project to subcortical areas receive inputs from acoustic relay nuclei of the mid-brain, particularly the inferior colliculus. The rat MG was first parcelled into three major cytoarchitectural areas: the ventral, medial, and dorsal divisions. The suprageniculate nucleus, located within the body of the MG just dorsal to the medial division, was also identified. Efferent projections of the MG were determined by combined anterograde and retrograde tracing methods. Injections of WGA-HRP in the MG produced anterograde transport to cortex and several subcortical areas, including the posterior caudate-putamen and amygdala, the ventromedial nucleus of the hypothalamus, and the subparafascicular thalamic nucleus. The cells of origin of the subcortical projections were then mapped retrogradely after injections in the anterogradely labeled areas. Injections in the caudate-putamen or amygdala retrogradely labeled the medial division of the MG and the suprageniculate nucleus, as well as several adjacent areas of the posterior thalamus surrounding the MG. In contrast, injections in the ventromedial nucleus of the hypothalamus or the subparafascicular thalamic nucleus only produced labeling in the areas surrounding MG. Afferents to MG from the inferior colliculus were then identified. The central nucleus of the inferior colliculus, the main lemniscal acoustic relay nucleus in the midbrain, was found to project to the ventral and medial divisions of the MG. In contrast, the dorsal cortex and external nucleus of the inferior colliculus project to each division of the MG and to several additional nuclei in adjacent areas of the posterior thalamus. These data demonstrate that the medial division of MG, the suprageniculate nucleus, and immediately adjacent areas of the posterior thalamus provide a direct linkage between auditory neurons in the inferior colliculus and subcortical areas of the forebrain and thereby support the view that thalamic sensory nuclei relay afferent signals to subcortical as well as cortical areas.