Affective facilitation of early visual cortex during rapid picture presentation at 6 and 15 Hz

Abstract

The steady-state visual evoked potential (SSVEP), a neurophysiological marker of attentional resource allocation with its generators in early visual cortex, exhibits enhanced amplitude for emotional compared to neutral complex pictures. Emotional cue extraction for complex images is linked to the N1-EPN complex with a peak latency of ∼140-160 ms. We tested whether neural facilitation in early visual cortex with affective pictures requires emotional cue extraction of individual images, even when a stream of images of the same valence category is presented. Images were shown at either 6 Hz (167 ms, allowing for extraction) or 15 Hz (67 ms per image, causing disruption of processing by the following image). Results showed SSVEP amplitude enhancement for emotional compared to neutral images at a presentation rate of 6 Hz but no differences at 15 Hz. This was not due to featural differences between the two valence categories. Results strongly suggest that individual images need to be displayed for sufficient time allowing for emotional cue extraction to drive affective neural modulation in early visual cortex.

Keywords: SSVEP; attention; emotional cue extraction; human early visual cortex.

Fig. 1.

Experimental design. Unpleasant and neutral picture scenes presented in a rapid visual serial presentation for ∼67 ms (15 Hz, Experiment 1) or ∼167 ms (6 Hz, Experiments 2 and 3). (A) Trial with a change in affective content of images: from neutral to unpleasant. (B) Trial with a change from unpleasant to neutral. (C) Example of spectrally equivalent, phase-scrambled image with an unpleasant content of the last unpleasant image in the sequence from 1A. (D) Example of spectrally equivalent, phase-scrambled image with a neutral content (corresponds to the last neutral image in the sequence from 1B). Note: Examples for unpleasant and neutral pictures are taken from GAPED database (Dan-Glauser and Scherer, 2011).

Fig. 2.

Left: Gabor filtered time course of 15 Hz SSVEP amplitudes for the stream of unpleasant and neutral pictures with a change in emotional content (upper panel) and without such a change (lower panel). Time point zero shows the onset of change in emotional content (or a corresponding time marker for conditions with no change). Right: Topographical distribution of grand average of 15 Hz SSVEP amplitude across all subjects and conditions for the entire epoch, i.e. 1 s before to 2 s after the change (or time marker).

Fig. 3.

Mean amplitude difference values (first minus second time window) for 15 Hz SSVEP in microvolts. Left panel: Trials with a change in emotional content. Right panel: Trials without a change in emotional content. Error bars represent 95% CIs.

Fig. 4.

SPMs of the 15 Hz SSVEP estimated cortical current source-density distributions averaged across all conditions. The scale represent t-values, the threshold 13.6 corresponds to P < 0.001 and was Bonferroni corrected for multiple comparisons.

Fig. 5.

Left: Gabor filtered time course of 6 Hz SSVEP amplitudes for the stream of unpleasant and neutral pictures with a change in emotional content (upper panel) and without such a change (lower panel). Time point zero shows the onset of change in emotional content. Right: The grand average of 6 Hz SSVEP amplitude across all subjects and conditions for the time period of 1 s before and 2 after the change in emotional content.

Fig. 6.

Mean amplitude difference values (first minus second time window) for 6 Hz SSVEP in microvolts. Left panel: Trials with a change in emotional content. Right panel: Trials without a change in emotional content. Error bars represent 95% CIs. Significant change corresponding to P-value < 0.01 is marked with *.

Fig. 7.

SPMs of the 6 Hz SSVEP estimated cortical current source-density distributions. The scale represent t-values, the threshold 13.6 corresponds to P < 0.001 and was Bonferroni corrected for multiple comparisons. (A) SPMs of the 6 Hz averaged across all conditions (B) SPMs of the contrast between unpleasant and neutral time windows (all unpleasant time windows tested against neutral time windows in the experiment).

Fig. 8.

Left: Gabor filtered time course of SSVEP amplitudes for the stream of concrete (upper panel) and scrambled (lower panel) unpleasant and neutral pictures with change in emotional content. Time point zero shows the onset of change in emotional content. Right: The grand average of 6 Hz SSVEP amplitude across all subjects and conditions for the time period of 1 s before and 2 after the change in emotional content.

Fig. 9.

Mean amplitude difference values (first minus second time window) in microvolts for intact (left panel) and scrambled (right panel) trials. Error bars represent 95% CIs. Significant change corresponding to P-value < 0.05 is marked with *.