Decoding the temporal dynamics of affective scene processing.

Natural images containing affective scenes are used extensively to investigate the neural mechanisms of visual emotion processing. Functional fMRI studies have shown that these images activate a large-scale distributed brain network that encompasses areas in visual, temporal, and frontal cortices. The underlying spatial and temporal dynamics, however, remain to be better characterized. We recorded simultaneous EEG-fMRI data while participants passively viewed affective images from the International Affective Picture System (IAPS). Applying multivariate pattern analysis to decode EEG data, and representational similarity analysis to fuse EEG data with simultaneously recorded fMRI data, we found that: (1) ∼80 ms after picture onset, perceptual processing of complex visual scenes began in early visual cortex, proceeding to ventral visual cortex at ∼100 ms, (2) between ∼200 and ∼300 ms (pleasant pictures: ∼200 ms; unpleasant pictures: ∼260 ms), affect-specific neural representations began to form, supported mainly by areas in occipital and temporal cortices, and (3) affect-specific neural representations were stable, lasting up to ∼2 s, and exhibited temporally generalizable activity patterns. These results suggest that affective scene representations in the brain are formed temporally in a valence-dependent manner and may be sustained by recurrent neural interactions among distributed brain areas.

Decoding Neural Representations of Affective Scenes in Retinotopic Visual Cortex.

The perception of opportunities and threats in complex visual scenes represents one of the main functions of the human visual system. The underlying neurophysiology is often studied by having observers view pictures varying in affective content. It has been shown that viewing emotionally engaging, compared with neutral, pictures (1) heightens blood flow in limbic, frontoparietal, and anterior visual structures and (2) enhances the late positive event-related potential (LPP). The role of retinotopic visual cortex in this process has, however, been contentious, with competing theories predicting the presence versus absence of emotion-specific signals in retinotopic visual areas. Recording simultaneous electroencephalography-functional magnetic resonance imaging while observers viewed pleasant, unpleasant, and neutral affective pictures, and applying multivariate pattern analysis, we found that (1) unpleasant versus neutral and pleasant versus neutral decoding accuracy were well above chance level in retinotopic visual areas, (2) decoding accuracy in ventral visual cortex (VVC), but not in early or dorsal visual cortex, was correlated with LPP, and (3) effective connectivity from amygdala to VVC predicted unpleasant versus neutral decoding accuracy, whereas effective connectivity from ventral frontal cortex to VVC predicted pleasant versus neutral decoding accuracy. These results suggest that affective scenes evoke valence-specific neural representations in retinotopic visual cortex and that these representations are influenced by reentry signals from anterior brain regions.

Aversive perception in a threat context: Separate and independent neural activation.

Unpleasant, compared to neutral, scenes reliably prompt enhanced functional brain activity in the amygdala and inferotemporal cortex. Considering data from psychophysiological studies in which defensive reactivity is further enhanced when viewing unpleasant scenes under threat of shock (compared to safety), the current study investigates functional activation in the amygdala-inferotemporal circuit when unpleasant (or neutral) scenes are viewed under threat of shock or safety. In this paradigm, a cue signaling threat or safety was presented in conjunction with either an unpleasant or neutral picture. Replicating previous studies, unpleasant, compared to neutral, scenes reliably enhanced activation in the amygdala and inferotemporal cortex. Functional activity in these regions, however, did not differ whether scenes were presented in a context threatening shock exposure, compared to safety, which instead activated regions of the anterior insula and cingulate cortex. Taken together, the data support a view in which neural regions activated in different defensive situations act independently.