Parametric increases in behavioral performance and activation strength in the fronto-parietal attentional network
Here, 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).
Our 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).
Figure 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.
In 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.
Figure 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.