How is spatial position encoded in a non-retinotopic visual cortex?

Visual cortex has been almost exclusively studied in mammals. Yet, mammals are not the only vertebrates with a cortex; reptiles, such as lizards and turtles, also possess a well-defined, though exclusively three-layered cortex, similar to the "ancient" cortices of mammals (olfactory and hippocampal). Mammals and reptiles both derive from a common amniote ancestor that existed some 320 million years ago. In turtles, the dorsal cortex is analogous to the early visual cortex of mammals in that it receives inputs from the retina through the same disynaptic retino-thalamic pathway. By studying the responses of turtle visual cortical neurons, we found that their selectivity to position in the visual field is fundamentally different from that seen in mammalian visual cortex. It suggests that the principles of spatial encoding derived from studies of the visual cortex of mammals may not be ancestral, but rather acquired more recently in the mammalian lineage, possibly together with the evolution of the 6-layered neocortex.

HFSP Long-Term Fellow Julien Fournier and colleagues
authored on Fri, 16 March 2018

Cerebral cortex is not a mammalian invention. It most likely appeared in the forebrain of ancestral amniotes for it is found in mammals and in sauropsids but not in fish or amphibians. The cortex of today's reptiles, a three-layered structure similar to the piriform or hippocampal cortex in mammals, is probably similar to the cortex of ancestral amniotes. In turtles, the dorsal cortex, which extends over each hemisphere of the dorsal telencephalon, receives direct afferents from the visual thalamus and can thus be considered analogous to the primary visual cortex of mammals (V1). Yet, at a functional level, this visual area seems to process visual information in a very different way compared to mammalian V1.

Figure: Response of a typical dorsal cortex neuron to bright (left) and dark (right) spots flashed in 3 x 5 different positions in the visual field.

Turtle dorsal cortex used to be a classical model in vision research but no physiological evidence ever demonstrated the existence of any form of encoding of stimulus position. To assess if and how positions in the visual field are represented in turtle dorsal cortex, we recorded the activity of populations of dorsal cortex neurons in both awake and anesthetized turtles while presenting natural images or flashes of light in different positions of the visual field.

We found that although dorsal cortex exhibits weak spatial selectivity and shows no clear retinotopic mapping of positions in the visual field (unlike primary visual cortex in mammals), it may still encode information about the position of a visual stimulus, both at the single-neuron and population scale. Indeed, dorsal cortex is sensitive to the presence of salient edges in natural images and some dorsal cortex neurons may be slightly selective to oriented edges. Unlike neurons in mammals V1, turtle dorsal cortex neurons generally responded to all positions in the visual field. Yet, we found that their responses are not entirely uniform across space and across neurons, such that one can read out the position and contrast polarity of a stimulus in the visual field from the activity of local populations of dorsal cortex neurons recorded simultaneously. We further showed that spatial information may also be encoded in the form of a selective adaptation of dorsal cortex neurons to the spatiotemporal correlations of the visual inputs: repeated stimulation in one position of the visual field resulted in a complete extinction of responses in that position while responses to stimuli in surrounding positions were almost unaffected.

Overall, our results demonstrate that spatial features of visual images are represented in turtle visual cortex. However, this representation does not rely on a clear parametric analysis of visual features as described in mammals but rather takes the form of a distributed encoding across large ensembles of dorsal cortex neurons. The sensory representation in turtle visual cortex thus appears to be more similar to that observed in olfactory cortex or higher visual areas in mammals. It suggests that the fine spatial mapping of sensory attributes described in mammalian primary sensory areas (such as V1, S1, or A1), is not an ancestral feature of amniote cortex, but rather appears in the mammalian lineage, paralleling the expansion of cortical areas and cortical layers.

Reference

Spatial Information in a Non-retinotopic Visual Cortex. Fournier J*, Müller CM*, Schneider I, Laurent G. Neuron. 2018 Jan 3;97(1):164-180.e7

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