Spatial summation revealed in the earliest visual evoked component C1 and the effect of attention on its linearity

Abstract

In natural scenes, multiple objects are usually presented simultaneously. How do specific areas of the brain respond to multiple objects based on their responses to each individual object? Previous functional magnetic resonance imaging (fMRI) studies have shown that the activity induced by a multiobject stimulus in the primary visual cortex (V1) can be predicted by the linear or nonlinear sum of the activities induced by its component objects. However, there has been little evidence from electroencephelogram (EEG) studies so far. Here we explored how V1 responded to multiple objects by comparing the EEG signals evoked by a three-grating stimulus with those evoked by its two components (the central grating and 2 flanking gratings). We focused on the earliest visual component C1 (onset latency of ∼50 ms) because it has been shown to reflect the feedforward responses of neurons in V1. We found that when the stimulus was unattended, the amplitude of the C1 evoked by the three-grating stimulus roughly equaled the sum of the amplitudes of the C1s evoked by its two components, regardless of the distances between these gratings. When the stimulus was attended, this linear spatial summation existed only when the three gratings were far apart from each other. When the three gratings were close to each other, the spatial summation became compressed. These results suggest that the earliest visual responses in V1 follow a linear summation rule when attention is not involved and that attention can affect the earliest interactions between multiple objects.