Extrafield activity shifts the place field center of mass to encode aversive experience

Abstract

Hippocampal place cells are known to have a key role in encoding spatial information. Aversive stimuli, such aspredator odor, evoke place field remapping and a change in preferred firing locations. However, it remains unclearhow place cells use positive or negative experiences to remap. We investigated whether CA1 place cells,recorded from behaving rats, remap randomly or whether their reconfiguration depends on the perceived locationof the aversive stimulus. Exposure to trimethylthiazoline (TMT; an innately aversive odor), increased the amplitudeof hippocampal oscillations in the two arms of the maze in which TMT exposure occurred. We found that apopulation of place cells with fields located outside the TMT arms increased their activity (extrafield spiking) in theTMT arms during the aversive episodes. Moreover, in the subsequent post-TMT recording, these cells exhibiteda significant shift in their center of mass (COM) towards the TMTarms. The induction of extrafield plasticity wasmediated by the basolateral amygdala complex (BLA). Photostimulation of the BLA triggered aversive behavior,synchronized hippocampal local field oscillations, and increased the extrafield spiking of the hippocampal place cellsfor the first 100 ms after light delivery. Optogenetic BLA activation triggered an increase in extrafield spiking activity thatwas correlated with the degree of place field plasticity. Furthermore, BLA-mediated increase of the extrafield activitypredicts the degree of subsequent field plasticity. Our findings demonstrate that that the remapping of hippocampalplace cells during aversive episodes is not random but it depends on the location of the aversive stimulus.