Context-dependent reward-driven modulation of perception

147

between reward and sensory integration processing may occur that can be categorized as whether reward and multisensory integration occur at the same stage and hence reward is processed in a supra-additive principle (i.e. the response of the multisensory cues exceeded the sum of responses of the unisensory cues), a hallmark of multisensory integration phenomena (Stein et al., 1993; Stein and Stanford, 2008), or they are two independent mechanisms that may affect each other at different stages of processing. Our evidence pointed out that the two systems are regulated independently, as indexed by the response time and the neural correlates.

Specifically, we observed that reward effects accelerated the response similarly across sensory configurations and supra-additive sensory integration was evident in the multisensory cues, but there was no interaction between reward and sensory integration. Similarly, the neural correlates demonstrated that reward modulation was observed pre-dominantly in the midbrain, while multisensory integration was modulating the superior temporal areas, typical areas that have been linked to the processing of multimodal cues (Calvert et al., 2001). Interestingly, areas in the Caudate responded to both reward and sensory integration. However, the areas regulating the two processes were not overlapping, indicating different functionalities exist within the Caudate structure. Hence, our evidence demonstrated that reward is immune to the supra- additive integration processes, indicating that reward is regulated independently from sensory integration. Specifically, the results are aligned with the second proposal, where the two systems are independent as they occurred at different stages of processing. However, in the paradigm employed to test reward interaction with multisensory processes, we held the uncertainty for reward and sensory information at a constant level. It is interesting for future studies to test whether the two systems might develop a dependency when the ambiguity of the reward and/or sensory information is increased.

148

The stronger modulation of reward in performance contingent reward is aligned with the previous literature that demonstrated when reward was associated with a task-relevant feature, reward enhances perception by engaging attentional and motivational networks in the brain to modulate the target sensory perceptual areas (Chelazzi et al., 2013; Pessoa, 2015). Therefore, the contingency of reward to performance enables reward to access higher cognitive resources (Pessoa, 2009, 2015) and behaviorally can be observed as the reward modulation of pupillary dilation and energized behavior (i.e. faster response time). Moreover, as a preliminary observation in Figure 1, the strongest areas in the striatum were recruited during the conditioning phase in the second study and the reward effects across sensory configuration in the third study. This observation is aligned with the previous study demonstrating that the striatum received a dopaminergic projection (Schultz, 2000) and is related to the integration of motivational and goal-directed behavior (Delgado, 2007).

In contrast, when reward deliveries were halted, previous studies showed divergent reward modulation: when reward cues were irrelevant to the task at hand, reward-driven modulation captured attention away from the target and impaired performance (Anderson et al., 2011;

Anderson and Yantis, 2012; Qin et al., 2020; Watson et al., 2020) or reward effect on the target persisted, engaging a mechanism that continues to facilitate performance (Leo and Noppeney, 2014; Pooresmaeili et al., 2014; De Tommaso et al., 2017). Therefore, what underlies the divergent observations in the previously rewarded cues? There are two possibilities: the first one is based on the previous studies employing cross-modal previously reward-associated cues (Leo and Noppeney, 2014; Pooresmaeili et al., 2014). In these studies, by signaling reward from another sensory modality, reward might engage a dissociated mechanism that is not overlapping with the attentional mechanism required for processing the target, hence utilizing independent resources as used by the target cues. The second factor is the spatial relationship between the reward and target cues. For instance, as reward and the target cues were located or trained at the same spatial location, previously reward-associated cues facilitated perceptual decision- making (De Tommaso, 2017; Pooresmaeili et al., 2014). In contrast, as the reward and target cues were separated spatially, previously-rewarded cues captured the attention and impaired performance (Anderson et al., 2011; Theeuwes and Belopolsky, 2012). Thus, the spatial position determined whether reward-driven modulation may facilitate or impair the performance of the target cues.

149

Supporting the claim of existing dissociation between performance-contingent and previously rewarded cues, previous studies examining the neural correlation underlying the previously rewarded cues demonstrated that reward relies on other neural mechanisms, without the involvement of the striatum (Kim and Anderson, 2019). Instead, as observed from our second study, reward-driven modulation relies on another neural mechanism involving the frontal- parietal areas, such as the lateral orbitofrontal and anterior intraparietal areas, and sensory association areas in the superior temporal. Furthermore, previous studies comparing the neural underpinnings of reward-driven modulation on task relevance also demonstrated that there is a dissociation between the task-relevant and task-irrelevant reward association, where for instance the nucleus accumbens was engaged in a task-relevant association, while task- irrelevant reward association rather involved the medial frontal areas in the pre-supplementary motor areas (Krebs et al., 2011).

Moreover, not only the distinction between reward modulation in the context of reward contingency relies on the switch of neural mechanisms mentioned above, but also reward- driven effects became dependent on which sensory modality the reward was signaled from. In our second study, we examined the underlying neural mechanism of the intra- and cross-modal previously rewarded cues using effective connectivity. Our effective connectivity results revealed a dissociated pathway for the intra- and cross-modal cues, where intra-modal cues were mediated through attention-related areas in the anterior intraparietal, and cross-modal cues were mediated through both attention-related and sensory association areas in the superior temporal. Our findings are aligned with a previous study observing modulation by cross-modal reward-associated cues in the superior temporal sulcus, indexed by an increase in the BOLD response magnitude for high compared to low reward conditions (Pooresmaeili et al., 2014).

Extending the findings from the previous study (Pooresmaeili et al., 2014), we observed further a dissociation in how the direction of reward modulation depended on the sensory modality of the. Specifically, the results can be divided into two observations. First, as the intra-modal cues relied on an excitatory modulation from attention-related to reward-related areas (i.e.

feedforward), cross-modal cues relied on inhibitory modulation. The excitation in the intra- modal cues might reflect an enhancement of the reward-driven saliency, where higher reward associated percept had more gain and thus were represented in the higher valuation area more effectively (Hickey and Peelen, 2017). In contrast, the inhibition in the cross-modal cues between the attention- and reward-related areas might reflect the suppression of the irrelevant sensory features in the auditory to enhance the visual target. Second, the communication

150

between the early visual areas and the mediation areas (i.e. IPS for intra-modal, STS for cross- modal cues) also differed. Specifically, as intra-modal cues relied on inhibitory feedback communication, cross-modal cues relied on excitatory feedback and feedforward communication. The inhibition in the intra-modal cues might reflect a down-weighting of the reward cues, hence enabling the target to access the resources in the early visual areas.

Meanwhile, there was no necessity for the cross-modal reward information to be suppressed, as the reward cues originated from different sources (i.e. another sensory modality), thus there was no competition of resources between the cue and the target. Our findings are aligned with a previous electrophysiological study, demonstrating competition of the intra-modal reward associated cues that were reflected in the early suppression, as observed in the depression of P1 component in the early visual areas, whereas cross-modal cues were observed to be enhanced at a later stage, as indexed by the N1 component facilitation (Vakhrushev et al., 2021).

In summary, we demonstrated that there are dependencies observed in how reward is regulated under different contexts of reward cueing. The dissociation lies in which resources reward can access, such as when reward was contingent on the performance, reward may mobilize different resources from the higher cognition, resulting in a more effective behavior. Meanwhile, previously rewarded cues engaged other mechanisms that regulate goal-directed behavior, involving areas in the frontal and parietal (Corbetta and Shulman, 2002; Pessoa, 2015). As reward relies on a more specific mechanism, other factors, such as the source of the reward cues signal also play a role, dictating how reward would be communicated to aid goal-directed behavior.