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

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.

Dynamic Normalization

“…3e). These results are similar to a variety of electrophysiological measurements (50,58,84,(113)(114)(115)(116)(117)(118).…”

“…All of these results, except for one, are commensurate with experimental observations that oscillation amplitudes and frequencies depend systematically on stimulus contrast, size, and spatial pattern (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86), and that oscillations are linked to normalization (31,72). Like the simulation results, oscillation amplitudes have been observed to increase with stimulus contrast and size, oscillation frequencies increase with stimulus contrast, and oscillations are smaller for plaids than for gratings (and even smaller for stimuli composed of multiple components, also predicted by the model).…”

“…LFPs exhibit so-called gamma oscillations (~30-80 Hz) that have also been linked to normalization (31,72). Oscillation amplitude and frequency depend systematically on stimulus contrast, size, and spatial pattern (31,(72)(73)(74)(75)(76)(77)(78)(79)(80)(81)(82)(83)(84)(85)(86).…”

Layer-specificity in the effects of attention and working memory on activity in primary visual cortex

“…The speed at which the enhanced neuronal activity spreads over the target curve is comparable to the speed with which human observers trace the curve27. Furthermore, it was recently shown that neuronal firing rates in the human visual cortex elicited by target curves are higher than those elicited by distractors, just as is the case in monkey visual cortex30. Thus, the curve-tracing task is useful to study the top-down influences related to perceptual organization and object-based attention in the visual cortex25.…”

Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala

“…This will require human single-neuron latency estimates in higher cortical visual areas, which have not been performed to date. Notably, recordings from early visual areas V2/V3 in humans indicate that the response latencies in these areas do not differ between monkeys and humans (Self et al, 2016). This raises the possibility that local processing in higher areas specific to humans is responsible for this substantial increase in response latency.…”