Task preparation processes related to reward prediction precede those related to task-difficulty expectation

Abstract

Recently, attempts have been made to disentangle the neural underpinnings of preparatory processes related to reward and attention. Functional magnetic resonance imaging (fMRI) research showed that neural activity related to the anticipation of reward and to attentional demands invokes neural activity patterns featuring large-scale overlap, along with some differences and interactions. Due to the limited temporal resolution of fMRI, however, the temporal dynamics of these processes remain unclear. Here, we report an event-related potentials (ERP) study in which cued attentional demands and reward prospect were combined in a factorial design. Results showed that reward prediction dominated early cue processing, as well as the early and later parts of the contingent negative variation (CNV) slow-wave ERP component that has been associated with task-preparation processes. Moreover these reward-related electrophysiological effects correlated across participants with response time speeding on reward-prospect trials. In contrast, cued attentional demands affected only the later part of the CNV, with the highest amplitudes following cues predicting high-difficulty potential-reward targets, thus suggesting maximal task preparation when the task requires it and entails reward prospect. Consequently, we suggest that task-preparation processes triggered by reward can arise earlier, and potentially more directly, than strategic top-down aspects of preparation based on attentional demands.

Keywords: Attention; CNV; Contingent negative variation; EEG; ERP; Event-related potentials; ICA; ISI; ROI; RT; Reward; SPN; Visual attention; contingent negative variation; electroencephalography; event-related potential; fMRI; functional magnetic resonance imaging; independent component analysis; inter-stimulus interval; rANOVA; region of interest; repeated-measure analysis of variance; response time; stimulus-preceding negativity.

Figure 1

Paradigm. In active-attention trials cues indicated the target location (direction of arrow), availability of reward (color of arrow) and task difficulty (color of fixation square). After a variable ISI a target was presented and participants had to indicate whether the top or bottom gap was larger. Subsequent feedback indicated the amount of money won or lost (4 eurocents for reward trials or 0 eurocents for no-reward trials).

Figure 2

Mid-range cue-related potentials. (A) Grand average ERPs elicited by cues in all four conditions at electrode sites C1, C2, Cz and CPz between 200 and 250 ms, and a topographic map reflecting the difference in P2 amplitude between reward-predicting cues and trials without reward prediction (electrodes of interest are indicated by white markers). (B) Grand average ERPs locked to the onset of the cue at electrode sites P1, P2, PO3, PO4, Pz and POz between 300 and 500 ms, reflecting P3 amplitudes in all conditions, and a topographic plot for reward condition versus no-reward condition.

Figure 3

Contingent negative variation. (A) Electrophysiological waveform indicating the CNV, with an early (700–1100 ms) and late (1100–1500 ms) phase at electrode sites C1, C2 and Cz. (B) Topographic maps resulting from condition-wise contrasts in the early and late time window of the CNV (ME = main effect). (C) Correlation between difficulty effect in the reward condition on the late CNV amplitude and target RTs (high minus low task difficulty, respectively).

Figure 4

Target- and feedback-related potentials. (A) Grand average ERPs indicating target P3 amplitudes at parietal electrode sites P1, P2, Pz and POz between 300 and 600 ms and a topographic map reflecting the average of all four main conditions, with the ROI being indicated by white electrode markers. (B) Electrophysiological waveforms time-locked to the onset of the feedback electrodes CP1, CP2 and CPz (from 200 to 400 ms) and a topographic map averaging the four main conditions.