Contextual encoding by ensembles of medial prefrontal cortex neurons
James M. Hyman, Liya Ma, Emili Balaguer-Ballester, Daniel Durstewitz, and Jeremy K. Seamans
PNAS March 27, 2012 vol. 109 no. 13 5086-5091
Contextual representations serve to guide many aspects of behavior and influence the way stimuli or actions are encoded and interpreted. The medial prefrontal cortex (mPFC), including the anterior cingulate subregion, has been implicated in contextual encoding, yet the nature of contextual representations formed by the mPFC is unclear. Using multiple single-unit tetrode recordings in rats, we found that different activity patterns emerged in mPFC ensembles when animals moved between different environmental contexts. These differences in activity patterns were significantly larger than those observed for hippocampal ensembles. Whereas ≈11% of mPFC cells consistently preferred one environment over the other across multiple exposures to the same environments, optimal decoding (prediction) of the environmental setting occurred when the activity of up to ≈50% of all mPFC neurons was taken into account. On the other hand, population activity patterns were not identical upon repeated exposures to the very same environment. This was partly because the state of mPFC ensembles seemed to systematically shift with time, such that we could sometimes predict the change in ensemble state upon later reentry into one environment according to linear extrapolation from the time-dependent shifts observed during the first exposure. We also observed that many strongly action-selective mPFC neurons exhibited a significant degree of context-dependent modulation. These results highlight potential differences in contextual encoding schemes by the mPFC and hippocampus and suggest that the mPFC forms rich contextual representations that take into account not only sensory cues but also actions and time.