A negative fMRI response to reward in human visual cortex

Purpose. A previous monkey fMRI study (Arsenault and Vanduffel, SfN abstract 2011) has discovered a novel response to juice rewards in monkey visual cortex (areas V1-V4, TEO) in a classical conditioning paradigm. Specifically, the reward elicited a negative fMRI response without the conditioned visual stimulus as well as a reduction of the stimulus response. Here, we test if monetary reward evokes an analogous fMRI response in the human brain. Methods. We used a 2 x 2 factorial design (factors: visual stimulus X reward). Visual stimuli were gratings presented around fixation (full contrast, vertical, randomly counterphasing at 10Hz, spatial frequency 1 cycle/degree, presentation 1s, size 8 degrees of visual angle), and reward (€ 0.20) was signaled by one of two sounds, the other indicating no reward. Sounds were 200 ms in duration and occurred 800 ms after stimulus onset. Trials were separated by a variable ITI (range 4.5 -9 s). Thus, half of the sounds indicated that reward occurred unexpectedly. These rewards were not preceded by a visual stimulus. Which sound indicated reward was counterbalanced between subjects. Event-related fMRI responses to sounds and visual stimulation were measured from several retinotopic visual cortical areas (V1-V4, V3A/B). Concurrently, eye movements and pupil diameter were recorded. Results. The stimulus-selective subregions (defined based on a separate localizer) of all visual cortical areas exhibited strong positive fMRI responses to visual stimulus presentation. In the absence of a visual stimulus, these same regions showed a transient negative fMRI response triggered by the reward. In the presence of a visual stimulus, these regions showed a reduced response to the visual stimulus. These response reductions for reward trials compared to no-reward trials were similar regardless of the presence or absence of visual stimulation, and did not reflect the sound indicating reward. Conclusion. In accordance with monkey results, we find a transient negative fMRI response in visual cortex to sounds that predict reward. Thus, this negative reward response seems to generalize across species and does not seem to depend on whether reward is primary or secondary. The negative sign of this response suggests that it is distinct from attention or working memory, as these factors predict an increase in fMRI signal in response to reward.status: publishe