Evolutionary constraints on visual cortex architecture from the dynamics of hallucinations

Thomas Charles Butler, Marc Benayoun, Edward Wallace, Wim Van Drongelenc, Nigel Goldenfelda, Jack Cowane

Research output: Contribution to journalArticlepeer-review

Abstract

In the cat or primate primary visual cortex (V1), normal vision corresponds to a state where neural excitation patterns are driven by external visual stimuli. A spectacular failure mode of V1 occurs when such patterns are overwhelmed by spontaneously generated spatially self-organized patterns of neural excitation. These are experienced as geometric visual hallucinations. The problem of identifying the mechanisms by which V1 avoids this failure is made acute by recent advances in the statistical mechanics of pattern formation, which suggest that the hallucinatory state should be very robust. Here, we report how incorporating physiologically realistic long-range connections between inhibitory neurons changes the behavior of a model of V1. We find that the sparsity of long-range inhibition in V1 plays a previously unrecognized but key functional role in preserving the normal vision state. Surprisingly, it also contributes to the observed regularity of geometric visual hallucinations. Our results provide an explanation for the observed sparsity of long-range inhibition in V1-this generic architectural feature is an evolutionary adaptation that tunes V1 to the normal vision state. In addition, it has been shown that exactly the same long-range connections play a key role in the development of orientation preference maps. Thus V1's most striking long-range features-patchy excitatory connections and sparse inhibitory connections-are strongly constrained by two requirements: the need for the visual state to be robust and the developmental requirements of the orientational preference map.

Original languageEnglish (US)
Pages (from-to)606-609
Number of pages4
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number2
DOIs
StatePublished - Jan 10 2012

Keywords

  • Evolution
  • Fluctuations

ASJC Scopus subject areas

  • General

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