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

Matthew W Self, Judith C Peters, Jessy K Possel, Joel Reithler, Rainer Goebel, Peterjan Ris, Danique Jeurissen, Leila Reddy, Steven Claus, Johannes C Baayen, Pieter R Roelfsema

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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.

Original languageEnglish
Article numbere1002420
Number of pages26
JournalPLoS Biology
Volume14
Issue number3
DOIs
Publication statusPublished - Mar 2016

Keywords

  • MACAQUE V1 NEURONS
  • FIGURE-GROUND SEGREGATION
  • VENTRAL EXTRASTRIATE CORTEX
  • OBJECT-BASED ATTENTION
  • RECEPTIVE-FIELDS
  • SURROUND SUPPRESSION
  • STRIATE CORTEX
  • AREA V1
  • ORIENTATION SELECTIVITY
  • FUNCTIONAL ARCHITECTURE

Cite this

Self, Matthew W ; Peters, Judith C ; Possel, Jessy K ; Reithler, Joel ; Goebel, Rainer ; Ris, Peterjan ; Jeurissen, Danique ; Reddy, Leila ; Claus, Steven ; Baayen, Johannes C ; Roelfsema, Pieter R. / The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex. In: PLoS Biology . 2016 ; Vol. 14, No. 3.
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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.",
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Self, MW, Peters, JC, Possel, JK, Reithler, J, Goebel, R, Ris, P, Jeurissen, D, Reddy, L, Claus, S, Baayen, JC & Roelfsema, PR 2016, 'The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex', PLoS Biology , vol. 14, no. 3, e1002420. https://doi.org/10.1371/journal.pbio.1002420

The Effects of Context and Attention on Spiking Activity in Human Early Visual Cortex. / Self, Matthew W; Peters, Judith C; Possel, Jessy K; Reithler, Joel; Goebel, Rainer; Ris, Peterjan; Jeurissen, Danique; Reddy, Leila; Claus, Steven; Baayen, Johannes C; Roelfsema, Pieter R.

In: PLoS Biology , Vol. 14, No. 3, e1002420, 03.2016.

Research output: Contribution to journalArticleAcademicpeer-review

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KW - STRIATE CORTEX

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