Hippocampal Place Cells

Nature, volume 566, pages 533–537 (2019)

Recalibration of path integration in hippocampal place cells

Ravikrishnan P. Jayakumar, et.al.

Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, USA

Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, MD, USA

Department of Psychology, UCLA, Los Angeles, CA, USA

Laboratory for Computational Sensing and Robotics, Johns Hopkins University, Baltimore, MD, USA

Solomon H. Snyder Department of Neuroscience, Johns Hopkins University, Baltimore, MD, USA

[paraphrase]

Hippocampal place cells are spatially tuned neurons that serve as elements of a ‘cognitive map’ in the mammalian brain. To detect the animal’s location, place cells are thought to rely upon two interacting mechanisms: sensing the position of the animal relative to familiar landmarks and measuring the distance and direction that the animal has travelled from previously occupied locations. The latter mechanism—known as path integration—requires a finely tuned gain factor that relates the animal’s self-movement to the updating of position on the internal cognitive map, as well as external landmarks to correct the positional error that accumulates. Models of hippocampal place cells and entorhinal grid cells based on path integration treat the path-integration gain as a constant, but behavioural evidence in humans suggests that the gain is modifiable. Here we show, using physiological evidence from rat hippocampal place cells, that the path-integration gain is a highly plastic variable that can be altered by persistent conflict between self-motion cues and feedback from external landmarks.

In an augmented-reality system, visual landmarks were moved in proportion to the movement of a rat on a circular track, creating continuous conflict with path integration. Sustained exposure to this cue conflict resulted in predictable and prolonged recalibration of the path-integration gain, as estimated from the place cells after the landmarks were turned off. We propose that this rapid plasticity keeps the positional update in register with the movement of the rat in the external world over behavioural timescales. These results also demonstrate that visual landmarks not only provide a signal to correct cumulative error in the path-integration system , but also rapidly fine-tune the integration computation itself.

Path integration is an evolutionarily conserved strategy that enables an organism to maintain an internal representation of its current location by integrating, over time, a movement vector that represents distance and direction travelled. Place cells and entorhinal grid cells have been implicated as key components of a path-integration system in the mammalian brain.

It is widely accepted that visual landmarks provide a signal to correct the error that accumulates during path integration. The results in this paper demonstrate physiological evidence for a role of vision in the path-integration computation itself by providing an error signal that is analogous to retinal slip in the vestibulo-ocular reflex. Specifically, this error signal fine-tunes the gain of the path integrator, which minimizes the accumulation of error in the first place. Although recalibration of the path-integrator gain may be expected over developmental timescales, these results indicate that the path-integration gain is fine-tuned even at behavioural timescales. The augmented-reality system described here will enable the investigation of mechanisms that underlie the interaction between external sensory input and the internal neural dynamics at the core of the path-integration system.

 

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