Space and Time: The Hippocampus as a Sequence Generator.

Neural computations are often compared to instrument-measured distance or duration, and such relationships are interpreted by a human observer. However, neural circuits do not depend on human-made instruments but perform computations relative to an internally defined rate-of-change. While neuronal correlations with external measures, such as distance or duration, can be observed in spike rates or other measures of neuronal activity, what matters for the brain is how such activity patterns are utilized by downstream neural observers. We suggest that hippocampal operations can be described by the sequential activity of neuronal assemblies and their internally defined rate of change without resorting to the concept of space or time.

• Publication year

  2018

• Venue

  Trends in Cognitive Sciences

• Publication date

  2018-10-01

• Fields of study

  Biology, Medicine, Psychology

• Identifiers
  DOI 10.1016/j.tics.2018.07.006PMID 30266146PMCID PMC6166479
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

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  2018cited by this paper
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  2017cited by this paper
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  2017cited by this paper
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