Novel encoding and updating of positional, or directional, spatial cues are processed by distinct hippocampal subfields: Evidence for parallel information processing and the "what" stream

Hippocampus. 2018 May;28(5):315-326. doi: 10.1002/hipo.22833. Epub 2018 Feb 19.

Abstract

The specific roles of hippocampal subfields in spatial information processing and encoding are, as yet, unclear. The parallel map theory postulates that whereas the CA1 processes discrete environmental features (positional cues used to generate a "sketch map"), the dentate gyrus (DG) processes large navigation-relevant landmarks (directional cues used to generate a "bearing map"). Additionally, the two-streams hypothesis suggests that hippocampal subfields engage in differentiated processing of information from the "where" and the "what" streams. We investigated these hypotheses by analyzing the effect of exploration of discrete "positional" features and large "directional" spatial landmarks on hippocampal neuronal activity in rats. As an indicator of neuronal activity we measured the mRNA induction of the immediate early genes (IEGs), Arc and Homer1a. We observed an increase of this IEG mRNA in CA1 neurons of the distal neuronal compartment and in proximal CA3, after novel spatial exploration of discrete positional cues, whereas novel exploration of directional cues led to increases in IEG mRNA in the lower blade of the DG and in proximal CA3. Strikingly, the CA1 did not respond to directional cues and the DG did not respond to positional cues. Our data provide evidence for both the parallel map theory and the two-streams hypothesis and suggest a precise compartmentalization of the encoding and processing of "what" and "where" information occurs within the hippocampal subfields.

Keywords: fluorescence in situ hybridization; hippocampus; immediate early gene; information encoding; spatial learning.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cues
  • Cytoskeletal Proteins / metabolism
  • Exploratory Behavior / physiology*
  • Gene Expression Regulation
  • Hippocampus / anatomy & histology
  • Hippocampus / metabolism*
  • Homer Scaffolding Proteins / metabolism
  • In Situ Hybridization, Fluorescence
  • Long-Term Synaptic Depression / physiology
  • Male
  • Memory, Long-Term / physiology
  • Memory, Short-Term / physiology
  • Nerve Tissue Proteins / metabolism
  • Neurons / cytology
  • Neurons / metabolism*
  • Orientation / physiology
  • Rats, Wistar
  • Space Perception / physiology*
  • Spatial Memory / physiology
  • Spatial Processing / physiology*

Substances

  • Cytoskeletal Proteins
  • Homer Scaffolding Proteins
  • Homer1 protein, rat
  • Nerve Tissue Proteins
  • activity regulated cytoskeletal-associated protein