Neuron
Volume 104, Issue 6, 18 December 2019, Pages 1180-1194.e7
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Article
A Critical Role for Neocortical Processing of Threat Memory

https://doi.org/10.1016/j.neuron.2019.09.025Get rights and content
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Highlights

  • Auditory cortex is selectively required for complex stimulus threat memory

  • Adjacent temporal association cortex controls all forms of auditory threat memory

  • Cortico-amygdala information transmission governs complex stimulus memory

  • Amygdala-projecting neurons show population plasticity for stimulus discrimination

Summary

Memory of cues associated with threat is critical for survival and a leading model for elucidating how sensory information is linked to adaptive behavior by learning. Although the brain-wide circuits mediating auditory threat memory have been intensely investigated, it remains unclear whether the auditory cortex is critically involved. Here we use optogenetic activity manipulations in defined cortical areas and output pathways, viral tracing, pathway-specific in vivo 2-photon calcium imaging, and computational analyses of population plasticity to reveal that the auditory cortex is selectively required for conditioning to complex stimuli, whereas the adjacent temporal association cortex controls all forms of auditory threat memory. More temporal areas have a stronger effect on memory and more neurons projecting to the lateral amygdala, which control memory to complex stimuli through a balanced form of population plasticity that selectively supports discrimination of significant sensory stimuli. Thus, neocortical processing plays a critical role in cued threat memory.

Keywords

neocortical circuits
threat conditioning
associative learning
behavior
auditory cortex
stimulus complexity
temporal association cortex
brain-wide circuits
learning-related plasticity
neural population coding

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