Extra-field activity shifts the place field center of mass to encode aversion experience

The hippocampal place cells encode spatial representation but it remains unclear how they store concurrent positive or negative experiences. Here, we report on place field reconfiguration in response to an innately aversive odor trimethylthiazoline (TMT). The advantage of TMT is the absence of learning curve required for associative fear conditioning. Our study investigated if CA1 place cells, recorded from behaving rats, remap randomly or if their reconfiguration depends on the location of the aversive stimulus perception. Exposure to TMT increased the amplitude of hippocampal beta oscillations in two arms of a maze (TMT arms). We found that a population of place cells with fields located outside the TMT arms increased their activity (extra-field spiking) in the TMT arms during the aversive episodes. These cells exhibited significant shift of the center of mass towards the TMT arms in the subsequent post-TMT recording. The induction of extra-field plasticity was mediated by the basolateral amygdala complex (BLA). Photostimulation of the BLA triggered aversive behavior, synchronized response of hippocampal local field oscillations, augmented theta rhythm amplitude and increased the spiking of place cells for the first 100ms after the light delivery. This occurred only for the extra-field-but not for intra-field spikes. Optogenetic BLA-triggered an increase in extra-field spiking activity correlated to the degree of place field plasticity in the post-ChR2 recording session. Our findings demonstrate that the increased extra-field activity during aversive episodes mediates the degree of subsequent field plasticity.