Aversive prediction error signals in the amygdala.

McHugh SB
Barkus C
Huber A
Capitão L
Lima J
Lowry JP
Bannerman DM

Prediction errors represent the difference between what was expected and what actually happened. Prediction errors for rewards are believed to be encoded by dopamine neurons but the neural basis for aversive prediction errors is unknown. Here we show that activity patterns in the amygdala, a brain region necessary for aversive learning, are consistent with aversive prediction error signals.

Scientific Abstract

Prediction error signals are fundamental to learning. Here, in mice, we show that aversive prediction signals are found in the hemodynamic responses and theta oscillations recorded from the basolateral amygdala. During fear conditioning, amygdala responses evoked by footshock progressively decreased, whereas responses evoked by the auditory cue that predicted footshock concomitantly increased. Unexpected footshock evoked larger amygdala responses than expected footshock. The magnitude of the amygdala response to the footshock predicted behavioral responses the following day. The omission of expected footshock led to a decrease below baseline in the amygdala response suggesting a negative aversive prediction error signal. Thus, in mice, amygdala activity conforms to temporal difference models of aversive learning.

Aversive prediction error signals in the amygdala.
Aversive prediction error signals in amygdala theta oscillations during fear learning. (A) Spectrogram from training day 1 (T1) showing the pre-CS, CS+, and US periods. US (footshock) onset at 29.5s (arrow), offset at 30s. (B) Same as in A, but showing training day 3 (T3). During T3, CS+ evoked theta oscillations were stronger and US evoked theta oscillations were weaker compared to T1. (C) Peak theta power during CS+ and US periods for T1-T3. Note the increase in CS+ evoked theta and the decrease in US evoked theta over training. (D) Theta power was significantly higher for unexpected than expected shock, consistent with an aversive prediction error signal.
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