Abstract
The balance between activities of fear neurons and extinction neurons in the basolateral nucleus of the basal amygdala (BAL) has been hypothesized to encode fear states after extinction. However, it remains unclear whether these neurons are solely responsible for encoding fear states. In this study, we stably recorded single-unit activities in the BAL during fear conditioning and extinction for 3 days, providing a comprehensive view on how different BAL neurons respond during fear learning. We found BAL neurons that showed excitatory responses to the conditioned stimulus (CS) after fear conditioning (‘conditioning-potentiated neurons’) and another population that showed excitatory responses to the CS after extinction (‘extinction-potentiated neurons’). Interestingly, we also found BAL neurons that developed inhibitory responses to the CS after fear conditioning (‘conditioning-inhibited neurons’) or after extinction (‘extinction-inhibited neurons’). BAL neurons that showed excitatory responses to the CS displayed various functional connectivity with each other, whereas less connectivity was observed among neurons with inhibitory responses to the CS. Intriguingly, we found correlative neuronal activities between conditioning-potentiated neurons and neurons with inhibitory responses to the CS. Our findings suggest that distinct BAL neurons, which are responsive to the CS with excitation or inhibition, encode various facets of fear conditioning and extinction.
Highlights
The balance between activities of fear neurons and extinction neurons in the basolateral nucleus of the basal amygdala (BAL) has been hypothesized to encode fear states after extinction
We found two sub-populations of B AL neurons that exhibited either conditioned stimulus (CS)-evoked excitation or inhibition in fear conditioning and subsequent extinction (Supplementary Fig. S7a)
We found new neuronal sub-populations in the B AL; one that showed CS-evoked excitation even before conditioning and another population that developed CS-evoked excitation after fear conditioning and retained the potentiated responses even after extinction
Summary
The balance between activities of fear neurons and extinction neurons in the basolateral nucleus of the basal amygdala (BAL) has been hypothesized to encode fear states after extinction. There have been relatively few studies in which the activity of single neurons in the B AL are monitored longitudinally during fear conditioning and e xtinction[21,22] These studies focused on specific populations of B AL neurons (‘fear neurons’, ’extinction neurons’ and ‘extinction-resistant neurons’), and we still lack a comprehensive and unbiased picture of changes in the activity of BAL neurons throughout conditioning and extinction. We used fixed-microwire recordings to track longitudinal changes in the neural activity of single BAL neurons during a 3-day procedure encompassing conditioning and multiple sessions of extinction. We here report that distinct sub-populations of B AL neurons that encode various aspects of fear conditioning and extinction and the functional connectivity among distinct B AL neurons
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