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.

Nicotine withdrawal disrupts both foreground and background contextual fear conditioning but not pre-pulse inhibition of the acoustic startle response in C57BL/6 mice

“…Background Training: There are multiple measures of conditioned fear that include changes in heart rate [48], freezing [6] and potentiated startle [7,47] this study used freezing as the behavioral measure of conditioned fear. During training, mice were placed in conditioning chambers for 5 minutes and 30 seconds and freezing was assessed.…”

Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear

“…All tests involved presentation of the CS during extinction trials (no US) conducted in the animal's home cage on the day after conditioning. This procedure, used in previous studies (LeDoux et al, 1984, b, Iwata et al, 1986a, allows the measurement of cardiovascular responses during a quiescent state and provides a relatively pure assessment of the responses elicited by the CS, independent of contextual cues associated with the conditioning apparatus.…”

“…The central circuitry mediating the classical conditioning of fear to an acoustic stimulus in rats involves transmission through primary auditory structures of the brain stem to the auditory receptive region of the thalamus and, from there, directly to the amygdala (LeDoux et al, 1984LeDoux, 1986LeDoux, , 1987Iwata et al, 1986a). The critical amygdaloid regions are located in the dorsal part of this structure, and include the lateral and central nuclei and the amygdalostriatal transition zone LeDoux et al, 1986a).…”

Emotional memory and psychopathology

“…These data suggest that the acoustic CS is transmitted through the auditory system to the MG and from there to some region in addition to the auditory cortex. Antereograde labelling studies demonstrate that the MG and adjacent nuclei receiving auditory input, in addition to projecting to the auditory cortex, also sends e¡erents to LA (LeDoux et al 1984(LeDoux et al , 1990b. Conditioning of fear reactions to simple acoustic stimuli can be mediated by direct projections to LA from the thalamus, and lesions of LA block fear conditioning.…”