Evolutionary constraints on visual cortex architecture from the dynamics of hallucinations.
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.
Department of Physics, University of Illinois, Urbana-Champaign, 1110 West Green Street, Urbana, IL 61801, USA.
Thomas Charles
TC
Butler
Marc
M
Benayoun
Edward
E
Wallace
Wim
W
van Drongelen
Nigel
N
Goldenfeld
Jack
J
Cowan
D000220:Adaptation, Biological / Q000502:physiology*; D005075:Biological Evolution; D006212:Hallucinations / Q000503:physiopathology*; D006801:Humans; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology; D009949:Orientation / Q000502:physiology*; D010364:Pattern Recognition, Visual / Q000502:physiology; D014793:Visual Cortex / Q000033:anatomy & histology* / Q000502:physiology