Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 50 (2), 657-64

Adaptive and Aberrant Reward Prediction Signals in the Human Brain

Affiliations

Adaptive and Aberrant Reward Prediction Signals in the Human Brain

Jonathan P Roiser et al. Neuroimage.

Abstract

Theories of the positive symptoms of schizophrenia hypothesize a role for aberrant reinforcement signaling driven by dysregulated dopamine transmission. Recently, we provided evidence of aberrant reward learning in symptomatic, but not asymptomatic patients with schizophrenia, using a novel paradigm, the Salience Attribution Test (SAT). The SAT is a probabilistic reward learning game that employs cues that vary across task-relevant and task-irrelevant dimensions; it provides behavioral indices of adaptive and aberrant reward learning. As an initial step prior to future clinical studies, here we used functional magnetic resonance imaging to examine the neural basis of adaptive and aberrant reward learning during the SAT in healthy volunteers. As expected, cues associated with high relative to low reward probabilities elicited robust hemodynamic responses in a network of structures previously implicated in motivational salience; the midbrain, in the vicinity of the ventral tegmental area, and regions targeted by its dopaminergic projections, i.e. medial dorsal thalamus, ventral striatum and prefrontal cortex (PFC). Responses in the medial dorsal thalamus and polar PFC were strongly correlated with the degree of adaptive reward learning across participants. Finally, and most importantly, differential dorsolateral PFC and middle temporal gyrus (MTG) responses to cues with identical reward probabilities were very strongly correlated with the degree of aberrant reward learning. Participants who showed greater aberrant learning exhibited greater dorsolateral PFC responses, and reduced MTG responses, to cues erroneously inferred to be less strongly associated with reward. The results are discussed in terms of their implications for different theories of associative learning.

Figures

Fig. 1
Fig. 1
Salience Attribution Test. Participants were required to respond to the square as quickly as possible. On 50% of trials, participants won more money for quicker responses, with the probability of reward signaled by the cue appearing immediately prior to the probe.
Fig. 2
Fig. 2
Hemodynamic responses associated with high- relative to low-probability reward cues. Presenting cues associated with a high relative to low probability of reinforcement elicited responses bilaterally in the ventral striatum (peak coordinates: right [x = 12, y = 12, z = − 3]; left [x = − 12, y = 9, z = − 3]) (A) and medial dorsal thalamus (peak coordinates: right [x = 3, y = − 9, z = 9]; left [x = − 3, y = − 9, z = 9]) (B). Responses in the thalamus were strongly correlated with the degree of explicit adaptive reward learning across participants (peak coordinates: right [x = 6, y = − 12, z = 15]; left [x = − 3, y = − 12, z = 15], r = 0.71 (plotted in scatterplot)) (C).
Fig. 3
Fig. 3
Hemodynamic responses associated with low- relative to high-probability reward cues. (A) Presenting cues associated with a low relative to high probability of reinforcement elicited responses in the lateral frontal pole bilaterally (peak coordinates: right [x = 24, y = 54, z = 6]; left [x = − 21, y = 63, z = 12])), which were strongly correlated with the degree of explicit adaptive reward learning across participants (peak coordinates: right [x = 9, y = 69, z = 6]; left [x = − 27, y = 48, z = 18], r = − 0.80 (plotted in scatterplot)) (B).
Fig. 4
Fig. 4
Hemodynamic responses associated with explicit aberrant reward learning. Differential response to two cues associated with equal (50%) probability of reward in the dorsolateral prefrontal cortex (peak coordinates: [x = − 18, y = 45, z = 36]) (A) was strongly correlated with the degree of explicit aberrant reward learning pertaining to those stimuli across participants (r = − 0.82) (B).

Similar articles

See all similar articles

Cited by 17 articles

See all "Cited by" articles

References

    1. Abi-Dargham A. Do we still believe in the dopamine hypothesis? New data bring new evidence. Int. J. Neuropsychopharmacol. 2004;7(Suppl 1):S1–S5. - PubMed
    1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986;9:357–381. - PubMed
    1. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Rev. 1998;28:309–369. - PubMed
    1. Bischoff-Grethe A., Proper S.M., Mao H., Daniels K.A., Berns G.S. Conscious and unconscious processing of nonverbal predictability in Wernicke's area. J. Neurosci. 2000;20:1975–1981. - PMC - PubMed
    1. Blyler C.R., Gold J.M., Iannone V.N., Buchanan R.W. Short form of the WAIS-III for use with patients with schizophrenia. Schizophr. Res. 2000;46:209–215. - PubMed

Publication types

Feedback