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Head direction and the evolutionary origins of spatial representation

Sayre, Marcel E. LU orcid ; Narendra, Ajay ; Heinze, Stanley LU orcid and Barron, Andrew B. (2026) In Trends in Neurosciences 49(6). p.423-432
Abstract

Spatial representations are a fundamental aspect of cognition. It remains largely unknown when and why the capacity to neurally represent space first evolved. In this opinion article, we argue that a strong candidate for the earliest such representation is the encoding of head direction. Dedicated circuits that compute head direction by integrating self-motion and external cues have been described in both vertebrates and insects and are likely to be ancestral in each lineage. This suggests a Cambrian or possibly Precambrian origin for head direction representation. In both lineages, head direction circuits occupy an evolutionarily and functionally foundational position. They occur in deeply conserved brain structures, sit upstream of... (More)

Spatial representations are a fundamental aspect of cognition. It remains largely unknown when and why the capacity to neurally represent space first evolved. In this opinion article, we argue that a strong candidate for the earliest such representation is the encoding of head direction. Dedicated circuits that compute head direction by integrating self-motion and external cues have been described in both vertebrates and insects and are likely to be ancestral in each lineage. This suggests a Cambrian or possibly Precambrian origin for head direction representation. In both lineages, head direction circuits occupy an evolutionarily and functionally foundational position. They occur in deeply conserved brain structures, sit upstream of other spatial representations, and can emerge from minimal neural architecture. In mammals, they also develop before other spatial systems. Together, these features suggest that head direction was the first neural representation of space, offering a window into the evolution of neural representation and spatial cognition more generally.

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author
; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
animal navigation, neural circuit evolution, neural representation, ring attractor, spatial cognition
in
Trends in Neurosciences
volume
49
issue
6
pages
10 pages
publisher
Elsevier
external identifiers
  • scopus:105036322256
  • pmid:42031613
ISSN
0166-2236
DOI
10.1016/j.tins.2026.04.001
language
English
LU publication?
yes
additional info
Publisher Copyright: © 2026 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY license. http://creativecommons.org/licenses/by/4.0/
id
3bbfe9bd-2a66-40e1-8691-82514d0738fc
date added to LUP
2026-06-09 07:47:10
date last changed
2026-08-05 18:12:12
@article{3bbfe9bd-2a66-40e1-8691-82514d0738fc,
  abstract     = {{<p>Spatial representations are a fundamental aspect of cognition. It remains largely unknown when and why the capacity to neurally represent space first evolved. In this opinion article, we argue that a strong candidate for the earliest such representation is the encoding of head direction. Dedicated circuits that compute head direction by integrating self-motion and external cues have been described in both vertebrates and insects and are likely to be ancestral in each lineage. This suggests a Cambrian or possibly Precambrian origin for head direction representation. In both lineages, head direction circuits occupy an evolutionarily and functionally foundational position. They occur in deeply conserved brain structures, sit upstream of other spatial representations, and can emerge from minimal neural architecture. In mammals, they also develop before other spatial systems. Together, these features suggest that head direction was the first neural representation of space, offering a window into the evolution of neural representation and spatial cognition more generally.</p>}},
  author       = {{Sayre, Marcel E. and Narendra, Ajay and Heinze, Stanley and Barron, Andrew B.}},
  issn         = {{0166-2236}},
  keywords     = {{animal navigation; neural circuit evolution; neural representation; ring attractor; spatial cognition}},
  language     = {{eng}},
  number       = {{6}},
  pages        = {{423--432}},
  publisher    = {{Elsevier}},
  series       = {{Trends in Neurosciences}},
  title        = {{Head direction and the evolutionary origins of spatial representation}},
  url          = {{http://dx.doi.org/10.1016/j.tins.2026.04.001}},
  doi          = {{10.1016/j.tins.2026.04.001}},
  volume       = {{49}},
  year         = {{2026}},
}