Reward processing in the value-driven attention network: reward signals tracking cue identity and location

Abstract

Through associative reward learning, arbitrary cues acquire the ability to automatically capture visual attention. Previous studies have examined the neural correlates of value-driven attentional orienting, revealing elevated activity within a network of brain regions encompassing the visual corticostriatal loop [caudate tail, lateral occipital complex (LOC) and early visual cortex] and intraparietal sulcus (IPS). Such attentional priority signals raise a broader question concerning how visual signals are combined with reward signals during learning to create a representation that is sensitive to the confluence of the two. This study examines reward signals during the cued reward training phase commonly used to generate value-driven attentional biases. High, compared with low, reward feedback preferentially activated the value-driven attention network, in addition to regions typically implicated in reward processing. Further examination of these reward signals within the visual system revealed information about the identity of the preceding cue in the caudate tail and LOC, and information about the location of the preceding cue in IPS, while early visual cortex represented both location and identity. The results reveal teaching signals within the value-driven attention network during associative reward learning, and further suggest functional specialization within different regions of this network during the acquisition of an integrated representation of stimulus value.

Keywords: attention networks; fMRI; reward learning; selective attention; vision.

Fig. 1

Sequence and time course of the events for a trial. Participants searched for a color-defined target (red or green) and reported the orientation of the bar within the target as vertical or horizontal. Correct responses resulted in a small amount of money added to the participant's bank total. One color target yielded a high reward for correct responses on 80% of trials (high-reward target), whereas the other color target yielded a high reward on only 20% of correct response trials (low-reward target).

Fig. 2

The value-driven attention network as revealed by contrasting high- vs low-reward feedback. Voxels shown were more active in response to high vs low reward at P < 0.001 in each of the two experiments, reflecting a robust reward signal in visual areas. LOC, lateral occipital complex; IPS, intraparietal sulcus.

Fig. 3

Mean beta-weights for responses to high-reward feedback when the preceding target was presented in the contralateral vs ipsilateral hemifield by region. Reward signals in both the IPS and early visual cortex were modulated by the position of the preceding target. Error bars reflect the SEM *P < 0.05.

Fig. 4

Regions in which reward prediction error signals were evident. (A) A significant interaction between value (i.e. the magnitude of reward feedback) and expectation (based on the reward probabilities assigned to the target color) was evident in the right OFC. (B) A main effect of expectation, with a stronger response for expected rewards, was evident in a region encompassing the posterior cingulate and ventral precuneus.