Human Visual Cortex Responses to Rapid Cone and Melanopsin-Directed Flicker

J Neurosci. 2016 Feb 3;36(5):1471-82. doi: 10.1523/JNEUROSCI.1932-15.2016.

Abstract

Signals from cones are recombined in postreceptoral channels [luminance, L + M; red-green, L - M; blue-yellow, S - (L + M)]. The melanopsin-containing retinal ganglion cells are also active at daytime light levels and recent psychophysical results suggest that melanopsin contributes to conscious vision in humans. Here, we measured BOLD fMRI responses to spectral modulations that separately targeted the postreceptoral cone channels and melanopsin. Responses to spatially uniform (27.5° field size, central 5° obscured) flicker at 0.5, 1, 2, 4, 8, 16, 32, and 64 Hz were recorded from areas V1, V2/V3, motion-sensitive area MT, and the lateral occipital complex. In V1 and V2/V3, higher temporal sensitivity was observed to L + M + S (16 Hz) compared with L - M flicker (8 Hz), consistent with psychophysical findings. Area MT was most sensitive to rapid (32 Hz) flicker of either L + M + S or L - M. We found S cone responses only in areas V1 and V2/V3 (peak frequency: 4-8 Hz). In addition, we studied an L + M modulation and found responses that were effectively identical at all temporal frequencies to those recorded for the L + M + S modulation. Finally, we measured the cortical response to melanopsin-directed flicker and compared this response with control modulations that addressed stimulus imprecision and the possibility of stimulation of cones in the shadow of retinal blood vessels (penumbral cones). For our stimulus conditions, melanopsin flicker did not elicit a cortical response exceeding that of the control modulations. We note that failure to control for penumbral cone stimulation could be mistaken for a melanopsin response.

Significance statement: The retina contains cone photoreceptors and ganglion cells that contain the photopigment melanopsin. Cones provide brightness and color signals to visual cortex. Melanopsin influences circadian rhythm and the pupil, but its contribution to cortex and perception is less clear. We measured the response of human visual cortex with fMRI using spectral modulations tailored to stimulate the cones and melanopsin separately. We found that cortical responses to cone signals vary systematically across visual areas. Differences in temporal sensitivity for achromatic, red-green, and blue-yellow stimuli generally reflect the known perceptual properties of vision. We found that melanopsin signals do not produce a measurable response in visual cortex at temporal frequencies between 0.5 and 64 Hz at daytime light levels.

Keywords: color vision; flicker; ipRGCs; melanopsin; temporal sensitivity; visual cortex.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Female
  • Flicker Fusion / physiology*
  • Humans
  • Magnetic Resonance Imaging / methods
  • Male
  • Photic Stimulation / methods*
  • Pupil / physiology*
  • Retinal Cone Photoreceptor Cells / metabolism*
  • Rod Opsins / metabolism*
  • Visual Cortex / metabolism*

Substances

  • Rod Opsins
  • melanopsin