Rapid synaptic plasticity contributes to a learned conjunctive code of position and choice-related information in the hippocampus

Xinyu Zhao,Ching-Lung Hsu,Nelson Spruston

doi:10.1016/j.neuron.2021.10.003

Xinyu Zhao, Ching-Lung Hsu + Show 1 more

Open Access

https://doi.org/10.1016/j.neuron.2021.10.003

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Abstract

To successfully perform goal-directed navigation, animals must know where they are and what they are doing-e.g., looking for water, bringing food back to the nest, or escaping from a predator. Hippocampal neurons code for these critical variables conjunctively, but little is known about how this "where/what" code is formed or flexibly routed to other brain regions. To address these questions, we performed intracellular whole-cell recordings in mouse CA1 during a cued, two-choice virtual navigation task. We demonstrate that plateau potentials in CA1 pyramidal neurons rapidly strengthen synaptic inputs carrying conjunctive information about position and choice. Plasticity-induced response fields were modulated by cues only in animals previously trained to collect rewards based on available cues. Thus, we reveal that gradual learning is required for the formation of a conjunctive population code, upstream of CA1, while plateau-potential-induced synaptic plasticity in CA1 enables flexible routing of the code to downstream brain regions.

Highlights

Animals rely on information from memories to perform many survival-related behaviors
We previously demonstrated that population activities of CA3 cells can be inferred from the membrane potential dynamics in behavioral time-scale synaptic plasticity (BTSP)-induced CA1 place fields (Zhao et al, 2020)
Our results reveal that the rapid synaptic plasticity induced by plateau potentials can support the manifestation of a conjunctive code of the animal’s current position and choice-related information in CA1, enabling the flexible relay of task-specific variables to extra-hippocampal brain regions

Summary

Introduction

Animals rely on information from memories to perform many survival-related behaviors. A fraction of place cells in the CA1 subregion of the hippocampus has been shown to exhibit firing rate modulation based on the animal’s past and/or future trajectories in spatial alternation tasks (Wood et al, 2000; Frank et al, 2000; Ito et al, 2015; Ainge et al, 2007b; Ferbinteanu and Shapiro, 2003; Kinsky et al, 2020), which require animals to make alternating left and right turns in a figure-8-like maze or sequentially explore different arms of a W-shaped maze In these tasks, some cells fire selectively in a common location prior to left or right turns.

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