Temporally Extended Dopamine Responses to Perceptually Demanding Reward-Predictive Stimuli
Open accessAbstract
Midbrain dopamine neurons respond to reward-predictive stimuli. In the natural environment reward-predictive stimuli are often perceptually complicated. Thus, to discriminate one stimulus from another, elaborate sensory processing is necessary. Given that previous studies have used simpler types of reward-predictive stimuli, it has yet to be clear whether and, if so, how dopamine neurons obtain reward information from perceptually complicated stimuli. To investigate this, we recorded the activities of monkey dopamine neurons while they were performing discrimination between two coherent motion directions in random-dot motion stimuli. These coherent directions were paired with different magnitudes of reward. We found that dopamine neurons showed reward-predictive responses to random-dot motion stimuli. Moreover, dopamine neurons showed temporally extended activity correlated with changes in reward prediction (i.e., reward prediction error) from coarse to fine scales between initial motion detection and subsequent motion discrimination phases. Noticeably, dopamine reward-predictive responses became differential in a later phase than previously reported. This response pattern was consistent with the time course of processing required for the estimation of expected reward value that parallels the motion direction discrimination processing. The results demonstrate that dopamine neurons are able to reflect the reward value of perceptually complicated stimuli, and suggest that dopamine neurons use the moment-to-moment reward prediction associated with environmental stimuli to compute a reward prediction error.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The initial activation is sensitive to the time of stimulus occurrence and thus codes a temporal-event prediction error.
“True to the notion that dopamine neurons are involved in temporal prediction-error coding, the initial activation is sensitive to the time of stimulus occurrence and thus codes a temporal-event prediction error33.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [33]
Dopamine responses in elaborate tasks constitute standard reward prediction-error signals.
“However, on closer inspection, dopamine responses in such elaborate tasks constitute standard reward prediction-error signals2,33,59,66,69,75,151–153.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [33]
Dopamine neurons in medial and lateral, or dorsal and ventral, midbrain positions show graded differences in responses to rewarding and aversive stimuli.
“Dopamine neurons in medial and lateral, or dorsal and ventral, midbrain positions do show graded differences in responses to rewarding and aversive stimuli2,23,24,26,33.”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [33]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Press, W. H., Teukolsky, S. A., Vetterling, W. T., & Flannery, B. P. (1994) · Cited by 15,411 · see citing works
Predictive reward signal of dopamine neurons
Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.1 · Cited by 4,564 · see citing works
Self-citationDopamine, learning and motivation.
Wise, R. A. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1406 · Cited by 3,379 · cited 1× · see citing works
“Dopamine plays a central role in reward information processing (Schultz, 1998; Wise, 2004).”
BackgroundThe psychometric function: I. Fitting, sampling, and goodness of fit
Wichmann, F. A., & Hill, N. J. (2001) · Perception & Psychophysics · doi:10.3758/bf03194544 · Cited by 2,359 · see citing works
Discrete coding of reward probability and uncertainty by dopamine neurons
Fiorillo, C. D., Tobler, P. N., & Schultz, W. (2003) · Science · doi:10.1126/science.1077349 · Cited by 2,085 · see citing works
Self-citationThe analysis of visual motion: a comparison of neuronal and psychophysical performance
Britten, K., Shadlen, M., Newsome, W., & Movshon, J. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04745.1992 · Cited by 1,958 · see citing works
Neural Basis of a Perceptual Decision in the Parietal Cortex (Area LIP) of the Rhesus Monkey
Shadlen, M. N., & Newsome, W. T. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.4.1916 · Cited by 1,755 · see citing works
Newsome, W., & Pare, E. (1988) · The Journal of Neuroscience · doi:10.1523/jneurosci.08-06-02201.1988 · Cited by 1,615 · see citing works
Haber, S. N., Fudge, J. L., & McFarland, N. R. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-06-02369.2000 · Cited by 1,610 · see citing works
Roitman, J. D., & Shadlen, M. N. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-21-09475.2002 · Cited by 1,589 · cited 5× · see citing works
“This is consistent with a time course in which neural discrimination begins at 200 ms after RDM onset in the LIP area (Roitman and Shadlen, 2002).”
BackgroundMethodResultInfluentialMidbrain dopamine neurons encode a quantitative reward prediction error signal
Bayer, H. M., & Glimcher, P. W. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.020 · Cited by 1,304 · see citing works
Lateral habenula as a source of negative reward signals in dopamine neurons
Matsumoto, M., & Hikosaka, O. (2007) · Nature · doi:10.1038/nature05860 · Cited by 1,292 · see citing works
Adaptive Coding of Reward Value by Dopamine Neurons
Tobler, P. N., Fiorillo, C. D., & Schultz, W. (2005) · Science · doi:10.1126/science.1105370 · Cited by 1,276 · see citing works
Self-citationNeuronal correlates of a perceptual decision
Newsome, W. T., Britten, K. H., & Movshon, J. A. (1989) · Nature · doi:10.1038/341052a0 · Cited by 1,177 · see citing works
Dopamine neurons report an error in the temporal prediction of reward during learning
Hollerman, J. R., & Schultz, W. (1998) · Nature Neuroscience · doi:10.1038/1124 · Cited by 1,103 · see citing works
Self-citationDopamine responses comply with basic assumptions of formal learning theory
Waelti, P., Dickinson, A., & Schultz, W. (2001) · Nature · doi:10.1038/35083500 · Cited by 1,018 · see citing works
Self-citationCortical microstimulation influences perceptual judgements of motion direction
Salzman, C. D., Britten, K. H., & Newsome, W. T. (1990) · Nature · doi:10.1038/346174a0 · Cited by 881 · cited 2× · see citing works
“For example, global motion signals such as found in random-dot motion (RDM) stimuli are processed in higherorder visual cortices such as the middle temporal (MT) and the medial superior temporal (MST) areas (Newsome et al., 1989; Salzman et al., 1990; Britten et al., 1992; Celebrini and Newsome, 1994), and a lesion of…”
BackgroundThe psychometric function: II. Bootstrap-based confidence intervals and sampling
Wichmann, F. A., & Hill, N. J. (2001) · Perception & Psychophysics · doi:10.3758/bf03194545 · Cited by 809 · see citing works
Expectation of reward modulates cognitive signals in the basal ganglia
Kawagoe, R., Takikawa, Y., & Hikosaka, O. (1998) · Nature Neuroscience · doi:10.1038/1625 · Cited by 632 · see citing works
A representation of the hazard rate of elapsed time in macaque area LIP
Janssen, P., & Shadlen, M. N. (2005) · Nature Neuroscience · doi:10.1038/nn1386 · Cited by 601 · see citing works
Roesch, M. R., Calu, D. J., & Schoenbaum, G. (2007) · Nature Neuroscience · doi:10.1038/nn2013 · Cited by 597 · see citing works
Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons
Morris, G., Arkadir, D., Nevet, A., Vaadia, E., & Bergman, H. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.012 · Cited by 574 · see citing works
Midbrain dopamine neurons encode decisions for future action
Morris, G., Nevet, A., Arkadir, D., Vaadia, E., & Bergman, H. (2006) · Nature Neuroscience · doi:10.1038/nn1743 · Cited by 503 · see citing works
Dopamine: generalization and bonuses
Kakade, S. M., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00048-5 · Cited by 477 · see citing works
Influence of Reward Delays on Responses of Dopamine Neurons
Kobayashi, S., & Schultz, W. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1600-08.2008 · Cited by 431 · see citing works
Self-citationPan, W.-X., Schmidt, R., Wickens, J. R., & Hyland, B. I. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1478-05.2005 · Cited by 429 · see citing works
Microstimulation of macaque area LIP affects decision-making in a motion discrimination task
Hanks, T. D., Ditterich, J., & Shadlen, M. N. (2006) · Nature Neuroscience · doi:10.1038/nn1683 · Cited by 360 · see citing works
Schultz, W., & Romo, R. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.3.607 · Cited by 334 · cited 1× · see citing works
“The stimulus generalization responses are the composite response pattern of brief activation and subsequent suppression to sensory stimuli that are not associated with reward (Schultz and Romo, 1990; Horvitz et al., 1997; Waelti et al., 2001; Tobler et al., 2003).”
BackgroundSelf-citationCelebrini, S., & Newsome, W. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-07-04109.1994 · Cited by 323 · see citing works
The temporal precision of reward prediction in dopamine neurons
Fiorillo, C. D., Newsome, W. T., & Schultz, W. (2008) · Nature Neuroscience · doi:10.1038/nn.2159 · Cited by 310 · see citing works
Self-citationCoding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm
Tobler, P. N., Dickinson, A., & Schultz, W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10402.2003 · Cited by 300 · see citing works
Self-citationCorrelated Coding of Motivation and Outcome of Decision by Dopamine Neurons
Satoh, T., Nakai, S., Sato, T., & Kimura, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09913.2003 · Cited by 298 · see citing works
Attentional modulation in visual cortex depends on task timing
Ghose, G. M., & Maunsell, J. H. R. (2002) · Nature · doi:10.1038/nature01057 · Cited by 297 · see citing works
Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat
Horvitz, J. C., Stewart, T., & Jacobs, B. L. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00265-5 · Cited by 283 · see citing works
Dopamine Neurons Can Represent Context-Dependent Prediction Error
Nakahara, H., Itoh, H., Kawagoe, R., Takikawa, Y., & Hikosaka, O. (2004) · Neuron · doi:10.1016/s0896-6273(03)00869-9 · Cited by 276 · see citing works
Microstimulation of visual cortex affects the speed of perceptual decisions
Ditterich, J., Mazurek, M. E., & Shadlen, M. N. (2003) · Nature Neuroscience · doi:10.1038/nn1094 · Cited by 234 · see citing works
Moment-to-moment tracking of state value in the amygdala
Belova, M. A., Paton, J. J., & Salzman, C. D. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1400-08.2008 · Cited by 221 · see citing works
Kawagoe, R., Takikawa, Y., & Hikosaka, O. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00721.2003 · Cited by 158 · see citing works
Oikawa, H., Sasaki, M., Tamakawa, Y., Ehara, S., & Tohyama, K. (2002) · PubMed Central · Cited by 149 · see citing works
Stereotaxic atlas of the brain of Macaca fuscata
Kusama, T., & Mabuchi, M. (1970) · Cited by 145 · see citing works
Dopamine neuronal responses in monkeys performing visually cued reward schedules
Ravel, S., & Richmond, B. J. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.04905.x · Cited by 41 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · see citing works
Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126 · see citing works
Self-citationDopamine reward prediction-error signalling: A two-component response
Schultz, W. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2015.26 · Cited by 1,036 · see citing works
Self-citationUpdating dopamine reward signals
Schultz, W. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.012 · Cited by 651 · see citing works
Self-citationDopamine reward prediction error coding
Schultz, W. (2016) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2016.18.1/wschultz · Cited by 597 · see citing works
Self-citationCollins, A. G. E., & Frank, M. J. (2014) · Psychological Review · doi:10.1037/a0037015 · Cited by 395 · see citing works
Predictive representations can link model-based reinforcement learning to model-free mechanisms
Russek, E. M., Momennejad, I., Botvinick, M., Gershman, S. J., & Daw, N. D. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005768 · Cited by 321 · see citing works
Cognitive Training for Impaired Neural Systems in Neuropsychiatric Illness
Vinogradov, S., Fisher, M., & de Villers‐Sidani, E. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.251 · Cited by 324 · see citing works
Dynamic modulation of decision biases by brainstem arousal systems
de Gee, J. W., Colizoli, O., Kloosterman, N. A., Knapen, T. H. J., Nieuwenhuis, S., & Donner, T. H. (2017) · eLife · doi:10.7554/elife.23232 · Cited by 312 · see citing works
What, If, and When to Move: Basal Ganglia Circuits and Self-Paced Action Initiation
Klaus, A., Alves da Silva, J., & Costa, R. M. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031033 · Cited by 284 · see citing works
Reward functions of the basal ganglia
Schultz, W. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1510-0 · Cited by 248 · see citing works
Self-citationDopamine reward prediction errors reflect hidden-state inference across time
Starkweather, C. K., Babayan, B. M., Uchida, N., & Gershman, S. J. (2017) · Nature Neuroscience · doi:10.1038/nn.4520 · Cited by 206 · see citing works
Gershman, S. J., & Uchida, N. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0220-7 · Cited by 236 · see citing works
Mesolimbic dopamine signaling in acute and chronic pain
Taylor, A. M. W., Becker, S., Schweinhardt, P., & Cahill, C. M. (2016) · Pain · doi:10.1097/j.pain.0000000000000494 · Cited by 229 · see citing works
Midbrain dopamine neurons signal belief in choice accuracy during a perceptual decision
Lak, A., Nomoto, K., Keramati, M., Sakagami, M., & Kepecs, A. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.026 · Cited by 170 · see citing works
Self-citationThe Basal Ganglia’s Contributions to Perceptual Decision Making
Ding, L., & Gold, J. I. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.042 · Cited by 201 · see citing works
Rao, R. P. N. (2010) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2010.00146 · Cited by 190 · see citing works
Redgrave, P., Vautrelle, N., & Reynolds, J. N. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.07.060 · Cited by 183 · see citing works
Model-based predictions for dopamine
Langdon, A. J., Sharpe, M. J., Schoenbaum, G., & Niv, Y. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.006 · Cited by 161 · see citing works
Schultz, W., Stauffer, W. R., & Lak, A. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.03.013 · Cited by 164 · see citing works
Self-citationLearning from Action: Reconsidering Movement Signaling in Midbrain Dopamine Neuron Activity
Coddington, L. T., & Dudman, J. T. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.036 · Cited by 150 · see citing works
Anatomical and functional organization of the human substantia nigra and its connections
Zhang, Y., Larcher, K. M.-H., Mišić, B., & Dagher, A. (2017) · eLife · doi:10.7554/elife.26653 · Cited by 148 · see citing works
Kim, K. M., Baratta, M. V., Yang, A., Lee, D., Boyden, E. S., & Fiorillo, C. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033612 · Cited by 144 · see citing works
The medial prefrontal cortex shapes dopamine reward prediction errors under state uncertainty
Starkweather, C. K., Gershman, S. J., & Uchida, N. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.036 · Cited by 136 · see citing works
Development and function of the midbrain dopamine system: what we know and what we need to
Bissonette, G. B., & Roesch, M. R. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12257 · Cited by 133 · see citing works
Ito, M., & Doya, K. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.04.001 · Cited by 131 · see citing works
Sub-second Dopamine and Serotonin Signaling in Human Striatum during Perceptual Decision-Making
Bang, D., Kishida, K. T., Lohrenz, T. M., White, J. P., Laxton, A. W., Tatter, S. B., Fleming, S. M., & Montague, P. R. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.015 · Cited by 123 · see citing works
Distinct Representations of Cognitive and Motivational Signals in Midbrain Dopamine Neurons
Matsumoto, M., & Takada, M. (2013) · Neuron · doi:10.1016/j.neuron.2013.07.002 · Cited by 117 · see citing works
Dopaminergic Reward Signals Selectively Decrease fMRI Activity in Primate Visual Cortex
Arsenault, J. T., Nelissen, K., Jarraya, B., & Vanduffel, W. (2013) · Neuron · doi:10.1016/j.neuron.2013.01.008 · Cited by 117 · see citing works
Dopamine neurons code subjective sensory experience and uncertainty of perceptual decisions
de Lafuente, V., & Romo, R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1117636108 · Cited by 117 · see citing works
How mechanisms of perceptual decision-making affect the psychometric function
Gold, J. I., & Ding, L. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.05.008 · Cited by 112 · see citing works
Human Scalp Potentials Reflect a Mixture of Decision-Related Signals during Perceptual Choices
Philiastides, M. G., Heekeren, H. R., & Sajda, P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3012-14.2014 · Cited by 110 · see citing works
Midbrain dopamine neurons signal aversion in a reward-context-dependent manner
Matsumoto, H., Tian, J., Uchida, N., & Watabe‐Uchida, M. (2016) · eLife · doi:10.7554/elife.17328 · Cited by 109 · see citing works
Fiorillo, C. D., Song, M. R., & Yun, S. R. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.3883-12.2013 · Cited by 98 · see citing works
Multiplicity of control in the basal ganglia: computational roles of striatal subregions
Bornstein, A. M., & Daw, N. D. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.009 · Cited by 97 · see citing works
Tsutsui‐Kimura, I., Matsumoto, H., Akiti, K., Yamada, M. M., Uchida, N., & Watabe‐Uchida, M. (2020) · eLife · doi:10.7554/elife.62390 · Cited by 91 · see citing works
Winstanley, C. A., Cocker, P. J., & Rogers, R. D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.230 · Cited by 98 · see citing works
van Kempen, J., Loughnane, G. M., Newman, D. P., Kelly, S. P., Thiele, A., O’Connell, R. G., & Bellgrove, M. A. (2019) · eLife · doi:10.7554/elife.42541 · Cited by 88 · see citing works
Dopamine neurons learn relative chosen value from probabilistic rewards
Lak, A., Stauffer, W. R., & Schultz, W. (2016) · eLife · doi:10.7554/elife.18044 · Cited by 87 · see citing works
Self-citationThe role of learning-related dopamine signals in addiction vulnerability
Huys, Q. J. M., Tobler, P. N., Hasler, G., & Flagel, S. B. (2014) · Progress in brain research · doi:10.1016/b978-0-444-63425-2.00003-9 · Cited by 87 · see citing works
Recent advances in understanding the role of phasic dopamine activity
Schultz, W. (2019) · F1000Research · doi:10.12688/f1000research.19793.1 · Cited by 89 · see citing works
Self-citationIn Pursuit of Healthy Aging: Effects of Nutrition on Brain Function
Melzer, T. M., Manosso, L. M., Yau, S., Gil‐Mohapel, J., & Brocardo, P. S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22095026 · Cited by 90 · see citing works
Hill-Bowen, L. D., Riedel, M. C., Poudel, R., Salo, T., Flannery, J. S., Camilleri, J. A., Eickhoff, S. B., Laird, A. R., & Sutherland, M. T. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.08.010 · Cited by 70 · see citing works
Complementary neural correlates of motivation in dopaminergic and noradrenergic neurons of monkeys
Bouret, S., Ravel, S., & Richmond, B. J. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00040 · Cited by 64 · see citing works
Components and characteristics of the dopamine reward utility signal
Stauffer, W. R., Lak, A., Kobayashi, S., & Schultz, W. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23880 · Cited by 62 · see citing works
Self-citationReward Contexts Extend Dopamine Signals to Unrewarded Stimuli
Kobayashi, S., & Schultz, W. (2014) · Current Biology · doi:10.1016/j.cub.2013.10.061 · Cited by 63 · see citing works
Self-citationSense, memory, and decision-making in the somatosensory cortical network
Romo, R., Lemus, L., & de Lafuente, V. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.08.002 · Cited by 60 · see citing works
Ongoing, rational calibration of reward-driven perceptual biases
Fan, Y., Gold, J. I., & Ding, L. (2018) · eLife · doi:10.7554/elife.36018 · Cited by 62 · see citing works
Context-Dependent Multiplexing by Individual VTA Dopamine Neurons
Kremer, Y., Flakowski, J., Rohner, C., & Lüscher, C. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.0502-20.2020 · Cited by 57 · see citing works
Wang, Y., Toyoshima, O., Kunimatsu, J., Yamada, H., & Matsumoto, M. (2021) · eLife · doi:10.7554/elife.63166 · Cited by 56 · see citing works
Dopamine neurons encode errors in predicting movement trigger occurrence
Pasquereau, B., & Turner, R. S. (2014) · Journal of Neurophysiology · doi:10.1152/jn.00401.2014 · Cited by 53 · see citing works
Park, J., & Moghaddam, B. (2017) · eLife · doi:10.7554/elife.30056 · Cited by 55 · see citing works
Dopamine-associated cached values are not sufficient as the basis for action selection
Hollon, N. G., Arnold, M. M., Gan, J. O., Walton, M. E., & Phillips, P. E. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419770111 · Cited by 52 · see citing works
Reinforcement Learning and Causal Models
Gershman, S. (2017) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780199399550.013.20 · Cited by 63 · see citing works
Evidence accumulation for value computation in the prefrontal cortex during decision making
Lin, Z., Nie, C., Zhang, Y., Yang, C., & Yang, T. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019077117 · Cited by 50 · see citing works
Stark, E. A., Vuust, P., & Kringelbach, M. L. (2018) · Progress in brain research · doi:10.1016/bs.pbr.2018.03.019 · Cited by 50 · see citing works
Takakuwa, N., Kato, R., Redgrave, P., & Isa, T. (2017) · eLife · doi:10.7554/elife.24459 · Cited by 47 · see citing works
Baudonnat, M., Huber, A., David, V., & Walton, M. E. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00175 · Cited by 42 · see citing works
Advanced Reinforcement Learning
Daw, N. D. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-416008-8.00016-4 · Cited by 44 · see citing works
A dopamine mechanism for reward maximization
Schultz, W. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2316658121 · Cited by 44 · see citing works
Self-citationA neural mechanism for conserved value computations integrating information and rewards
Bromberg-Martin, E. S., Feng, Y.-Y., Ogasawara, T., White, J. K., Zhang, K., & Monosov, I. E. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01511-4 · Cited by 43 · see citing works
High reward enhances perceptual learning
Zhang, P., Hou, F., Yan, F.-F., Xi, J., Lin, B.-R., Zhao, J., Yang, J., Ge, C., Zhang, M.-Y., He, Q., et al. (2018) · Journal of Vision · doi:10.1167/18.8.11 · Cited by 39 · see citing works
Carmichael, K., Sullivan, B. T., Lopez, E., Sun, L., & Cai, H. (2021) · Ageing and Neurodegenerative Diseases · doi:10.20517/and.2021.07 · Cited by 46 · see citing works
Persichetti, A. S., Aguirre, G. K., & Thompson‐Schill, S. L. (2014) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00760 · Cited by 35 · see citing works
Dopamine Modulation of Motor and Sensory Cortical Plasticity among Vertebrates
Macêdo-Lima, M., & Remage‐Healey, L. (2021) · Integrative and Comparative Biology · doi:10.1093/icb/icab019 · Cited by 35 · see citing works
Multiplexing signals in reinforcement learning with internal models and dopamine
Nakahara, H. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.001 · Cited by 31 · see citing works
Tanaka, S., O’Doherty, J. P., & Sakagami, M. (2019) · Nature Communications · doi:10.1038/s41467-019-11334-2 · Cited by 28 · see citing works
Self-citationSarno, S., de Lafuente, V., Romo, R., & Parga, N. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1712479114 · Cited by 30 · see citing works
The neuroscience of perceptual categorization in pigeons: A mechanistic hypothesis
Güntürkün, O., Koenen, C., Iovine, F., Garland, A., & Pusch, R. (2018) · Learning & Behavior · doi:10.3758/s13420-018-0321-6 · Cited by 30 · see citing works
Pando‐Naude, V., Matthews, T. E., Højlund, A., Jakobsen, S., Østergaard, K., Johnsen, E., Garza‐Villarreal, E. A., Witek, M. A. G., Penhune, V., & Vuust, P. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16128 · Cited by 29 · see citing works
Sensory regulation of dopaminergic cell activity: Phenomenology, circuitry and function
Overton, P. G., Vautrelle, N., & Redgrave, P. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.01.023 · Cited by 29 · see citing works
Multiple brain networks contribute to the acquisition of bias in perceptual decision-making
Chen, M.-Y., Jimura, K., White, C. N., Maddox, W. T., & Poldrack, R. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00063 · Cited by 28 · see citing works
Herold, C., Joshi, I., Chehadi, O., Hollmann, M., & Güntürkün, O. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036484 · Cited by 27 · see citing works
Models of neuromodulation for computational psychiatry
Iglesias, S., Tomiello, S., Schneebeli, M., & Stephan, K. E. (2016) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1420 · Cited by 26 · see citing works
Gil-Lievana, E., Ramírez-Mejía, G., Urrego-Morales, O., Luis-Islas, J., Gutiérrez, R., & Bermúdez‐Rattoni, F. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.823220 · Cited by 27 · see citing works
Finan, P. H., Remeniuk, B., & Dunn, K. E. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.07.029 · Cited by 26 · see citing works
Langdon, A., Song, M., & Niv, Y. (2019) · Behavioural Processes · doi:10.1016/j.beproc.2019.103891 · Cited by 25 · see citing works
Learning to represent reward structure: A key to adapting to complex environments
Nakahara, H., & Hikosaka, O. (2012) · Neuroscience Research · doi:10.1016/j.neures.2012.09.007 · Cited by 25 · see citing works
Colizoli, O., de Gee, J. W., van der Zwaag, W., & Donner, T. H. (2021) · Human Brain Mapping · doi:10.1002/hbm.25719 · Cited by 22 · see citing works
Visual cognition of birds and its underlying neural mechanism: A review
Niu, X., Jiang, Z., Peng, Y., Huang, S., Wang, Z., & Shi, L. (2022) · Avian Research · doi:10.1016/j.avrs.2022.100023 · Cited by 22 · see citing works
Jahn, C. I., Varazzani, C., Sallet, J., Walton, M. E., & Bouret, S. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa089 · Cited by 21 · see citing works
Sarno, S., Beirán, M., Falcó-Roget, J., Diaz-deLeon, G., Rossi-Pool, R., Romo, R., & Parga, N. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2113311119 · Cited by 20 · see citing works
Reward eliminates retrieval-induced forgetting
Imai, H., Kim, D., Sasaki, Y., & Watanabe, T. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404469111 · Cited by 21 · see citing works
Self-citationReward prediction error in learning-related behaviors
Yujun, D., Song, D. F., Ni, J., Qing, H., & Quan, Z. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1171612 · Cited by 25 · see citing works
Hasirci, A. S., Maldonado‐Devincci, A. M., Beattie, M. C., O’Buckley, T. K., & Morrow, A. L. (2017) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13300 · Cited by 19 · see citing works
Rubin, J. E., Vich, C., Clapp, M., Noneman, K. K., & Verstynen, T. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14745 · Cited by 22 · see citing works
Reward and value coding by dopamine neurons in non-human primates
Alikaya, A., Rack-Wildner, M., & Stauffer, W. R. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1793-9 · Cited by 18 · see citing works
Contributions of the Basal Ganglia to Visual Perceptual Decisions
Ding, L. (2023) · Annual Review of Vision Science · doi:10.1146/annurev-vision-111022-123804 · Cited by 20 · see citing works
Cortical regulation of dopaminergic neurons: role of the midbrain superior colliculus
Bertram, C., Dahan, L., Boorman, L. W., Harris, S., Vautrelle, N., Leriche, M., Redgrave, P., & Overton, P. G. (2013) · Journal of Neurophysiology · doi:10.1152/jn.00329.2013 · Cited by 17 · see citing works
Psychological and Neuroscientific Connections with Reinforcement Learning
Shah, A. (2012) · Adaptation, learning, and optimization · doi:10.1007/978-3-642-27645-3_16 · Cited by 17 · see citing works
Burkhardt, J. M., & Adermark, L. (2014) · Neurochemistry International · doi:10.1016/j.neuint.2014.07.006 · Cited by 17 · see citing works
Tomassini, A., Pollak, T. A., Edwards, M. J., & Bestmann, S. (2019) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2019.02.003 · Cited by 16 · see citing works
Blank, H., Biele, G., Heekeren, H. R., & Philiastides, M. G. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.4151-12.2013 · Cited by 18 · see citing works
Portella, A. K., Papantoni, A., Joseph, A. T., Chen, L., Lee, R. S., Silveira, P. P., Dubé, L., & Carnell, S. (2021) · Scientific Reports · doi:10.1038/s41598-021-02797-9 · Cited by 15 · see citing works
Fan, Y., Doi, T., Gold, J. I., & Ding, L. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0902-23.2023 · Cited by 20 · see citing works
Stimulus-Dependent Adjustment of Reward Prediction Error in the Midbrain
Takemura, H., Samejima, K., Vogels, R., Sakagami, M., & Okuda, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028337 · Cited by 15 · see citing works
Self-citationSaga, Y., Hashimoto, M., Tremblay, L., Tanji, J., & Hoshi, E. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1187-13.2013 · Cited by 14 · see citing works
Dopamine activity on the perceptual salience for recognition memory
Osorio‐Gómez, D., Guzmán-Ramos, K. R., & Bermúdez‐Rattoni, F. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.963739 · Cited by 13 · see citing works
Signals of anticipation of reward and of mean reward rates in the human brain
Viviani, R., Dommes, L., Bosch, J., Steffens, M., Paul, A., Schneider, K. L., Stingl, J., & Beschoner, P. (2020) · Scientific Reports · doi:10.1038/s41598-020-61257-y · Cited by 14 · see citing works
Pasquereau, B., Tremblay, L., & Turner, R. S. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.12.016 · Cited by 13 · see citing works
- Authors
- Nomoto, K., Schultz, W., Watanabe, T., & Sakagami, M.
- Affiliations
- Tamagawa University (JP)
- Boston University (US)
- Corresponding author
- Sakagami, Masamichi
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-08-11
- Volume
- 30
- Issue
- 32
- Pages
- 10692-10702
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3297489
- OpenAlex
- W2120222754
- Cited by
- 158
- References
- 41
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 7 · 2023: 9 · 2022: 7 · 2021: 11 · 2020: 11 · 2019: 10 · 2018: 14 · 2017: 16 · 2016: 14 · 2015: 5 · 2014: 16 · 2013: 13 · 2012: 10
- FWCI
- 4.26
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (095495)
- National Institutes of Health
- National Eye Institute (R01EY015980, R01EY019466)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- dopaminergic neurons, reward prediction error, reward prediction, random dot motion, motion direction discrimination, midbrain dopamine
- MeSH terms
- Acoustic Stimulation, Analysis of Variance, Animals, Behavior, Animal, Conditioning, Operant, Discrimination, Psychological, Dopamine, Functional Laterality, Macaca fascicularis, Magnetic Resonance Imaging, Male, Mesencephalon, Motion Perception, Neurons, Orientation, Photic Stimulation, Predictive Value of Tests, Reward, Saccades, Time Factors, Tyrosine 3-Monooxygenase, Feedback, Physiological
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
