Precise spatial coding is preserved along the longitudinal hippocampal axis

Hippocampus. 2014 Dec;24(12):1533-48. doi: 10.1002/hipo.22333. Epub 2014 Aug 1.

Abstract

Compared with the dorsal hippocampus, relatively few studies have characterized neuronal responses in the ventral hippocampus. In particular, it is unclear whether and how cells in the ventral region represent space and/or respond to contextual changes. We recorded from dorsal and ventral CA1 neurons in freely moving mice exposed to manipulations of visuospatial and olfactory contexts. We found that ventral cells respond to alterations of the visuospatial environment such as exposure to novel local cues, cue rotations, and contextual expansion in similar ways to dorsal cells, with the exception of cue rotations. Furthermore, we found that ventral cells responded to odors much more strongly than dorsal cells, particularly to odors of high valence. Similar to earlier studies recording from the ventral hippocampus in CA3, we also found increased scaling of place cell field size along the longitudinal hippocampal axis. Although the increase in place field size observed toward the ventral pole has previously been taken to suggest a decrease in spatial information coded by ventral place cells, we hypothesized that a change in spatial scaling could instead signal a shift in representational coding that preserves the resolution of spatial information. To explore this possibility, we examined population activity using principal component analysis (PCA) and neural location reconstruction techniques. Our results suggest that ventral populations encode a distributed representation of space, and that the resolution of spatial information at the population level is comparable to that of dorsal populations of similar size. Finally, through the use of neural network modeling, we suggest that the redundancy in spatial representation along the longitudinal hippocampal axis may allow the hippocampus to overcome the conflict between memory interference and generalization inherent in neural network memory. Our results indicate that ventral population activity is well suited for generalization across locations and contexts.

Keywords: decoding; generalization; interference; population coding; reconstruction; ventral hippocampus.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Action Potentials
  • Animals
  • CA1 Region, Hippocampal / physiology*
  • Cues
  • Electrodes, Implanted
  • Exploratory Behavior / physiology
  • Male
  • Mice, Inbred C57BL
  • Models, Neurological
  • Neural Networks, Computer
  • Neurons / physiology*
  • Odorants
  • Olfactory Perception / physiology
  • Principal Component Analysis
  • Rotation
  • Signal Processing, Computer-Assisted
  • Space Perception / physiology*
  • Spatial Memory / physiology