Converging evidence: motivational effects on cognitive and sensory processing
Our 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.
A 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.
Given 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.
The 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).
Thus 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 needed.