Dissociable neural responses in human reward systems

Abstract

Reward is one of the most important influences shaping behavior. Single-unit recording and lesion studies in experimental animals have implicated a number of regions in response to reinforcing stimuli, in particular regions of the extended limbic system and the ventral striatum. In this experiment, functional neuroimaging was used to assess neural response within human reward systems under different psychological contexts. Nine healthy volunteers were scanned using functional magnetic resonance imaging during the performance of a gambling task with financial rewards and penalties. We demonstrated neural sensitivity of midbrain and ventral striatal regions to financial rewards and hippocampal sensitivity to financial penalties. Furthermore, we show that neural responses in globus pallidus, thalamus, and subgenual cingulate were specific to high reward levels occurring in the context of increasing reward. Responses to both reward level in the context of increasing reward and penalty level in the context of increasing penalty were seen in caudate, insula, and ventral prefrontal cortex. These results demonstrate dissociable neural responses to rewards and penalties that are dependent on the psychological context in which they are experienced.

Fig. 1.

Cognitive activation paradigm.a shows the task that was used; the pairs of black and red cards to one side of the screen and the cumulative reward bar to the other. b shows the sequence of outcomes, corresponding to the actual rewards and penalties experienced, derived from the constrained binomial random walk function. This same function determined outcomes in all subjects, who consequently experienced the same sequence of rewards and penalties. The red asterisks mark the point at which blocks of rest were intersposed. These rest blocks were used to model low frequency drift in signal and were not involved in the subsequent regression analysis.

Fig. 2.

Responses to reward level. The figure shows SPMs of the t statistic (after transformation to a SPM{Z}) rendered onto a standard MRI template.a shows the activation in right midbrain positively associated with reward level (x = 9;y = −12; z = −3), above the substantia nigra and below the thalamus. b shows activation in right ventral striatum (x = 18;y = 9 or 12; z = −6) lateral to the nucleus accumbens. Both activations were significant atp < 0.001. c shows activation of left hippocampus (x = −24; y = −18; z = −18; *p < 0.05) and right hippocampus (x = 33; y = −12; z = −21; p < 0.001) negatively associated with reward level.

Fig. 3.

Responses to reward in the context of a winning streak. The transverse slice in a displays activations of right anteroventral thalamus (area VA; x = 6;y = −12; z = 0; *p < 0.05), bilateral globus pallidus (x = +15; y = −3;z = 6; p < 0.001), and subgenual cingulate (x = +9; y= −36; z = 3; p < 0.001) associated with reward occurring during a winning streak. These group activations appear somewhat spread because of the spatial smoothing necessary for intersubject averaging. Therefore it should be noted that we cannot be certain that the putative thalamus and global pallidus activations indeed represent regionally distinct neural responses, although this is how we have chosen to interpret them. bshows enhanced neural response in the bilateral hippocampus associated with the experience of high levels of penalty during a losing streak. It should be noted that the activation in the right hippocampal region is contaminated by the large blood vessel.

Fig. 4.

Responses to generic risk-taking processes. Activations of right (x = 51;y = 15; z = −12;p < 0.001) and left (x = −33;y = 15; z = −15; *p < 0.05) orbitofrontal cortex, right (x = 42; y = 9;z = −6; *p < 0.05) and left (x = −36; y = −6;z = 6; *p < 0.05) insula, and right (x = 21; y = 24;z = 0; *p < 0.05) and left (x = −9; y = 12;z = 12; p < 0.001) caudate associated with both reward during a winning streak and penalties during a losing streak. These activations may represent responses to risk-taking, independent of outcome.