Emergence of neuronal signals supporting naturalistic texture discrimination

C M Ziemba, R L T Goris, G M Stine, E P Simoncelli and J A Movshon

Published in Computational and Systems Neuroscience (CoSyNe), Feb 2016.

In anesthetized macaque monkeys, neuronal sensitivity to complex features of visual textures is substantially stronger in V2 than in V1, suggesting that V2 neuronal activity might directly support texture perception. To test this idea, we investigated the relationship between single neuron activity in V1 and V2 and simultaneously measured psychophysical judgments of texture. We generated stimuli along a continuum between naturalistic texture and spectrally-matched, phase-randomized noise, and trained macaque monkeys to classify them according to which end of this "naturalness" continuum they resembled. Monkeys learned to discriminate briefly presented (500 ms) near-peripheral stimuli well, with performance rivaling that of human observers. The firing rates of single V1 and V2 neurons carried much less information about texture naturalness than the behavioral reports, although V2 neurons were significantly more sensitive than V1 neurons on average. Selectivity for naturalness evolved with a time course that differed across areas. In V2, selectivity emerged early and peaked 50 ms after the initial transient. In V1, selectivity was initially absent, but increased gradually throughout the stimulus period. Both V1 and V2 showed significant decision-related activity: choice probability was modest but significant, and of similar magnitude in V1 and V2. Mirroring the difference in the dynamics of selectivity, decision-related activity in the two areas evolved with different time courses: choice probability emerged early in V2 and remained stable, but emerged later and more gradually in V1. Together, these results suggest that V2 establishes sensitivity to naturalistic visual structure, and feeds this information back to V1. The comparatively weak sensitivity of single neurons suggests that texture perception likely arises from the combined activity of many V2 neurons, and may be further consolidated downstream.
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