Human primary visual cortex (V1) is selective for second-order spatial frequency

J Neurophysiol. 2011 May;105(5):2121-31. doi: 10.1152/jn.01007.2010. Epub 2011 Feb 23.

Abstract

A variety of cues can differentiate objects from their surrounds. These include "first-order" cues such as luminance modulations and "second-order" cues involving modulations of orientation and contrast. Human sensitivity to first-order modulations is well described by a computational model involving spatially localized filters that are selective for orientation and spatial frequency (SF). It is widely held that first-order modulations are represented by the firing rates of simple and complex cells ("first-order" neurons) in primary visual cortex (V1) that, likewise, have spatially localized receptive fields that are selective for orientation- and SF. Human sensitivity to second-order modulations is well described by a filter-rectify-filter (FRF) model, with first- and second-order filters selective for orientation and SF. However, little is known about how neuronal activity in visual cortex represents second-order modulations. We tested the FRF model by using an functional (f)MRI-adaptation protocol to characterize the selectivity of activity in visual cortex to second-order, orientation-defined gratings of two different SFs. fMRI responses throughout early visual cortex exhibited selective adaptation to these stimuli. The low-SF grating was a more effective adapter than the high-SF grating, incompatible with the FRF model. To explain the results, we extended the FRF model by incorporating normalization, yielding a filter-rectify-normalize-filter model, in which normalization enhances selectivity for second-order SF but only for low spatial frequencies. We conclude that neurons in human visual cortex are selective for second-order SF, that normalization (surround suppression) contributes to this selectivity, and that the selectivity in higher visual areas is simply fed forward from V1.

Publication types

  • Randomized Controlled Trial
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adaptation, Ocular / physiology
  • Adult
  • Humans
  • Magnetic Resonance Imaging / methods
  • Middle Aged
  • Orientation / physiology*
  • Photic Stimulation / methods*
  • Reaction Time / physiology
  • Space Perception / physiology*
  • Visual Cortex / physiology*
  • Young Adult