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Cue-based feedback enables remapping in a multiple oscillator model of place cell activity

Joseph D. Monaco1*, Kechen Zhang2, Hugh T. Blair3, 4 and James J. Knierim1
  • 1 Johns Hopkins, Krieger Mind/Brain Institute, United States
  • 2 Johns Hopkins, Biomedical Engineering, United States
  • 3 UCLA, Psychology, United States
  • 4 UCLA , Brain Research Institute, United States

Place fields in rat hippocampus consist of both a firing-rate component [6] and a temporal component defined by spike-phase precession relative to local theta [7]. Previous models based on oscillatory phase interference [e.g., 5] can account for phase precession, but not for the remapping that can occur when an animal is exposed to novel spatial information. A novel room may elicit complete remapping in which the population spatial code becomes statistically independent. However, subtler cue manipulations can induce partial remapping and other more graded spatial recoding effects in which some degree of coherence with previous representations is retained. Double-rotation experiments, in which sets of local and distal cues are rotated relative to each other around a circular track, have shown that activity in the CA3 subregion is significantly more coherent than in CA1 [4]. Thus, it is critical to our understanding of hippocampal function to have models of spatial coding that can explain graded remapping as well as all-or-none complete remapping. While somato-dendritic dual-oscillator models have been examined closely [5], it is not clear how to couple them with environmental cues to explore these sorts of effects. We demonstrate a more recent generalization of oscillatory interference models featuring multiple oscillator inputs [1]. Each oscillator’s phase is modulated by the velocity vector of the trajectory such that the population phase code provides stable path integration. First, we show that arbitrarily connected output units can produce spatially-modulated activity. Further, due to the combinatoric rarity of synchronizing N oscillators, there is a lower bound on the number of theta inputs to achieve sparse responses. Second, we demonstrate a cue-based phase-code feedback that represents learned fixed-points of the trajectory. This makes spatial representations robust to noise, but also allows cue manipulations similar to double-rotation experiments. Simulating double-rotation using actual trajectories, we found that the diversity of remapping behavior among the output population depended on the number of cues, the feedback gain and the relative contributions of path integration and phase-code feedback. We found a diversity of both cue-following and ambiguous outputs qualitatively similar to the experimental data using moderate overall feedback gain and a small number of low-spatial-extent cues. Recent intracellular recordings of place cells demonstrated increased theta power within-field and intracellular phase precession relative to extracellular theta [3], both of which result from this model. Notably, this model enables complete remapping with a phase reset of the sort that may occur upon introduction to a novel environment and provides a possible common-input explanation for the concurrency of hippocampal remapping and entorhinal grid realignment [2]. Thus, the multiple oscillator model provides insight into phase code mechanisms that may underlie a wide array of rate and temporal coding effects and remapping phenomena in hippocampus.

References

1. Blair, Zhang. (2009). SfN Abstract, 192.27

2. Fyhn, Hafting, Treves, Moser, Moser. (2007). Nature, 446(7132):190-194

3. Harvey, Collman, Dombeck, Tank. (2009). Nature, 461(7266):941-946

4. Lee, Yoganarasimha, Rao, Knierim. (2004). Nature, 430(6998):456-459

5. O’Keefe, Burgess. (2005). Hippocampus, 15:853-866

6. O’Keefe, Dostrovsky. (1971). Brain Research, 34(1):171-175

7. O’Keefe, Recce. (1993). Hippocampus, 3(3):317-330.

Conference: Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.

Presentation Type: Poster Presentation

Topic: Poster session III

Citation: Monaco JD, Zhang K, Blair HT and Knierim JJ (2010). Cue-based feedback enables remapping in a multiple oscillator model of place cell activity. Front. Neurosci. Conference Abstract: Computational and Systems Neuroscience 2010. doi: 10.3389/conf.fnins.2010.03.00192

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Received: 03 Mar 2010; Published Online: 03 Mar 2010.

* Correspondence: Joseph D Monaco, Johns Hopkins, Krieger Mind/Brain Institute, Baltimore, United States, joe@selfmotion.net