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

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

doi:10.1371/journal.pbio.1002420

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.

Highlights

The early visual cortex consists of three areas, V1, V2, and V3, which provide a retinotopic map of the visual field
Our results demonstrate that spiking activity in human visual cortex shares many properties with that in macaque cortex, such as orientation and spatial frequency tuning, contrast saturation and surround suppression
We recorded the envelope of multi-unit spiking activity (MUA), thresholded spiking activity (MUAt), and local field potential (LFP) from microwires situated in early visual cortex from the left hemisphere of a 35-y-old, female patient (Fig 1A and S1 Fig)

Summary

Introduction

The early visual cortex consists of three areas, V1, V2, and V3, which provide a retinotopic map of the visual field. The pioneering work of Hubel and Wiesel revealed that cells in early visual areas respond to visual stimuli in their receptive field, a circumscribed region of the retina. Visual cortical neurons are typically tuned for orientation [1] and spatial frequency [2] and give saturating responses when the contrast of the stimulus increases [3]. Later studies revealed that the neuronal responses in early visual cortex can be modified by the context set by image elements outside the neurons’ receptive field. Texturedefined figures elicit stronger responses than textured backgrounds if the receptive field stimulus is held constant [4], and cognitive factors such as visual attention influence the neuronal responses [5]

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