The brain areas that mediate the formation of auditory threat memory and perceptual decisions remain uncertain to date. Candidates include the primary (A1) and secondary (A2) auditory cortex, the medial division of the medial geniculate body (MGm), amygdala, and the temporal association cortex. We used chemogenetic and optogenetic manipulations with in vivo and in vitro patch-clamp recordings to assess the roles of these brain regions in threat memory learning in female mice. We found that conditioned sound (CS) frequency-dependent plasticity resulted in the formation of auditory threat memory in the temporal association cortex. This neural correlated auditory threat memory depended on CS frequency information from A1 glutamatergic subthreshold monosynaptic inputs, CS lateral inhibition from A2 glutamatergic disynaptic inputs, and non-frequency-specific facilitation from MGm glutamatergic monosynaptic inputs. These results indicate that the A2 and MGm work together in an inhibitory-facilitative role.SIGNIFICANCE STATEMENT: The ability to recognize specific sounds to avoid predators or seek prey is a useful survival tool. Improving this ability through experiential learning is an added advantage requiring neural plasticity. As an example, humans must learn to distinguish the sound of a car horn, and thus avoid oncoming traffic. Our research discovered that the temporal association cortex can encode this kind of auditory information through tonal receptive field plasticity. In addition, the results revealed the underlying synaptic mechanisms of this process. These results extended our understanding of how meaningful auditory information is processed in an animal's brain.
Keywords: auditory cortex; auditory fear conditioning; medial geniculate body; plasticity; temporal association cortex.
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