The neuroecology of the water-to-land transition and the evolution of the vertebrate brain

Malcolm A. MacIver*, Barbara L. Finlay*

*Corresponding author for this work

Research output: Contribution to journalReview articlepeer-review

22 Scopus citations

Abstract

The water-to-land transition in vertebrate evolution offers an unusual opportunity to consider computational affordances of a new ecology for the brain. All sensory modalities are changed, particularly a greatly enlarged visual sensorium owing to air versus water as a medium, and expanded by mobile eyes and neck. The multiplication of limbs, as evolved to exploit aspects of life on land, is a comparable computational challenge. As the total mass of living organisms on land is a hundredfold larger than the mass underwater, computational improvements promise great rewards. In water, the midbrain tectum coordinates approach/avoid decisions, contextualized by water flow and by the animal’s body state and learning. On land, the relative motions of sensory surfaces and effectors must be resolved, adding on computational architectures from the dorsal pallium, such as the parietal cortex. For the large-brained and long-living denizens of land, making the right decision when the wrong one means death may be the basis of planning, which allows animals to learn from hypothetical experience before enactment. Integration of value-weighted, memorized panoramas in basal ganglia/frontal cortex circuitry, with allocentric cognitive maps of the hippocampus and its associated cortices becomes a cognitive habit-to-plan transition as substantial as the change in ecology. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Original languageEnglish (US)
Article number20200523
JournalPhilosophical Transactions of the Royal Society B: Biological Sciences
Volume377
Issue number1844
DOIs
StatePublished - 2022
Externally publishedYes

Funding

M.A.M. was supported by the NSF Brain Initiative under ECCS-1835389 and NSF IIS-2123725.

Keywords

  • brain
  • computation
  • fish-tetrapod transition
  • terrestriality

ASJC Scopus subject areas

  • General Biochemistry, Genetics and Molecular Biology
  • General Agricultural and Biological Sciences

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