Lateral habenula neurons signal errors in the prediction of reward information
Open accessAbstract
Humans and animals have the ability to predict future events, which they cultivate by continuously searching their environment for sources of predictive information. However, little is known about the neural systems that motivate this behavior. We hypothesized that information-seeking is assigned value by the same circuits that support reward-seeking, such that neural signals encoding reward prediction errors (RPEs) include analogous information prediction errors (IPEs). To test this, we recorded from neurons in the lateral habenula, a nucleus that encodes RPEs, while monkeys chose between cues that provided different chances to view information about upcoming rewards. We found that a subpopulation of lateral habenula neurons transmitted signals resembling IPEs, responding when reward information was unexpectedly cued, delivered or denied. These signals evaluated information sources reliably, even when the monkey's decisions did not. These neurons could provide a common instructive signal for reward-seeking and information-seeking behavior.
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?
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 [152]
These slow changes fail to occur with more-controlled arm, mouth and eye movements in a considerable range of studies.
“these changes fail to occur with more-controlled arm, mouth and eye movements in a considerable range of studies2,5,9,13,151,152,154”
From Dopamine reward prediction-error signalling: A two-component response (2016) · cites this paper as [152]
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
Reinforcement Learning: An Introduction
Sutton, R. S., & Barto, A. (2005) · IEEE Transactions on Neural Networks · doi:10.1109/tnn.2004.842673 · Cited by 25,263 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Rescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268 · see citing works
Classical conditioning II: Current research and theory.
Black, A. H., & Prokasy, W. F. (1972) · Appleton-Century-Crofts eBooks · Cited by 4,449 · see citing works
Holroyd, C. B., & Coles, M. G. H. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.679 · Cited by 4,027 · see citing works
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
Self-citationCortical substrates for exploratory decisions in humans
Daw, N. D., O'Doherty, J. P., Dayan, P., Seymour, B., & Dolan, R. J. (2006) · Nature · doi:10.1038/nature04766 · Cited by 2,224 · see citing works
A framework for mesencephalic dopamine systems based on predictive Hebbian learning
Montague, P., Dayan, P., & Sejnowski, T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-05-01936.1996 · Cited by 2,066 · see citing works
Temporal Resolution of Uncertainty and Dynamic Choice Theory
Kreps, D. M., & Porteus, E. L. (1978) · Econometrica · doi:10.2307/1913656 · Cited by 1,753 · see citing works
Temporal difference models and reward-related learning in the human brain
O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00169-7 · Cited by 1,522 · see citing works
Two types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378 · see citing works
Self-citationMidbrain 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
Self-citationModels of Information Processing in the Basal Ganglia
(1994) · doi:10.7551/mitpress/4708.001.0001 · Cited by 1,190 · see citing works
Honig, W. K., & Staddon, J. E. R. (2022) · Routledge eBooks · doi:10.4324/9781003256670 · Cited by 970 · see citing works
The habenula: from stress evasion to value-based decision-making
Hikosaka, O. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2866 · Cited by 955 · see citing works
Self-citationTemporal Prediction Errors in a Passive Learning Task Activate Human Striatum
McClure, S. M., Berns, G. S., & Montague, P. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00154-5 · Cited by 917 · see citing works
Psychological Expected Utility Theory and Anticipatory Feelings
Caplin, A., & Leahy, J. V. (2001) · The Quarterly Journal of Economics · doi:10.1162/003355301556347 · Cited by 812 · see citing works
The short-latency dopamine signal: a role in discovering novel actions?
Redgrave, P., & Gurney, K. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn2022 · Cited by 762 · see citing works
Metalearning and neuromodulation
Doya, K. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00044-8 · Cited by 704 · see citing works
Roesch, M. R., Calu, D. J., & Schoenbaum, G. (2007) · Nature Neuroscience · doi:10.1038/nn2013 · Cited by 597 · see citing works
A Model of How the Basal Ganglia Generate and Use Neural Signals That Predict Reinforcement
Houk, J. C., Adams, J. L., & Barto, A. G. (1994) · The MIT Press eBooks · doi:10.7551/mitpress/4708.003.0020 · Cited by 555 · see citing works
Midbrain Dopamine Neurons Signal Preference for Advance Information about Upcoming Rewards
Bromberg-Martin, E. S., & Hikosaka, O. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.009 · Cited by 548 · see citing works
Self-citationRepresentation of negative motivational value in the primate lateral habenula
Matsumoto, M., & Hikosaka, O. (2009) · Nature Neuroscience · doi:10.1038/nn.2233 · Cited by 547 · see citing works
Self-citationThe role of observing responses in discrimination learning. Part I.
Wyckoff, L. B. (1952) · Psychological Review · doi:10.1037/h0053932 · Cited by 507 · 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
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Medial prefrontal cell activity signaling prediction errors of action values
Matsumoto, M., Matsumoto, K., Abe, H., & Tanaka, K. (2007) · Nature Neuroscience · doi:10.1038/nn1890 · Cited by 440 · see citing works
Christoph, G., Leonzio, R., & Wilcox, K. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-03-00613.1986 · Cited by 418 · see citing works
Ji, H., & Shepard, P. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0958-07.2007 · Cited by 388 · see citing works
The globus pallidus sends reward-related signals to the lateral habenula
Hong, S., & Hikosaka, O. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.035 · Cited by 346 · see citing works
Self-citationSeo, H., & Lee, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2369-07.2007 · Cited by 324 · see citing works
Observing and conditioned reinforcement
Dinsmoor, J. A. (1983) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00017969 · Cited by 307 · see citing works
Reward-Dependent Modulation of Neuronal Activity in the Primate Dorsal Raphe Nucleus
Nakamura, K., Matsumoto, M., & Hikosaka, O. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0021-08.2008 · Cited by 243 · see citing works
Self-citationRole of Striatum in Updating Values of Chosen Actions
Kim, H., Sul, J. H., Huh, N., Lee, D., & Jung, M. W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2728-09.2009 · Cited by 225 · see citing works
Ranade, S., & Mainen, Z. F. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00507.2009 · Cited by 174 · see citing works
Neural Dissociation of Delay and Uncertainty in Intertemporal Choice
Luhmann, C. C., Chun, M. M., Yi, D.-J., Lee, D., & Wang, X. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5058-08.2008 · Cited by 150 · see citing works
The acquisition of observing responses in the absence of differential external reinforcement.
Prokasy, W. F. (1956) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0046740 · Cited by 146 · see citing works
BOLD responses to negative reward prediction errors in human habenula
Salas (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00036 · Cited by 131 · see citing works
Hope: An empirical study of attitude toward the timing of uncertainty resolution
Chew, S. H., & Ho, J. L. Y. (1994) · Journal of Risk and Uncertainty · doi:10.1007/bf01064045 · Cited by 127 · see citing works
Lecourtier, L., Oranburg, T. D., & Moghaddam, B. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06130.x · Cited by 125 · see citing works
The dynamics of dopamine in control of motor behavior
Joshua, M., Adler, A., & Bergman, H. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.001 · Cited by 109 · see citing works
Toward a quantitative theory of secondary reinforcement.
Wyckoff, L. B. (1959) · Psychological Review · doi:10.1037/h0046882 · Cited by 106 · see citing works
Ambiguity aversion in rhesus macaques
Hayden, B. Y. (2010) · Frontiers in Neuroscience · doi:10.3389/fnins.2010.00166 · Cited by 101 · see citing works
Friedman, A., Lax, E., Dikshtein, Y., Abraham, L., Flaumenhaft, Y., Sudai, E., Ben‐Tzion, M., & Yadid, G. (2010) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.10.006 · Cited by 96 · see citing works
Reward Prediction Error Coding in Dorsal Striatal Neurons
Oyama, K., Hernádi, I., Iijima, T., & Tsutsui, K. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1719-10.2010 · Cited by 91 · see citing works
Multiple Timescales of Memory in Lateral Habenula and Dopamine Neurons
Bromberg-Martin, E. S., Matsumoto, M., Nakahara, H., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.031 · Cited by 91 · see citing works
Self-citationGormezano, I. (2013) · Psychology Press eBooks · doi:10.4324/9780203772515 · Cited by 86 · see citing works
Shumake, J., Ilango, A., Scheich, H., Wetzel, W., & Ohl, F. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3604-09.2010 · Cited by 82 · see citing works
Self-stimulation of the habenular complex in the rat.
Sutherland, R. J., & Nakajima, S. (1981) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077833 · Cited by 77 · see citing works
Experimental Testing of Intrinsic Preferences for NonInstrumental Information
Eliaz, K., & Schotter, A. (2007) · American Economic Review · doi:10.1257/aer.97.2.166 · Cited by 72 · see citing works
Infomax Control of Eye Movements
Butko, N. J., & Movellan, J. R. (2010) · IEEE Transactions on Autonomous Mental Development · doi:10.1109/tamd.2010.2051029 · Cited by 51 · see citing works
Pavlovian-Instrumental Interaction in ‘Observing Behavior’
Beierholm, U., & Dayan, P. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000903 · Cited by 35 · see citing works
Acquisition and extinction of the observing response as a function of stimulus predictive validity
Ward, E. F. (1971) · Psychonomic Science · doi:10.3758/bf03331790 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
Dopamine 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
The Psychology and Neuroscience of Curiosity
Kidd, C., & Hayden, B. Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.010 · Cited by 1,026 · see citing works
Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance
Stamatakis, A. M., & Stuber, G. D. (2012) · Nature Neuroscience · doi:10.1038/nn.3145 · Cited by 564 · see citing works
Reward processing by the lateral habenula in normal and depressive behaviors
Proulx, C. D., Hikosaka, O., & Malinow, R. (2014) · Nature Neuroscience · doi:10.1038/nn.3779 · Cited by 461 · see citing works
Self-citationHow people decide what they want to know
Sharot, T., & Sunstein, C. R. (2020) · Nature Human Behaviour · doi:10.1038/s41562-019-0793-1 · Cited by 386 · see citing works
The ventral pallidum: Subregion-specific functional anatomy and roles in motivated behaviors
Root, D. H., Meléndez, R. I., Záborszky, L., & Napier, T. C. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.005 · Cited by 343 · see citing works
A computational framework for the study of confidence in humans and animals
Kepecs, A., & Mainen, Z. F. (2012) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0037 · Cited by 305 · see citing works
Blanchard, T. C., Hayden, B. Y., & Bromberg-Martin, E. S. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.050 · Cited by 301 · see citing works
Self-citationPutting Reward in Art: A Tentative Prediction Error Account of Visual Art
de Cruys, S. V., & Wagemans, J. P. (2011) · i-Perception · doi:10.1068/i0466aap · Cited by 296 · see citing works
Curiosity and reward: Valence predicts choice and information prediction errors enhance learning.
Marvin, C. B., & Daphna Shohamy, A. (2016) · Journal of Experimental Psychology General · doi:10.1037/xge0000140 · Cited by 263 · see citing works
Valuation of knowledge and ignorance in mesolimbic reward circuitry
Charpentier, C. J., Bromberg-Martin, E. S., & Sharot, T. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800547115 · Cited by 237 · see citing works
Self-citationNeural Circuit Motifs in Valence Processing
Tye, K. M. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.001 · Cited by 247 · see citing works
NOW vs LATER brain circuits: implications for obesity and addiction
Volkow, N. D., & Baler, R. D. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.002 · Cited by 237 · see citing works
Surprise and Error: Common Neuronal Architecture for the Processing of Errors and Novelty
Wessel, J. R., Danielmeier, C., Morton, J. B., & Ullsperger, M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6352-11.2012 · Cited by 226 · see citing works
Distributed and Mixed Information in Monosynaptic Inputs to Dopamine Neurons
Tian, J., Huang, R., Cohen, J. Y., Osakada, F., Kobak, D., Machens, C. K., Callaway, E. M., Uchida, N., & Watabe-Uchida, M. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.018 · Cited by 224 · see citing works
Identity-specific coding of future rewards in the human orbitofrontal cortex
Howard, J. D., Gottfried, J. A., Tobler, P. N., & Kahnt, T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503550112 · Cited by 222 · see citing works
A new control center for dopaminergic systems: pulling the VTA by the tail
Bourdy, R., & Barrot, M. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.06.007 · Cited by 208 · see citing works
A universal role of the ventral striatum in reward-based learning: Evidence from human studies
Daniel, R., & Pollmann, S. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.05.002 · Cited by 209 · see citing works
Intrinsic Valuation of Information in Decision Making under Uncertainty
Bennett, D., Bode, S., Brydevall, M., Warren, H. A., & Murawski, C. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005020 · Cited by 186 · see citing works
A hypothalamus-habenula circuit controls aversion
Lazaridis, I., Tzortzi, O., Weglage, M., Märtin, A., Xuan, Y., Parent, M. A., Johansson, Y., Fuzik, J., Fürth, D., Fenno, L. E., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0369-5 · Cited by 180 · see citing works
Molecular Mechanisms Underlying Behaviors Related to Nicotine AddictionPreprint
Picciotto, M. R., & Kenny, P. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012112 · Cited by 178 · see citing works
Nicotine aversion: Neurobiological mechanisms and relevance to tobacco dependence vulnerability
Fowler, C. D., & Kenny, P. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.09.008 · Cited by 167 · see citing works
Oleson, E. B., Beckert, M., Morra, J. T., Lansink, C. S., Cachope, R., Abdullah, R. A., Loriaux, A. L., Schetters, D., Pattij, T., Roitman, M. F., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.018 · Cited by 168 · see citing works
Pezzulo, G., Rigoli, F., & Chersi, F. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00092 · Cited by 163 · see citing works
Mechanisms of Nicotine Addiction
Picciotto, M. R., & Kenny, P. J. (2021) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039610 · Cited by 157 · see citing works
Induction and Relief of Curiosity Elicit Parietal and Frontal Activity
van Lieshout, L. L. F., Vandenbroucke, A. R. E., Müller, N. C. J., Cools, R., & de Lange, F. P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2816-17.2018 · Cited by 151 · see citing works
Orsini, C. A., Moorman, D. E., Young, J. W., Setlow, B., & Floresco, S. B. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.009 · Cited by 153 · see citing works
Common neural code for reward and information value
Kobayashi, K., & Hsu, M. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820145116 · Cited by 148 · see citing works
Behavioral, Physiological, and Neural Signatures of Surprise during Naturalistic Sports Viewing
Antony, J. W., Hartshorne, T. H., Pomeroy, K., Gureckis, T. M., Hasson, U., McDougle, S. D., & Norman, K. A. (2020) · Neuron · doi:10.1016/j.neuron.2020.10.029 · Cited by 146 · see citing works
Irrational choice and the value of information
Vasconcelos, M., Monteiro, T., & Kacelnik, A. (2015) · Scientific Reports · doi:10.1038/srep13874 · Cited by 139 · see citing works
Namboodiri, V. M. K., Rodríguez-Romaguera, J., & Stuber, G. D. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.051 · Cited by 143 · see citing works
Overriding Phasic Dopamine Signals Redirects Action Selection during Risk/Reward Decision Making
Stopper, C. M., Tse, M. T. L., Montes, D. R., Wiedman, C. R., & Floresco, S. B. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.033 · Cited by 136 · see citing works
What's better for me? Fundamental role for lateral habenula in promoting subjective decision biases
Stopper, C. M., & Floresco, S. (2013) · Nature Neuroscience · doi:10.1038/nn.3587 · Cited by 129 · see citing works
Unmasking the mysteries of the habenula in pain and analgesia
Shelton, L., Becerra, L. R., & Borsook, D. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.01.004 · Cited by 128 · see citing works
A neural network for information seeking
White, J. K., Bromberg-Martin, E. S., Heilbronner, S. R., Zhang, K., Pai, J., Haber, S. N., & Monosov, I. E. (2019) · Nature Communications · doi:10.1038/s41467-019-13135-z · Cited by 129 · see citing works
Self-citationMapping pain activation and connectivity of the human habenula
Shelton, L., Pendse, G., Maleki, N., Moulton, E. A., Lebel, A., Becerra, L. R., & Borsook, D. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00012.2012 · Cited by 128 · see citing works
Prediction errors disrupt hippocampal representations and update episodic memories
Sinclair, A. H., Manalili, G. M., Brunec, I. K., Adcock, R. A., & Barense, M. D. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2117625118 · Cited by 128 · see citing works
The neural encoding of information prediction errors during non-instrumental information seeking
Brydevall, M., Bennett, D., Murawski, C., & Bode, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-24566-x · Cited by 117 · see citing works
Hsu, Y. A., Wang, S. D., Wang, S., Morton, G., Zariwala, H. A., de la Iglesia, H. O., & Turner, E. E. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1861-14.2014 · Cited by 115 · see citing works
The modulation of savouring by prediction error and its effects on choice
Iigaya, K., Story, G. W., Kurth-Nelson, Z. L., Dolan, R. J., & Dayan, P. (2016) · eLife · doi:10.7554/elife.13747 · Cited by 110 · see citing works
Pistillo, F., Clementi, F., Zoli, M., & Gotti, C. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.10.002 · Cited by 113 · see citing works
Anhedonia in depression symptomatology: appetite dysregulation and defective brain reward processing
Coccurello, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112041 · Cited by 106 · see citing works
Bloem, B., Huda, R., Sur, M., & Graybiel, A. M. (2017) · eLife · doi:10.7554/elife.32353 · Cited by 99 · see citing works
Excitatory pathways from the lateral habenula enable propofol-induced sedation
Gelegen, C., Miracca, G., Ran, M. Z., Harding, E. C., Ye, Z., Yu, X., Tossell, K., Houston, C. M., Yustos, R., Hawkins, E. D., et al. (2018) · Current Biology · doi:10.1016/j.cub.2017.12.050 · Cited by 100 · see citing works
Affective Value in the Predictive Mind
Van De Cruys, S. (2017) · Theoretical Philosophy/MIND Group – JGU Mainz · doi:10.15502/9783958573253 · Cited by 100 · see citing works
Progress in understanding mood disorders: optogenetic dissection of neural circuits
Lammel, S., Tye, K. M., & Warden, M. R. (2014) · Genes, Brain and Behavior · doi:10.1111/gbb.12049 · Cited by 98 · see citing works
A primate temporal cortex–zona incerta pathway for novelty seeking
Ogasawara, T., Sogukpinar, F., Zhang, K., Feng, Y.-Y., Pai, J., Jezzini, A., & Monosov, I. E. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00950-1 · Cited by 96 · see citing works
Play, Curiosity, and Cognition
Chu, J., & Schulz, L. E. (2020) · Annual Review of Developmental Psychology · doi:10.1146/annurev-devpsych-070120-014806 · Cited by 93 · see citing works
The seductive lure of curiosity: information as a motivationally salient reward
FitzGibbon, L., Lau, J. K. L., & Murayama, K. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.05.014 · Cited by 94 · see citing works
The habenula in psychiatric disorders: More than three decades of translational investigation
Fakhoury, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.010 · Cited by 90 · see citing works
The Lateral Habenula and Adaptive Behaviors
Mizumori, S. J. Y., & Baker, P. M. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.06.001 · Cited by 86 · see citing works
Review of the cytology and connections of the lateral habenula, an avatar of adaptive behaving
Zahm, D. S., & Root, D. H. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.06.004 · Cited by 91 · see citing works
Neural circuitry of information seeking
Bromberg-Martin, E. S., & Monosov, I. E. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.07.006 · Cited by 89 · see citing works
Self-citationBrown, P. L., Palacorolla, H., Brady, D. L., Riegger, K. E., Elmer, G. I., & Shepard, P. D. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1353-16.2016 · Cited by 90 · see citing works
Norepinephrine Activates Dopamine D 4 Receptors in the Rat Lateral Habenula
Root, D. H., Hoffman, A. F., Good, C. H., Zhang, S., Gigante, E. D., Lupica, C. R., & Morales, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4525-13.2015 · Cited by 80 · see citing works
Asking the right questions about the psychology of human inquiry: Nine open challenges
Coenen, A., Nelson, J. D., & Gureckis, T. M. (2018) · Psychonomic Bulletin & Review · doi:10.3758/s13423-018-1470-5 · Cited by 84 · see citing works
Dopamine D 4 Receptor Excitation of Lateral Habenula Neurons via Multiple Cellular Mechanisms
Good, C. H., Wang, H., Chen, Y.-H., Mejías-Aponte, C. A., Hoffman, A. F., & Lupica, C. R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1844-13.2013 · Cited by 80 · see citing works
Why so curious? Quantifying mechanisms of information seeking
van Lieshout, L. L. F., de Lange, F. P., & Cools, R. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.08.005 · Cited by 79 · see citing works
Median raphe controls acquisition of negative experience in the mouse
Szőnyi, A., Zichó, K., Barth, A. M., Gönczi, R., Schlingloff, D., Török, B., Sipos, E., Major, Á., Bardóczi, Z., Sos, K. E., et al. (2019) · Science · doi:10.1126/science.aay8746 · Cited by 76 · see citing works
Iigaya, K., Hauser, T. U., Kurth-Nelson, Z. L., O’Doherty, J. P., Dayan, P., & Dolan, R. J. (2020) · Science Advances · doi:10.1126/sciadv.aba3828 · Cited by 87 · see citing works
Wong, A. L., Lindquist, M. A., Haith, A. M., & Krakauer, J. W. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00218.2015 · Cited by 76 · see citing works
Understanding the habenula: A major node in circuits regulating emotion and motivation
Ables, J. L., Park, K., & Ibáñez-Tallon, I. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106734 · Cited by 76 · see citing works
Anhedonia in Depression and Schizophrenia: Brain Reward and Aversion Circuits
Liang, S., Wu, Y. Z., Hanxiaoran, L., Greenshaw, A. J., & Li, T. (2022) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s367839 · Cited by 72 · see citing works
Cell-type-specific population dynamics of diverse reward computations
Sylwestrak, E., Jo, Y., Vesuna, S. S., Wang, X., Holcomb, B., Tien, R. H., Kim, D. K., Fenno, L. E., Ramakrishnan, C., Allen, W. E., et al. (2022) · Cell · doi:10.1016/j.cell.2022.08.019 · Cited by 68 · see citing works
From controlled to compulsive drug-taking: The role of the habenula in addiction
Mathis, V., & Kenny, P. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.06.018 · Cited by 71 · see citing works
A model of mood as integrated advantage.
Bennett, D., Davidson, G., & Niv, Y. (2021) · Psychological Review · doi:10.1037/rev0000294 · Cited by 69 · see citing works
Tricomi, E., & Fiez, J. A. (2012) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-011-0077-3 · Cited by 64 · see citing works
Rolls, E. T. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.013 · Cited by 62 · see citing works
Addiction‐related neuroadaptations following chronic nicotine exposure
Wills, L., & Kenny, P. J. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15356 · Cited by 61 · see citing works
Arbel, Y., Goforth, K., & Donchin, E. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00385 · Cited by 61 · see citing works
A shared novelty-seeking basis for creativity and curiosity
Ivancovsky, T., Baror, S., & Bar, M. (2023) · Behavioral and Brain Sciences · doi:10.1017/s0140525x23002807 · Cited by 62 · see citing works
Li, H., Vento, P. J., Parrilla-Carrero, J., Pullmann, D., Chao, Y. S., Eid, M., & Jhou, T. C. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.040 · Cited by 59 · see citing works
The neuroscience of active learning and direct instruction
Dubinsky, J. M., & Hamid, A. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105737 · Cited by 101 · see citing works
“I Want to Know the Answer! Give Me Fish ’n’ Chips!”: The Impact of Curiosity on Indulgent Choice
Wang, C., & Huang, Y. (2017) · Journal of Consumer Research · doi:10.1093/jcr/ucx086 · Cited by 57 · see citing works
Mathis, V., Cosquer, B., Avallone, M., Cassel, J., & Lecourtier, L. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.140 · Cited by 55 · see citing works
Latent learning, cognitive maps, and curiosity
Wang, M. Z., & Hayden, B. Y. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.06.003 · Cited by 58 · see citing works
Predicting the Accuracy of a Decision: A Neural Mechanism of ConfidencePreprint
Fetsch, C. R., Kiani, R., & Shadlen, M. N. (2014) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2014.79.024893 · Cited by 54 · see citing works
Phosphorylation of MeCP2 at Ser421 Contributes to Chronic Antidepressant Action
Hutchinson, A. N., Deng, J. V., Cohen, S., & West, A. E. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.2156-12.2012 · Cited by 53 · see citing works
On the joys of perceiving: Affect as feedback for perceptual predictions
Четвериков, А. А., & Kristjansson, A. K. (2016) · Acta Psychologica · doi:10.1016/j.actpsy.2016.05.005 · Cited by 53 · see citing works
Reinforcement learning with Marr
Niv, Y., & Langdon, A. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.04.005 · Cited by 49 · see citing works
Marvin, C. B., Tedeschi, E., & Daphna Shohamy, A. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.08.003 · Cited by 50 · see citing works
Monosov, I. E., & Rushworth, M. F. S. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01079-2 · Cited by 48 · see citing works
Systems neuroscience of curiosity
Cervera, R. L., Wang, M. Z., & Hayden, B. Y. (2020) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2020.06.011 · Cited by 56 · see citing works
Curiosity-driven exploration: foundations in neuroscience and computational modeling
Modirshanechi, A., Kondrakiewicz, K., Gerstner, W., & Haesler, S. (2023) · Trends in Neurosciences · doi:10.1016/j.tins.2023.10.002 · Cited by 48 · see citing works
The Lateral Habenula as a Relay of Cortical Information to Process Working Memory
Mathis, V., Barbelivien, A., Majchrzak, M. J., Mathis, C., Cassel, J., & Lecourtier, L. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw316 · Cited by 48 · see citing works
Anxiety during alcohol withdrawal involves 5-HT2C receptors and M-channels in the lateral habenula
Fu, R., Mei, Q., Shiwalkar, N., Zuo, W., Zhang, H., Gregor, D. M., Patel, S., & Ye, J.-H. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107863 · Cited by 46 · see citing works
The lateral habenula: A hub for value-guided behavior
Groos, D., & Helmchen, F. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113968 · Cited by 43 · see citing works
Baker, P. M., Raynor, S. A., Francis, N.-M., & Mizumori, S. J. Y. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.02.010 · Cited by 43 · see citing works
The ventral striatum dissociates information expectation, reward anticipation, and reward receipt
Filimon, F., Nelson, J. D., B, T. J. S. A., Sereno, M. I., & Cottrell, G. W. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1911778117 · Cited by 46 · see citing works
Bennett, D., Sutcliffe, K., Tan, N. P., Smillie, L. D., & Bode, S. (2020) · Journal of Experimental Psychology General · doi:10.1037/xge0000966 · Cited by 43 · see citing works
Control of behavioral flexibility by the lateral habenula
Baker, P. M., & Mizumori, S. J. Y. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.07.012 · Cited by 44 · see citing works
Curiosity or savouring? Information seeking is modulated by both uncertainty and valence
van Lieshout, L. L. F., Traast, I. J., de Lange, F. P., & Cools, R. (2021) · PLoS ONE · doi:10.1371/journal.pone.0257011 · Cited by 44 · see citing works
Uncertainty increases curiosity, but decreases happiness
van Lieshout, L. L. F., de Lange, F. P., & Cools, R. (2021) · Scientific Reports · doi:10.1038/s41598-021-93464-6 · Cited by 44 · see citing works
A 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
Self-citationCocaine facilitates glutamatergic transmission and activates lateral habenular neurons
Zuo, W., Chen, L., Wang, L., & Ye, J.-H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.01.008 · Cited by 42 · see citing works
The ventral habenulae of zebrafish develop in prosomere 2 dependent on Tcf7l2 function
Beretta, C. A., Dross, N., Bankhead, P., & Carl, M. (2013) · Neural Development · doi:10.1186/1749-8104-8-19 · Cited by 42 · see citing works
Networks of habenula-projecting cortical neurons regulate cocaine seeking
Mathis, V., Williams, M., Fillinger, C., & Kenny, P. J. (2021) · Science Advances · doi:10.1126/sciadv.abj2225 · Cited by 38 · see citing works
Retrospective model-based inference guides model-free credit assignment
Moran, R., Keramati, M., Dayan, P., & Dolan, R. J. (2019) · Nature Communications · doi:10.1038/s41467-019-08662-8 · Cited by 40 · see citing works
Stievenard, A., Méquinion, M., Andrews, Z. B., Destée, A., Chartier-Harlin, M.-C., Viltart, O., & Vanbesien-Mailliot, C. C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.11.021 · Cited by 39 · see citing works
- Authors
- Bromberg-Martin, E. S., & Hikosaka, O.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Bromberg-Martin, Ethan S
- Venue
- Nature Neuroscience
- Published
- 2011-08-21
- Volume
- 14
- Issue
- 9
- Pages
- 1209-1216
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3164948
- OpenAlex
- W2056746865
- Cited by
- 275
- References
- 54
- Citations by year
- 2026: 14 · 2025: 12 · 2024: 22 · 2023: 17 · 2022: 24 · 2021: 28 · 2020: 23 · 2019: 20 · 2018: 18 · 2017: 17 · 2016: 20 · 2015: 18 · 2014: 13 · 2013: 14 · 2012: 10
- FWCI
- 6.82
- Type
- journal article
- Language
- en
- Update notices
- erratum (2011-11-23)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 EY999999)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- lateral habenula, reward prediction error, information seeking, reward seeking, value of information, neural coding, decision-making, predictive information
- MeSH terms
- Action Potentials, Animals, Choice Behavior, Cues, Macaca mulatta, Male, Models, Neurological, Neurons, Photic Stimulation, Predictive Value of Tests, Probability, Reaction Time, Reward, ROC Curve, Time Factors, Signal Detection, Psychological, Habenula
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
