The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex

PLoS Biol. 2016 Mar 25;14(3):e1002420. doi: 10.1371/journal.pbio.1002420. eCollection 2016 Mar.

Abstract

Here we report the first quantitative analysis of spiking activity in human early visual cortex. We recorded multi-unit activity from two electrodes in area V2/V3 of a human patient implanted with depth electrodes as part of her treatment for epilepsy. We observed well-localized multi-unit receptive fields with tunings for contrast, orientation, spatial frequency, and size, similar to those reported in the macaque. We also observed pronounced gamma oscillations in the local-field potential that could be used to estimate the underlying spiking response properties. Spiking responses were modulated by visual context and attention. We observed orientation-tuned surround suppression: responses were suppressed by image regions with a uniform orientation and enhanced by orientation contrast. Additionally, responses were enhanced on regions that perceptually segregated from the background, indicating that neurons in the human visual cortex are sensitive to figure-ground structure. Spiking responses were also modulated by object-based attention. When the patient mentally traced a curve through the neurons' receptive fields, the accompanying shift of attention enhanced neuronal activity. These results demonstrate that the tuning properties of cells in the human early visual cortex are similar to those in the macaque and that responses can be modulated by both contextual factors and behavioral relevance. Our results, therefore, imply that the macaque visual system is an excellent model for the human visual cortex.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Adult
  • Animals
  • Attention / physiology
  • Female
  • Humans
  • Macaca
  • Magnetic Resonance Imaging
  • Visual Cortex / physiology*
  • Visual Perception / physiology*

Grants and funding

This work was supported by NWO (OnderzoeksTalent 406-12-072 awarded to MWS and JKP, Brain and Cognition grant 433-09-208 and ALW grant 823-02-010 awarded to PRR), the European Union’s Seventh Framework Program (Marie-Curie Action PITN-GA-2011-290011 awarded to PRR, ERC advanced grant #339490 awarded to PRR, ERC advanced grant #269853 awarded to RG, and HBP competitive call #604102 awarded to RG), as well as a Neuroscience Campus Amsterdam proof of concept grant awarded to PRR. http://www.nwo.nl/. http://ec.europa.eu/research/fp7/index_en.cfm. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.