Scanning behavior in novel environments promotes de novo formation of hippocampal place fields in rats

This is a poster that was presented on November 12, 2013, at the Society for Neuroscience meeting in San Diego, CA:

J. Monaco, G. Rao, E. D. Roth, J. J. Knierim. "Scanning behavior in novel environments promotes de novo formation of hippocampal place fields in rats". Soc Neurosci Abstr 2013, 670.07.

The hippocampus is thought to play a critical role in episodic memory by incorporating the sensory input of an experience onto a spatial framework embodied by place cells. While the development of a new place field map has been shown to occur rapidly with experience [1], the interaction between discrete exploratory behaviors and the specific, immediate, and persistent modifications of neural representations required by episodic memory has not been established. We previously examined the relationship between place-field potentiation, a form of rate remapping, and head scanning behavior [2]. Here we investigate whether there is a similar interaction between head scanning and the formation of de novo place fields when the animals are first introduced to a completely novel environment. Place fields recorded in novel rooms [3] demonstrate both onset and, in some recordings, additional post-onset potentiation related to colocalized scanning activity on the prior lap. These results strongly suggest that, during the attentive behaviors that animals use to investigate their environments during exploration, place-cell activity mediates the one-trial encoding of ongoing experiences necessary for episodic memory.

The phenomenon of head scan–activation of place fields occurs during an animal’s first exploratory session in a novel environment, extending our previous results from familiar and altered environments [2]. Our results demonstrate that place-cell activity during scanning behavior is involved in more than just the recall of place fields previously formed during forward locomotion, because higher-than-expected scan firing often precedes and predicts the development of new place fields in the novel environment. We suggest that pauses to execute head scans are a functionally significant component of navigation by intermittent locomotion [4], a widely observed exploratory strategy thought to balance internally-generated movement with the acquisition of external sensory information [5]. Place field modulation by head scans is consistent with the idea that a critical function of the hippocampal cognitive map is to encode a dynamic record of ongoing experience tied to attentive exploration of the external world.

[1] Frank LM, Stanley GB, Brown EN. J Neurosci 24(35), 7681–9 (2004)
[2] Monaco JD, Rao G, Knierim JJ. Soc Neurosci Abstr 97.13 (2011)
[3] Roth ED, Yu X, Rao G, Knierim JJ. PLoS One 7(4), e36035 (2012)
[4] Kramer DL, McLaughlin RL. Am Zool 41(2), 137–53 (2001)
[5] Golani I, Benjamini Y, Eilam D. Behav Brain Res 53(1–2), 21–33 (1993); Tchernichovski O, Benjamini Y, Golani I. Biol Cybern, 78(6),423–32 (1998)