Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli

Abstract

The purpose of this study was to identify the afferent link in the neural pathway which mediates emotional responses coupled to auditory stimuli. We evaluated whether autonomic and behavioral responses elicited by acoustic conditioned emotional stimuli are based on afferent information derived from the auditory cortex or from the auditory thalamic relay station, the medial geniculate nucleus (MG), in rats. The rat auditory cortex was defined through anterograde neuroanatomical tracing studies involving the injection of HRP into MG. Lesions were then placed in the auditory cortex or in MG. After 10 to 20 days the rats were subjected to classical fear conditioning trials involving the pairing of a pure tone with electric footshock. Changes in mean arterial pressure and heart rate and the duration of immobilization ("freezing") and drink suppression elicited by presentation during extinction trials (no footshock) of the acoustic conditioned emotional stimulus were measured. Auditory cortex lesions did not affect the magnitude of the mean arterial pressure or heart rate conditioned responses nor the duration of freezing or drink suppression. In contrast, lesions of MG suppressed the magnitude of both the autonomic and somatomotor (behavioral) conditioned emotional responses but did not affect either autonomic or somatic responses elicited by the footshock unconditioned stimulus. Lesions of the inferior colliculus, the primary source of afferent input to MG, replicated the effects of MG lesions. These findings demonstrate that lesions of MG and lower auditory centers, but not lesions of the auditory cortex, block autonomic and behavioral conditioned emotional responses coupled to acoustic stimuli and indicate that subcortical rather than cortical efferents of MG sustain these responses. Our concurrent observation that MG projects to several subcortical areas (central and lateral amygdala; caudate-putamen; ventromedial hypothalamus) involved in emotional behavior and autonomic function suggests hypotheses concerning subsequent links in this emotional processing pathway.