PMC:2940450 / 4441-16860 JSONTXT

{"target":"https://pubannotation.org/docs/sourcedb/PMC/sourceid/2940450","sourcedb":"PMC","sourceid":"2940450","source_url":"https://www.ncbi.nlm.nih.gov/pmc/2940450","text":"Effects of Reward on Executive Function\n\nParametric increases in behavioral performance and activation strength in the fronto-parietal attentional network\nHere, we review evidence indicating that motivational factors guide perceptual and executive control processes, likely by modulating both bottom-up and top-down processes, thereby helping to solve the limited processing-resources dilemma. In a series of experiments, Engelmann and Pessoa (2007)andEngelmann et al. (2009) investigated the effects of motivation on task performance by probing the effects of parametric changes in incentive value on behavior during difficult spatial localization tasks. Participants were asked to indicate the location of a target stimulus (e.g., degraded face) relative to that of a distracter stimulus (e.g., random noise) as quickly and accurately as possible. Attention was manipulated by using a central cue that predicted target location with 70% validity (such that 30% of the time the cue indicated the incorrect target location) – in such cases, performance during validly cued trials is known to exceed that during invalidly cued ones. Motivation was parametrically manipulated in a blocked fashion by linking payoff to behavioral performance (if performance was both accurate and fast in a given block of trials, participants were given the chance to win cash incentives that varied from $0–$4, or to avoid losing money).\nOur behavioral findings revealed improved detection performance as a function of absolute incentive value (Figure 1A). Critically, because behavior was characterized via the detection sensitivity measure d′, the results revealed a “specific” effect of motivation on behavioral performance, instead of more unspecific influences such as arousal (e.g., purely faster response times) or response bias (e.g., more conservative responses) – but see below for further discussion on more general effects that may be, at least in part, linked to arousal. The same basic pattern of behavioral results was observed in three distinct versions of the task that varied in difficulty level, the type of target and distracter stimuli, and cue types (endogenous vs exogenous).\nFigure 1 Behavioral and neural effects of incentive motivation. (A) In all experiments, the detection sensitivity measure dprime (dp) increased as a function of absolute incentive magnitude. Red line: experiment 1 of Engelmann and Pessoa (2007); light orange line: experiment 2 of Engelmann and Pessoa (2007); dark red line: behavioral results of Engelmann et al. (2009). Parallel increases in evoked brain responses observed in the study by Engelmann et al. (2009) during the cue (B) and target (C) task phases in three types of regions, namely attentional, visual and reward-related (see Figure 2 for some of the sites). Results were obtained by pooling the responses from regions within these three networks. Net = network. One of the versions of the behavioral task was accompanied by fMRI scanning (Engelmann et al., 2009), allowing us to probe the neural basis of enhanced performance by incentive motivation. Specifically, we sought to elucidate the workings of “process-specific” effects of motivation on cue- and target-related processing during these attentional tasks. Non-specific motivational effects due to effort and arousal were removed by using a hybrid task design that included: (1) event-related (i.e., transient) components with relatively long, jittered and optimized intertrial and interstimulus intervals between cue and target periods; and (2) a blocked (i.e., sustained) motivational component. Hybrid designs allow for separate estimates of transient and sustained signals (Visscher et al., 2003). Importantly, transient processes could be dissociated from each other, i.e., cue- and target-related responses.\nIn parallel with the behavioral findings, the neuroimaging results revealed parametric increases in activation strength as a function of absolute incentive value in three types of brain regions (Figure 2): (i) fronto-parietal sites that are important for the control of attention, including frontal eye field (FEF), anterior cingulate cortex (ACC; and other sites along the midline), intraparietal sulcus (IPS) and temporo-parietal junction (TPJ); (ii) occipito-temporal visual cortical sites, including sites around the calcarine fissure and in the fusiform gyrus, a region that is sensitive to face stimuli (which were employed in the task); and (iii) nodes of the reward system, including caudate and substantia nigra (SN)/midbrain. Parametric influences of incentive motivation on evoked responses were obtained during both the cue (Figure 1B) and target (Figure 1C) periods. In particular, our findings concerning reward-related sites are consistent with previous reports of parametric response increases in the nucleus accumbens (e.g., Knutson et al., 2005), caudate nucleus (Delgado et al., 2003) and orbitofrontal cortex (e.g., O'Doherty et al., 2001). Taken together, our observations revealed that parametric improvements in detection performance were accompanied by systematic modulations in three sets of brain regions that, together, support task performance, namely attentional, visual and reward-related regions.\nFigure 2 Brain regions exhibiting correlations with absolute incentive magnitude during the cue and target task periods. Some of the attentional (blue font), visual (light green), and valuation (orange) regions are illustrated. ACC, anterior cingulate cortex; FEF, frontal eye field; IPS, intraparietal sulcus; pre-SMA, pre-supplementary motor area; and preSMA, pre-supplementary motor area.\n\nConverging evidence: motivational effects on cognitive and sensory processing\nOur findings support the notion that motivational signals act both at more “central” levels in fronto-parietal cortex and at sensory levels. Here, we briefly discuss other studies that support this view and, in particular, have evaluated how motivation influences cognitive function. In a study by Small et al. (2005), fast target detection could lead to monetary wins or avoidance of monetary losses and, in the control condition, did not involve monetary outcomes. Better performance during the disengagement of attention was associated with enhanced activity in the inferior parietal lobe in the vicinity of the TPJ, a region that has been implicated in the reorienting of attention. Importantly, this effect was enhanced by incentive motivation during trials in which participants could win or avoid losing money, and were accompanied by activations in valuation-related regions, including the orbitofrontal cortex. Of particular interest, responses in the posterior cingulate cortex (PCC) were correlated with visual spatial expectancy (defined as the degree to which the cue benefited performance as evidenced by faster reaction times), an effect that was enhanced by incentive motivation. Given the known connectivity of this region with areas of the brain involved in attention and motivational processing, it was proposed that the PCC serves as a neural interface between motivation and the top-down control of attention.\nA subsequent study by Mohanty et al. (2008) also investigated motivation effects on attention, this time manipulating motivational state, namely hunger. Specifically, in the context of a covert-orienting task with a central cue, participants detected motivationally relevant (food) or irrelevant (tools) targets under conditions of hunger and satiety. As in the study by Small et al., responses in sites in parietal cortex (e.g., intraparietal sulcus, IPS) exhibited correlations with the speed of attentional shifts that were sensitive to not just motivational state, but also to the motivational value of the target. Similar patterns were also observed in the PCC and the orbitofrontal cortex (OFC). Furthermore, amygdala, PCC, locus coeruleus and SN/midbrain showed sensitivity to food-related cues when hungry, but not when satiated, an effect that did not generalize to tools. These findings demonstrate that motivational state (hunger) modulates spatial attention via response modulations across several brain regions.\nGiven that the findings from the above studies are being explicitly related to those of our own neuroimaging study, it is of relevance to ascertain the degree of spatial concordance of the parietal activation sites. In some cases, the concordance was good when compared to other attentional studies in the literature (Corbetta et al., 2000; Hopfinger et al., 2000; Kincade et al., 2005), such as target-related activations in the IPS (distance between our study and relevant published reports: ∼6 mm). However, the concordance with the studies investigating attention and motivation per se (Small et al., 2005; Mohanty et al., 2008) was less impressive, such as ∼17 mm for the PCC, and even ∼23 mm for the TPJ. Hence, it will be important in the future to understand the reasons behind the sources of spatial variability.\nThe two studies reviewed above, in addition to our own work, provide evidence that motivation modulates fronto-parietal regions involved in attention. Additional evidence also supports the modulation of sensory cortex by motivation. For instance, Pantoja et al. (2007) investigated neuronal responses in the rat primary somatosensory cortex (S1) during a tactile discrimination task. Stimulus-related information encoded by S1 neuronal ensembles increased when the contingency between stimulus and response was crucial for reward, but not when reward was freely available. In addition, stimulus-related information was directly related to behavioral task performance. Related neuroimaging findings in humans were reported by Pleger et al. (2008, 2009), who used a tactile discrimination task coupled with financial rewards awarded for correct performance at the end of each trial. While reward improved discrimination performance and concordantly enhanced activity in the ventral striatum, the effect of reward on somatosensory responses was only observed in a post-stimulus phase between stimulus offset and reward delivery. Interestingly, the increase in somatosensory cortex responses varied parametrically as a function of reward magnitude. In addition, the effect of reward on somatosensory responses was mediated by the dopaminergic system, as evidenced via pharmacological manipulations (Pleger et al., 2009). As observed in our own study, the contribution of motivational signals to sensory processing extends to other sensory systems, with modulatory signals detected at the level of the primary visual cortex (V1) in both rats (Shuler and Bear, 2006) and humans (Serences, 2008). Thus, it appears that motivation not only modulates sensory processing, but that such influences are present at the first stages of cortical processing. Naturally, such effects likely reflect “late” contributions from other processing stages (see next section).\nThus far, we have reviewed motivational effects that appear to be more transient in nature; however, although relatively little is known about sustained motivational signals, such modulations have also been observed. For instance, in our experiment discussed above, we employed an experimental design in which incentive was manipulated in a blocked fashion, allowing us to investigate sustained responses throughout the block of trials and how they were modulated by motivation. State-like effects were observed in several brain regions, including sites in the prefrontal cortex (PFC; e.g., FEF, middle frontal gyrus), parietal cortex (e.g., IPS), in addition to the PCC. Related findings were also reported by Locke and Braver (2008) who reported increased sustained fMRI activity during rewarded blocks of a cognitive control task in a network of regions including the right lateral PFC, right parietal cortex, and dorsal medial frontal cortex. Importantly, in a recent study, Jimura et al. (in press) showed that the effect of an individual's sensitivity to reward on working memory performance was mediated by sustained effects of reward observed in the right lateral PFC. These studies highlight the importance of studying sustained effects of motivation, which may be more closely related to arousal processes. Indeed, future investigations seeking to unravel the contributions of both transient and sustained responses to behavioral performance are greatly 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