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Retrospective and prospective coding for predicted reward in the sensory thalamus

Nature volume 412, pages 546–549 (2001)Cite this article

Abstract

Reward is important for shaping goal-directed behaviour1,2,3,4. After stimulus–reward associative learning, an organism can assess the motivational value of the incoming stimuli on the basis of past experience (retrospective processing), and predict forthcoming rewarding events (prospective processing)1,2,3,4,5. The traditional role of the sensory thalamus is to relay current sensory information to cortex. Here we find that non-primary thalamic neurons respond to reward-related events in two ways. The early, phasic responses occurred shortly after the onset of the stimuli and depended on the sensory modality. Their magnitudes resisted extinction and correlated with the learning experience. The late responses gradually increased during the cue and delay periods, and peaked just before delivery of the reward. These responses were independent of sensory modality and were modulated by the value and timing of the reward. These observations provide new evidence that single thalamic neurons can code for the acquired significance of sensory stimuli in the early responses (retrospective coding) and predict upcoming reward value in the late responses (prospective coding).

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Figure 1: Rastergrams and spike-density functions (SDFs) of the neuronal activity to each cue stimulus (top panels, auditory cues; bottom panels, visual cues).
Figure 2: Effects of reward value and timing on the activity of the neuron with two response components, shown in Fig. 1a.
Figure 3: The plasticity of responses to tone 1 of the neuron shown in Fig. 1a during extinction and relearning.
Figure 4: Functional topography.

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Acknowledgements

We thank R. Norgren (invited by Gofo Life Sciences International Fund) for helpful comments on this manuscript, and T. Kitamura for technical assistance. This work was partly supported by Grants-in-Aid for Scientific Research from the Japanese Ministry of Education, Science and Culture.

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Authors and Affiliations

  1. Department of Physiology, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Toyama, 930-0194, Japan

    Yutaka Komura, Ryoi Tamura, Teruko Uwano, Hisao Nishijo & Taketoshi Ono

  2. Department of Otorhinolaryngology, University of Tokyo School of Medicine, Tokyo, 113-0033, Japan

    Yutaka Komura & Kimitaka Kaga

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  1. Yutaka Komura
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  6. Taketoshi Ono
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Correspondence to Taketoshi Ono.

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Komura, Y., Tamura, R., Uwano, T. et al. Retrospective and prospective coding for predicted reward in the sensory thalamus. Nature 412, 546–549 (2001). https://doi.org/10.1038/35087595

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