Retrorubral field is a hub for diverse threat and aversive outcome signals

Abstract

Adaptive fear scales to the degree of threat and requires diverse neural signals for threat and aversive outcome. We propose that the retrorubral field (RRF), a midbrain region containing A8 dopamine, is a neural origin of such signals. To reveal these signals, we recorded RRF single-unit activity while male rats discriminated danger, uncertainty, and safety. Many RRF neurons showed firing extremes to danger and safety that framed intermediate firing to uncertainty. The remaining neurons showed unique, threat-selective cue firing patterns. Diversity in firing direction, magnitude, and temporal characteristics led to the detection of at least eight functional neuron types. Neuron types defined with respect to threat showed unique firing patterns following aversive outcome. The result was RRF signals for foot shock receipt, positive prediction error, anti-positive prediction error, persistent safety, and persistent threat. The diversity of threat and aversive outcome signals points to a key role for the RRF in adaptive fear.

Keywords: A8; associative learning; conditioned suppression; dopamine; fear; safety; shock; single unit.