Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex

PLoS Biol. 2014 Oct 21;12(10):e1001965. doi: 10.1371/journal.pbio.1001965. eCollection 2014 Oct.

Abstract

Given the limited processing capabilities of the sensory system, it is essential that attended information is gated to downstream areas, whereas unattended information is blocked. While it has been proposed that alpha band (8-13 Hz) activity serves to route information to downstream regions by inhibiting neuronal processing in task-irrelevant regions, this hypothesis remains untested. Here we investigate how neuronal oscillations detected by electroencephalography in visual areas during working memory encoding serve to gate information reflected in the simultaneously recorded blood-oxygenation-level-dependent (BOLD) signals recorded by functional magnetic resonance imaging in downstream ventral regions. We used a paradigm in which 16 participants were presented with faces and landscapes in the right and left hemifields; one hemifield was attended and the other unattended. We observed that decreased alpha power contralateral to the attended object predicted the BOLD signal representing the attended object in ventral object-selective regions. Furthermore, increased alpha power ipsilateral to the attended object predicted a decrease in the BOLD signal representing the unattended object. We also found that the BOLD signal in the dorsal attention network inversely correlated with visual alpha power. This is the first demonstration, to our knowledge, that oscillations in the alpha band are implicated in the gating of information from the visual cortex to the ventral stream, as reflected in the representationally specific BOLD signal. This link of sensory alpha to downstream activity provides a neurophysiological substrate for the mechanism of selective attention during stimulus processing, which not only boosts the attended information but also suppresses distraction. Although previous studies have shown a relation between the BOLD signal from the dorsal attention network and the alpha band at rest, we demonstrate such a relation during a visuospatial task, indicating that the dorsal attention network exercises top-down control of visual alpha activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Attention / physiology*
  • Electroencephalography
  • Female
  • Humans
  • Magnetic Resonance Imaging
  • Male
  • Sensory Gating*
  • Space Perception
  • Visual Cortex / physiology*
  • Young Adult

Grant support

JMZ, OJ, and RS were supported by the Netherlands Organization for Scientific Research (NWO; www.nwo.nl) by the VICI scheme (453-09-002; http://www.nwo.nl/en/funding/our-funding-instruments/nwo/innovational-research-incentives-scheme/vici/index.html). OJ was supported by the Netherlands Initiative for Brain and Cognition “The healthy brain” scheme (056-14-011; https://www.hersenenencognitie.nl). RS was supported by the Netherlands Organization for Scientific Research (NWO; www.nwo.nl) by the Veni scheme (451-12-021; http://www.nwo.nl/en/funding/our-funding-instruments/nwo/innovational-research-incentives-scheme/veni/index.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.