Surround suppression supports second-order feature encoding by macaque V1 and V2 neurons

Luke E. Hallum, J. Anthony Movshon

Research output: Contribution to journalArticle

Abstract

Single neurons in areas V1 and V2 of macaque visual cortex respond selectively to luminance-modulated stimuli. These responses are often influenced by context, for example when stimuli extend outside the classical receptive field (CRF). These contextual phenomena, observed in many sensory areas, reflect a fundamental cortical computation and may inform perception by signaling second-order visual features which are defined by spatial relationships of contrast, orientation and spatial frequency. In the anesthetized, paralyzed macaque, we measured single-unit responses to a drifting preferred sinusoidal grating; low spatial frequency sinusoidal contrast modulations were applied to the grating, creating contrast-modulated, second-order forms. Most neurons responded selectively to the orientation of the contrast modulation of the preferred grating and were therefore second-order orientation-selective. Second-order selectivity was created by the asymmetric spatial organization of the excitatory CRF and suppressive extraclassical surround. We modeled these receptive field subregions using spatial Gaussians, sensitive to the modulation of contrast (not luminance) of the preferred carrier grating, that summed linearly and were capable of recovering asymmetrical receptive field organizations. Our modeling suggests that second-order selectivity arises both from elongated excitatory CRFs, asymmetrically organized extraclassical surround suppression, or both. We validated the model by successfully testing its predictions against conventional surround suppression measurements and spike-triggered analysis of second-order form responses. Psychophysical adaptation measurements on human observers revealed a pattern of second-order form selectivity consistent with neural response patterns. We therefore propose that cortical cells in primates do double duty, providing signals about both first- and second-order forms.

Original languageEnglish (US)
Pages (from-to)24-35
Number of pages12
JournalVision Research
Volume104
DOIs
StatePublished - Nov 1 2014

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Macaca
Neurons
Visual Cortex
Primates

Keywords

  • Filter-rectify-filter
  • Primary visual cortex
  • Receptive field
  • Second-order
  • Surround suppression
  • V2

ASJC Scopus subject areas

  • Ophthalmology
  • Sensory Systems

Cite this

Surround suppression supports second-order feature encoding by macaque V1 and V2 neurons. / Hallum, Luke E.; Movshon, J. Anthony.

In: Vision Research, Vol. 104, 01.11.2014, p. 24-35.

Research output: Contribution to journalArticle

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