A Normalization Framework for Emotional Attention

The normalization model of attention proposes that attention can affect performance by response- or contrast-gain changes, depending on the size of the stimulus and attention field. Here, we manipulated the attention field by emotional valence, negative faces versus positive faces, while holding stimulus size constant in a spatial cueing task. We observed changes in the cueing effect consonant with changes in response gain for negative faces and contrast gain for positive faces. Neuroimaging experiments confirmed that subjects’ attention fields were narrowed for negative faces and broadened for positive faces. Importantly, across subjects, the self-reported emotional strength of negative faces and positive faces correlated, respectively, both with response- and contrast-gain changes and with primary visual cortex (V1) narrowed and broadened attention fields. Effective connectivity analysis showed that the emotional valence-dependent attention field was closely associated with feedback from the dorsolateral prefrontal cortex (DLPFC) to V1. These findings indicate a crucial involvement of DLPFC in the normalization processes of emotional attention.Using a combination of psychophysics and functional MRI, this study reveals that emotional attention interacts with normalization processes depending on emotional valence (positive or negative faces), best explained by feedback modulation from the dorsolateral prefrontal cortex.Author Summary: Attentional selection is the mechanism by which the subset of incoming information is preferentially processed at the expense of distractors. The normalization model of attention suggests that attention-triggered modulatory effects on sensory responses in the visual cortex depend on two factors: the stimulus size and the attention field size. However, little is known regarding whether emotional attention shapes perception by means of the normalization framework. To test this hypothesis, we manipulated the attention field by emotional valence—negative faces versus positive faces—while holding the stimulus size constant in a spatial cueing task. We observed that attention increased response gain for negative faces, with the largest cueing effects occurring at high contrasts and little to no effect at low and mid-contrasts; however, attention increased contrast gain for positive faces, with the largest cueing effects occurring at mid-contrasts and little to no effect at low and high contrasts. A complementary neuroimaging experiment confirmed that subjects' attention fields were narrowed for negative faces and broadened for positive faces. Across subjects, the self-reported emotional strength of negative faces and positive faces correlated, respectively, both with response-gain and contrast-gain changes and with narrowed and broadened attention fields in the primary visual cortex. Mechanistically, we found that the emotional valence-dependent attention field was closely associated with feedback from the dorsolateral prefrontal cortex to the primary visual cortex. Our findings provide evidence for a normalization framework for emotional attention and for the critical role of feedback from the prefrontal cortex to the early visual cortex in this normalization.