RT Journal Article
SR Electronic
T1 Extrafield activity shifts the place field center of mass to encode aversive experience
JF eneuro
JO eNeuro
FD Society for Neuroscience
SP ENEURO.0423-17.2019
DO 10.1523/ENEURO.0423-17.2019
A1 Omar Mamad
A1 Beshoy Agayby
A1 Lars Stumpp
A1 Richard B. Reilly
A1 Marian Tsanov
YR 2019
UL http://www.eneuro.org/content/early/2019/03/04/ENEURO.0423-17.2019.abstract
AB Hippocampal place cells are known to have a key role in encoding spatial information. Aversive stimuli, such as predator odor, evoke place field remapping and a change in preferred firing locations. However, it remains unclear how 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 location of the aversive stimulus. Exposure to trimethylthiazoline (TMT, an innately aversive odor), increased the amplitude of hippocampal beta oscillations in the two arms of the maze in which TMT exposure occurred. We found that a population of place cells with fields located outside the TMT arms increased their activity (extrafield spiking) in the TMT arms during the aversive episodes. Moreover, in the subsequent post-TMT recording, these cells exhibited a significant shift in their center of mass towards the TMT arms. The induction of extrafield plasticity was mediated 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 cells for the first 100 ms after light delivery. Optogenetic BLA activation triggered an increase in extrafield spiking activity that was correlated with the degree of place field plasticity. Furthermore, BLA-mediated increase of the extrafield activity predicts the degree of subsequent field plasticity. Our findings demonstrate that that the remapping of hippocampal place cells during aversive episodes is not random but it depends on the location of the aversive stimulus.Significance statement Here, we successfully decoded the pattern of place field reconfiguration to an aversive experience after exposure to an innately aversive odor. For the first time, we reveal that the degree of place field plasticity closely correlates with the extrafield spiking rate during aversive episodes. Using a spatial optogenetic technique in behaving rats, we show that the link between aversive behavior and place field reconfiguration is mediated by the spatially confined activation of the basolateral amygdala. These findings demonstrate that the hippocampus not only maps the spatial environment but also stores the affective value of experienced events.