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'.
Highlights
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
The water to land transition in vertebrate life nearly 400 Ma was accompanied by conspicuous changes in two quite different realms: ecological, with 100-fold increases in total living organism mass [1] and visual range [2] over that of aquatic ecosystems; and neuroanatomical, with two of the largest radiations of land animals—mammals and birds—featuring 10-fold larger brains relative to body size than fishes [3]
We suggest several factors at work in the great brain expansion co-occurring with the endothermic land vertebrate radiations— mammals and birds
Summary
The water to land transition in vertebrate life nearly 400 Ma was accompanied by conspicuous changes in two quite different realms: ecological, with 100-fold increases in total living organism mass [1] and visual range [2] over that of aquatic ecosystems; and neuroanatomical, with two of the largest radiations of land animals—mammals and birds—featuring 10-fold larger brains relative to body size than fishes [3]. A million-fold increase in the volume of visually inspected space, from the higher transparency of air to light, enables enough time for this valuation to occur in a less stereotyped manner. This information enrichment includes more mobile sensory surfaces, such as a neck to swivel the greatly expanded visual sensorium, and new ways to integrate their information. The more challenging environments occurring on land may generate a selective benefit for learning with few or no trials. This occurs via planning, a process that can be thought of as learning from hypothetical experience, and abstraction. The ability to learn a high-acuity, value-tagged egocentric visual panorama characteristic of the cortex and its homologues and integration with the temporal-sequence computations of the hippocampus together seem critical to planning
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