4.8 Article

Action-driven remapping of hippocampal neuronal populations in jumping rats

Publisher

NATL ACAD SCIENCES
DOI: 10.1073/pnas.2122141119

Keywords

hippocampus; phase precession; theta oscillations; place cells; learning

Funding

  1. NIH [MH122391, U19 NS107616, U19 NS104590]
  2. NIH Training Grant for Computational Neuroscience [R90DA043849]

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This study investigates the role of action in the neuronal organization of the hippocampus through a behavioral experiment of training rats to jump a gap. The results indicate that jumping induces consistent electrophysiological patterns in the hippocampus, while the theta spike phase versus animal position relationship remains unchanged.
The current dominant view of the hippocampus is that it is a navigation device guided by environmental inputs. Yet, a critical aspect of navigation is a sequence of planned, coordinated actions. We examined the role of action in the neuronal organization of the hippocampus by training rats to jump a gap on a linear track. Recording local field potentials and ensembles of single units in the hippocampus, we found that jumping produced a stereotypic behavior associated with consistent electrophysiological patterns, including phase reset of theta oscillations, predictable global firing-rate changes, and population vector shifts of hippocampal neurons. A subset of neurons (jump cells) were systematically affected by the gap but only in one direction of travel. Novel place fields emerged and others were either boosted or attenuated by jumping, yet the theta spike phase versus animal position relationship remained unaltered. Thus, jumping involves an action plan for the animal to traverse the same route as without jumping, which is faithfully tracked by hippocampal neuronal activity.

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