Activities of visual cortical and hippocampal neurons co-fluctuate in freely moving rats during spatial behavior

Daniel Christopher Haggerty,Daoyun Ji

doi:10.7554/elife.08902

Abstract

Visual cues exert a powerful control over hippocampal place cell activities that encode external spaces. The functional interaction of visual cortical neurons and hippocampal place cells during spatial navigation behavior has yet to be elucidated. Here we show that, like hippocampal place cells, many neurons in the primary visual cortex (V1) of freely moving rats selectively fire at specific locations as animals run repeatedly on a track. The V1 location-specific activity leads hippocampal place cell activity both spatially and temporally. The precise activities of individual V1 neurons fluctuate every time the animal travels through the track, in a correlated fashion with those of hippocampal place cells firing at overlapping locations. The results suggest the existence of visual cortical neurons that are functionally coupled with hippocampal place cells for spatial processing during natural behavior. These visual neurons may also participate in the formation and storage of hippocampal-dependent memories.

Highlights

Spatial information is presumably encoded by hippocampal ‘place cells’, which fire predominantly when an animal is at one or a few specific places of a given space (O’Keefe and Dostrovsky, 1971; McNaughton et al, 1983; Wilson and McNaughton, 1993)
Over time rats became habituated to the task and repeatedly travelled back and forth along the two overlapping trajectories in order to maximize the number of rewards
We found that layers 2 and 3 (L2/3), layer 4 (L4) and layers 5 and 6 (L5/6) cells were correlated in Δrate and ΔCOM with CA1 cells

Summary

Introduction

Spatial information is presumably encoded by hippocampal ‘place cells’, which fire predominantly when an animal is at one or a few specific places (place fields) of a given space (O’Keefe and Dostrovsky, 1971; McNaughton et al, 1983; Wilson and McNaughton, 1993). How these cells establish the location specificity has been a subject under intensive investigation. Visual cues play a pivotal role in place cell activities (Muller, 1996; Knierim, 2002; Colgin et al, 2008; Ravassard et al, 2013). Changing the proximal or distal visual cues alters firing rates and/or firing locations of place cells in a one- or two-dimensional space (Lee et al, 2004a, 2004b; Leutgeb et al, 2005), and the rotation of a salient cue card on the wall of a symmetric open arena evokes an equivalent rotation of place field locations (Muller and Kubie, 1987)

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