Contextual novelty modulates the neural dynamics of reward anticipation

Abstract

We investigated how rapidly the reward-predicting properties of visual cues are signaled in the human brain and the extent these reward prediction signals are contextually modifiable. In a magnetoencephalography study, we presented participants with fractal visual cues that predicted monetary rewards with different probabilities. These cues were presented in the temporal context of a preceding novel or familiar image of a natural scene. Starting at ∼100 ms after cue onset, reward probability was signaled in the event-related fields (ERFs) over temporo-occipital sensors and in the power of theta (5-8 Hz) and beta (20-30 Hz) band oscillations over frontal sensors. While theta decreased with reward probability beta power showed the opposite effect. Thus, in humans anticipatory reward responses are generated rapidly, within 100 ms after the onset of reward-predicting cues, which is similar to the timing established in non-human primates. Contextual novelty enhanced the reward anticipation responses in both ERFs and in beta oscillations starting at ∼100 ms after cue onset. This very early context effect is compatible with a physiological model that invokes the mediation of a hippocampal-VTA loop according to which novelty modulates neural response properties within the reward circuitry. We conclude that the neural processing of cues that predict future rewards is temporally highly efficient and contextually modifiable.

Figure 1.

Experimental design (phase 3). Note that subjects underwent a familiarization and a conditioning phase inside the MEG during which no data were acquired.

Figure 2.

Event-related magnetic fields. A, Novelty effects emerged at ∼200 ms after stimulus onset over bilateral temporal sensors and peaked at ∼400 ms (x = 47, y = −68; nearest channel: MRT57). B, Reward probability was represented over right occipitotemporal sensors between 100 and 150 ms and peaked at 133 ms (x = 17, y = −95; nearest channel: MRO51). C, A novelty bonus effect was observed for the low reward probability condition peaking at 127 ms over occipitotemporal sensors (x = 42, y = −76; nearest channel: MRO53). Left columns show statistical parametric maps of the F-statistic. Middle columns show the time course of the effects as extracted from voxel space (on which the statistical analyses are based) (statistically significant differences, *p < 0.05), and right columns show the topographical maps of the MEG data before 3D conversion (see Materials and Methods).

Figure 3.

Results of the time-frequency analyses. A, Theta power increased over right frontal and left temporal sensors (x = −40, y = −14; nearest channel: MLT24) for familiar stimuli with a peak at 522 ms. B, Theta power over right temporal and centroparietal sensors (x = 17, y = −25; nearest channel: MRT41) decreased as a function of reward probability. C, Beta power increased with reward probability over frontocentral sensors (x = 0, y = 8; nearest channel: MZC02). Left columns show statistical parametric maps of the F-statistics, middle columns show the effects for each condition at the peak time point as extracted from voxel space, and right columns show the time-frequency plots as extracted from the nearest channel (before conversion to voxel space; see Materials and Methods). Error bars denote 1 SEM (statistically significant differences, *p < 0.05).

Figure 4.

Novelty bonus effects in the beta power. A, B, Over central sensors (A: x = 8, y = 5; nearest channel: MRC52; B: x = 4, y = 5; nearest channel: MZC02), beta power increased as a function of reward probability, and this effect was enhanced in the context of novelty for all reward probabilities (low, A; medium and high, B). Left columns show statistical parametric maps of the F-statistics, middle columns show the effects for each condition at the peak time point as extracted from voxel space, and right columns show the time-frequency plots as extracted from the nearest channel (before conversion to voxel space; see Materials and Methods). For A, right: p0 novel vs p0 familiar; for B, right: (p4 and p8) novel vs (p4 and p8) familiar. The dashed box indicates the beta frequency range (20–30 Hz) from 0 to 800 ms. It should be noted that the time-frequency data (right columns) were not rescaled by any logarithmic function (see Materials and Methods).