Reward expectancy in primate prefrental neurons
Abstract
The prefrontal cortex is important in the organization of goal-directed behaviour. When animals are trained to work for a particular goal or reward, reward 'expectancy' is processed by prefrontal neurons. Recent studies of the prefrontal cortex have concentrated on the role of working memory in the control of behaviour. In spatial delayed-response tasks, neurons in the prefrontal cortex show activity changes during the delay period between presentation of the cue and the reward, with some of the neurons being spatially specific (that is, responses vary with the cue position). Here I report that the delay activity in prefrontal neurons is dependent also on the particular reward received for the behavioural response, and to the way the reward is given. It seems that the prefrontal cortex may monitor the outcome of goal-directed behaviour.
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From Neuropsychology to Mental Structure
Shallice, T. (1988) · doi:10.1017/cbo9780511526817 · Cited by 4,072 · see citing works
Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex
Funahashi, S., Bruce, C. J., & Goldman-Rakic, P. S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.2.331 · Cited by 2,685 · see citing works
Purposive Behavior in Animals and Men
Rodhom, C., & Tolman, E. C. (1950) · The American Journal of Psychology · doi:10.2307/1418946 · Cited by 2,455 · see citing works
The Prefrontal Cortex: Anatomy, Physiology, and Neuropsychology of the Frontal Lobe
Fuster, J. M. (1980) · Cited by 2,367 · see citing works
Purposive Behavior in Animals and Men
Irwin, F. W. (1932) · Europe PMC (PubMed Central) · Cited by 1,867 · see citing works
Higher Cortical Functions in Man
Luria, A. R. (1980) · Springer eBooks · doi:10.1007/978-1-4615-8579-4 · Cited by 1,322 · see citing works
Fuster, J. M. (1973) · Journal of Neurophysiology · doi:10.1152/jn.1973.36.1.61 · Cited by 995 · see citing works
Higher Cortical Functions in Man
Luria, A. R. (1995) · Springer eBooks · doi:10.1007/978-1-4684-7741-2 · Cited by 893 · see citing works
Neuronal activity in monkey ventral striatum related to the expectation of reward
Schultz, W., Apicella, P., Scarnati, E., & Ljungberg, T. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04595.1992 · Cited by 744 · see citing works
Prefrontal cortical unit activity and delayed alternation performance in monkeys.
Kubota, K., & Niki, H. (1971) · Journal of Neurophysiology · doi:10.1152/jn.1971.34.3.337 · Cited by 717 · see citing works
Petrides, M., Alivisatos, B., Evans, A. C., & Meyer, E. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.3.873 · Cited by 660 · see citing works
Hikosaka, O., Sakamoto, M., & Usui, S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.4.814 · Cited by 579 · see citing works
An experimental study of representative factors in monkeys.
Tinklepaugh, O. L. (1928) · Journal of comparative psychology · doi:10.1037/h0075798 · Cited by 578 · see citing works
Prefrontal and cingulate unit activity during timing behavior in the monkey
Niki, H., & Watanabe, M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90328-7 · Cited by 507 · see citing works
Self-citationMcCarthy, G., Blamire, A. M., Puce, A., Nobre, A. C., Bloch, G., Hyder, F., Goldman-Rakic, P., & Shulman, R. G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8690 · Cited by 459 · see citing works
Prefrontal unit activity and delayed response: Relation to cue location versus direction of response
Niki, H., & Watanabe, M. (1976) · Brain Research · doi:10.1016/0006-8993(76)90924-0 · Cited by 325 · see citing works
Self-citationNeuronal activity in monkey striatum related to the expectation of predictable environmental events
Apicella, P., Scarnati, E., Ljungberg, T., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.3.945 · Cited by 305 · see citing works
Differential activity of prefrontal units during right and left delayed response trials
Niki, H. (1974) · Brain Research · doi:10.1016/0006-8993(74)90324-2 · Cited by 220 · see citing works
Selective Impairments in Managerial Knowledge Following Pre-Frontal Cortex Damage
Angela Sirigu, B., Zalla, T., Pillon, B., Grafman, J. H., Agid, Y., & Dubois, B. (1995) · Cortex · doi:10.1016/s0010-9452(13)80364-4 · Cited by 207 · see citing works
Sakagami, M., & Niki, H. (1994) · Experimental Brain Research · doi:10.1007/bf00241536 · Cited by 152 · see citing works
Prefrontal unit activity during associative learning in the monkey
Watanabe, M. (1990) · Experimental Brain Research · doi:10.1007/bf00228157 · Cited by 149 · see citing works
Self-citationFrontal units of the monkey coding the associative significance of visual and auditory stimuli
Watanabe, M. (1992) · Experimental Brain Research · doi:10.1007/bf00228241 · Cited by 123 · see citing works
Self-citationThe prefrontal cortex: Anatomy physiology and neurophysiology of the frontal lobe
Passingham, R. E. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90204-9 · Cited by 107 · see citing works
The appropriateness of behavioral responses coded in post-trial activity of primate prefrontal units
Watanabe, M. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90450-3 · Cited by 64 · see citing works
Self-citation
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An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Well-being : the foundations of hedonic psychology
Kahneman, D. J., Diener, E. F., & Schwarz, N. (1999) · Cited by 7,472 · 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
“…1992; Tremblay and Schultzstimuli, the further behavioral improvement might be mainly due to the acquisition of predictive processing of spatial 1995), and 4) modulations of behavior-related activations by predicted reward (Hollerman et al. 1994; Watanabe 1990,positions by other neuronal systems.”
BackgroundThe Neural Basis of Decision Making
Gold, J. I., & Shadlen, M. N. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.113038 · Cited by 3,764 · see citing works
“…of value-based decisions. been described in orbitofrontal and cingulate cortex and the basal ganglia, areas of the brain traditionally associated with reward-seeking behavior (Kawagoe et al. 2004; Lauwereyns et al. 2002; McCoy et al. 2003; Schultz 1992, 1999, 2000; Watanabe 1996; Watanabe et al. ).”
BackgroundMesulam, M. (1998) · Brain · doi:10.1093/brain/121.6.1013 · Cited by 3,072 · see citing works
“Furthermore, an arbitrary sensory cue elicits greater responses from dorsolateral prefrontal neurons when it signals the impending delivery of a preferred food item, such as a piece of apple or cabbage, than when it signals a less favourite food such as a raisin (Watanabe, 1996).”
BackgroundGetting formal with dopamine and reward
Schultz, W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00967-4 · Cited by 2,574 · see citing works
“…and amounts of food and Given the central importance of rewards for survival, reproduction, and competitive gains, it may not be sur-liquid rewards (Watanabe, 1996; Leon and Shadlen, 1999; Tremblay and Schultz, 1999; Hassani et al., 2001) prising that several specialized and only partly…”
InfluentialOn the relationship between emotion and cognition
Pessoa, L. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2317 · Cited by 2,350 · see citing works
The prefontral cortex and cognitive control
Miller, E. K. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036228 · Cited by 2,016 · see citing works
The Neuropsychology of Anxiety
Gray, J. A., & McNaughton, N. (2003) · doi:10.1093/acprof:oso/9780198522713.001.0001 · Cited by 1,933 · see citing works
The Prefrontal Cortex—An Update
Fuster, J. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00285-9 · Cited by 1,760 · see citing works
Behavioral Theories and the Neurophysiology of Reward
Schultz, W. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070229 · Cited by 1,637 · see citing works
“…supplementary eye field (Amador et al. 2000, Apicella et al. 1992, Cromwell & Schultz 2003, Hikosaka et al. 1989, Hollerman et al. 1998, Pratt & Mizumori 2001, Schoenbaum et al. 1998, Schultz et al. 1992, Shidara & Richmond 2002, Tremblay & Schultz 1999, 2000a, Watanabe 1996, Watanabe et al. 2002).”
BackgroundInfluentialFunctional imaging of neural responses to expectancy and experience of monetary gains and losses
Breiter, H. C., Aharon, I., Kahneman, D., Dale, A., & Shizgal, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00303-8 · Cited by 1,404 · see citing works
Multiple dopamine functions at different time courses
Schultz, W. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135722 · Cited by 1,415 · see citing works
“…the specific stimulus, movement, and delay-related changes in the millisecond and second range in prefrontal, parietal, and striatal neurons (Watanabe 1996, Hollerman et al. 1998, Platt & Glimcher 1999), suggesting that influences of rewards on task-specific neuronal processes have…”
BackgroundPhillips, M. L., Ladouceur, C. D., & Drevets, W. C. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.65 · Cited by 1,383 · see citing works
Relative reward preference in primate orbitofrontal cortex
Tremblay, L., & Schultz, W. (1999) · Nature · doi:10.1038/19525 · Cited by 1,314 · see citing works
Neural Correlates of Behavioral Preference for Culturally Familiar Drinks
McClure, S. M., Li, J., Tomlin, D., Cypert, K. S., Montague, L. M., & Montague, P. R. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.019 · Cited by 1,347 · see citing works
“Eachfor employing affective information in biasing behavior subject participated in one of three similarly designed experiments(Watanabe, 1996; Davidson and Irwin, 1999).”
BackgroundMethodRole of the Basal Ganglia in the Control of Purposive Saccadic Eye Movements
Hikosaka, O., Takikawa, Y., & Kawagoe, R. (2000) · Physiological Reviews · doi:10.1152/physrev.2000.80.3.953 · Cited by 1,287 · see citing works
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303 · see citing works
Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience.
Davidson, R. J., Jackson, D. C., & Kalin, N. H. (2000) · Psychological Bulletin · doi:10.1037/0033-2909.126.6.890 · Cited by 1,322 · see citing works
“The PFC is likely to play a role in affective working memory, a process critical to anticipating future affective outcomes (see, e.g., Watanabe, 1996).”
BackgroundNeuronal 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
Baxter, M. G., & Murray, E. A. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn875 · Cited by 1,200 · see citing works
Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep
Louie, K., & Wilson, M. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00186-6 · Cited by 1,148 · see citing works
Working memory as an emergent property of the mind and brain
Postle, B. R. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.005 · Cited by 1,151 · see citing works
“For example, the gain of delay-period activity of spatially tuned units in dorsolateral PFC is modulated by the type of reward anticipated on a particular trial (Watanabe, 1996).”
Anxiety and affective style: role of prefrontal cortex and amygdala
Davidson, R. J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01328-2 · Cited by 1,139 · see citing works
“It is likely that the PFC plays a key role in this process (see e.g., Watanabe 1996).”
BackgroundDopamine 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
Mental fatigue: Costs and benefits
Boksem, M. A. S., & Tops, M. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.07.001 · Cited by 1,142 · see citing works
“DA projections from the ventral tegmental area (VTA) convey information on reward value to the prefrontal cortex (PFC; Watanabe, 1996, Tremblay and Schultz, 1999).”
BackgroundSingle neurons in prefrontal cortex encode abstract rules
Wallis, J. D., Anderson, K. C., & Miller, E. K. (2001) · Nature · doi:10.1038/35082081 · Cited by 1,075 · see citing works
“They are activated by stimuli from all sensory modalitie”
BackgroundRepresentation of Confidence Associated with a Decision by Neurons in the Parietal Cortex
Kiani, R., & Shadlen, M. N. (2009) · Science · doi:10.1126/science.1169405 · Cited by 1,027 · see citing works
Complementary roles of basal ganglia and cerebellum in learning and motor control
Doya, K. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00153-7 · Cited by 964 · see citing works
Motivation and cognitive control: from behavior to neural mechanism
Botvinick, M., & Braver, T. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-015044 · Cited by 909 · see citing works
“For example, work by Watanabe and colleagues (Watanabe 1996, Watanabe et al. 2002) showed that PFC neurons involved in working memory display tonically www.annualreviews.org • Motivation and Cognitive Control 97 A nn u.”
BackgroundResultRepresentation of Action-Specific Reward Values in the Striatum
Samejima, K., Ueda, Y., Doya, K., & Kimura, M. (2005) · Science · doi:10.1126/science.1115270 · Cited by 939 · see citing works
Reward processing in primate orbitofrontal cortex and basal ganglia
Schultz, W. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.272 · Cited by 942 · see citing works
“Similar activities have been reported for the dorsolateral prefrontal cortex (Watanabe, 1996).”
BackgroundAn adaptive coding model of neural function in prefrontal cortex
Duncan, J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35097575 · Cited by 874 · see citing works
Orbitofrontal cortex and its contribution to decision-making.
Wallis, J. D. (2007) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.30.051606.094334 · Cited by 938 · see citing works
“…that reward-selective neurons were also in DLPFC (Amemori & Sawaguchi 2006, Hikosaka & Watanabe 2000, Kobayashi et al. 2002, Leon & Shadlen 1999, Watanabe 1996), and DLPFC neurons showed similar responses to OFC neurons during the performance of stimulus-reward reversal tasks (Wallis & Miller…”
Kang, M. J., Hsu, M., Krajbich, I. M., Loewenstein, G., McClure, S. M., Wang, J. T.-Y., & Camerer, C. F. (2009) · Psychological Science · doi:10.1111/j.1467-9280.2009.02402.x · Cited by 882 · see citing works
“The dorsal striatum responds to magnitude of primary rewards and reward prediction (Leon & Shadlen, 1999; Rogers et al., 1999) and shows sustained phasic activations during reward expectation (Watanabe, 1996).”
Affective style, psychopathology, and resilience: Brain mechanisms and plasticity.
Davidson, R. J. (2000) · American Psychologist · doi:10.1037//0003-066x.55.11.1196 · Cited by 886 · see citing works
Orbitofrontal Cortex Encodes Willingness to Pay in Everyday Economic Transactions
Plassmann, H., O'Doherty, J., & Rangel, A. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2131-07.2007 · Cited by 855 · see citing works
“This is consistent with previous monkey neurophysiology studies that have found neurons in the DLPFC that encode aspects of the decision or the incentive value of stimuli (Watanabe, 1996; Wallis and Miller, 2003).”
ResultChoice, uncertainty and value in prefrontal and cingulate cortex
Rushworth, M. F. S., & Behrens, T. E. J. (2008) · Nature Neuroscience · doi:10.1038/nn2066 · Cited by 866 · see citing works
Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning
Schoenbaum, G. M., Chiba, A. A., & Gallagher, M. (1998) · Nature Neuroscience · doi:10.1038/407 · Cited by 849 · see citing works
Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies
D’Esposito, M., Postle, B. R., & Rypma, B. (2000) · Experimental Brain Research · doi:10.1007/s002210000395 · Cited by 796 · see citing works
“In these tasks, the monkey must keep " in mind " , or actively maintain, a representation of the target stimulus [or of the anticipated probe stimulus (Rainer et al. 1999; Watanabe 1996)] over a short delay.”
BackgroundDopamine neurons and their role in reward mechanisms
Schultz, W. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80007-4 · Cited by 769 · see citing works
Coordination of Actions and Habits in the Medial Prefrontal Cortex of Rats
Killcross, S. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.4.400 · Cited by 748 · see citing works
Neurocomputational models of working memory
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Nature Neuroscience · doi:10.1038/81460 · Cited by 710 · see citing works
Neural computations that underlie decisions about sensory stimuli
Gold, J. I., & Shadlen, M. N. (2001) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01567-9 · Cited by 881 · see citing works
Neural activity in the human brain relating to uncertainty and arousal during anticipation.
Critchley, H. D., Mathias, C. J., & Dolan, R. J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00225-2 · Cited by 681 · see citing works
Prefrontal cortex and decision making in a mixed-strategy game
Barraclough, D. J., Conroy, M. L., & Lee, D. (2004) · Nature Neuroscience · doi:10.1038/nn1209 · Cited by 678 · see citing works
Decision Making in Recurrent Neuronal Circuits
Wang, X.-J. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.034 · Cited by 679 · see citing works
“Brain structures activated in decision making and modulated by reward signals include caudate (Samejima et al., 2005; Hikosaka et al., 2006), lateral parietal cortex area LIP (Platt and Glimcher, 1999; Sugrue et al., 2004), and prefrontal cortex (Watanabe, 1996; Roesch and Olson, 2003).”
BackgroundManoach, D. S. (2003) · Schizophrenia Research · doi:10.1016/s0920-9964(02)00294-3 · Cited by 681 · see citing works
“It is also consistent with single unit recordings from nonhuman primates demonstrating that the activity of neurons in the principal sulcus depends on the motivational context of a task (Watanabe et al., 2002) and increases during WM delays in anticipation of a preferred reward (Watanabe, 1996).”
BackgroundResultSolving the Distal Reward Problem through Linkage of STDP and Dopamine Signaling
Izhikevich, E. M. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl152 · Cited by 664 · see citing works
Neuroeconomics: Decision Making and the Brain
Rushworth, M. F. S., & Walton, M. E. (2009) · Neuron · doi:10.1016/j.neuron.2009.07.005 · Cited by 669 · see citing works
Doya, K. (2008) · Nature Neuroscience · doi:10.1038/nn2077 · Cited by 642 · see citing works
Segregation of working memory functions within the dorsolateral prefrontal cortex
Lévy, R., & Goldman, P. S. (2000) · Experimental Brain Research · doi:10.1007/s002210000397 · Cited by 641 · see citing works
“And, indeed, a wide range of operations integral to WM, including preparation, inhibition, or sequencing of motor responses and context-contingencies, have been consistently observed in DL cortex (Funahashi et al. 1993b, 1997; Williams and Goldman-Rakic 1995; Watanabe 1996).”
BackgroundExpectation 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
“However, there have been few physiological studies that manipulated the outcome of an action in terms of reward (its amount or kind) while keeping the subject's actions constan”
BackgroundWallis, J. D., & Miller, E. K. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02922.x · Cited by 628 · see citing works
“6 ' 8 & ' % "" & +, 11$ 1 "!”
Dopamine-Mediated Stabilization of Delay-Period Activity in a Network Model of Prefrontal Cortex
Durstewitz, D., Seamans, J. K., & B, T. J. S. A. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.3.1733 · Cited by 617 · see citing works
Izquierdo, A., Suda, R. K., & Murray, E. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1921-04.2004 · Cited by 588 · see citing works
A new perspective on the role of the orbitofrontal cortex in adaptive behaviour
Schoenbaum, G., Roesch, M. R., Stalnaker, T. A., & Takahashi, Y. K. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2753 · Cited by 585 · see citing works
Cortical and limbic activation during viewing of high- versus low-calorie foods
Killgore, W. D. S., Young, A. D., Femia, L. A., Bogorodzki, P., Rogowska, J., & Yurgelun-Todd, D. A. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00191-5 · Cited by 581 · see citing works
“Research with primates suggests that neurons within the dorsolateral prefrontal cortex are selectively activated when a reward is expected following a behavioral response (Watanabe, 1996).”
BackgroundMetalearning and neuromodulation
Doya, K. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00044-8 · Cited by 704 · see citing works
“V(s(t)) V(s(t-1)) are dependent on the amount and type of the reward associated with the memorized items (Watanabe, 1996; Tremblay & Schultz, 2000).”
BackgroundCortex and memory: emergence of a new paradigm
Fuster, J. M. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21280 · Cited by 559 · see citing works
“…Fuster, 1999; Carlson, Rämä, Tanila, Linnankoski, & Mansikka, 1997; Fuster et al., 1982) and/or the reward expected or resulting from motor action (Ichihara-Takeda & Funahashi, 2008; Hikosaka & Watanabe, 2000; Schultz, Tremblay, & Hollerman, 2000; Watanabe, 1996; Rosenkilde, Bauer, & Fuster, 1981).”
Integration of emotion and cognition in the lateral prefrontal cortex
Gray, J. R., Braver, T. S., & Raichle, M. E. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.062381899 · Cited by 792 · see citing works
Gold, J. I., & Shadlen, M. N. (2002) · Neuron · doi:10.1016/s0896-6273(02)00971-6 · Cited by 547 · see citing works
Choosing the greater of two goods: neural currencies for valuation and decision making
Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1666 · Cited by 536 · see citing works
Neural basis of deciding, choosing and acting
Schall, J. D. (2001) · Nature reviews. Neuroscience · doi:10.1038/35049054 · Cited by 528 · see citing works
Cross-modal and cross-temporal association in neurons of frontal cortex
Fuster, J. M., Bodner, M., & Kroger, J. K. (2000) · Nature · doi:10.1038/35012613 · Cited by 528 · see citing works
Schultz, W. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.017 · Cited by 517 · see citing works
“After the pioneering study by Watanabe [21] on reward-discriminating prefrontal activity, this work makes the next step by investigating the actual gain in neural information derived from the expectation of reward.”
BackgroundAllen, N. B., & Badcock, P. B. T. (2003) · Psychological Bulletin · doi:10.1037/0033-2909.129.6.887 · Cited by 494 · see citing works
Manoach, D. S., Gollub, R. L., Benson, E., Searl, M. M., GOFF, D. C., Halpern, E. F., Saper, C. B., & Rauch, S. L. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00227-4 · Cited by 502 · see citing works
“The participation of the dorsolateral prefrontal cortex (DLPFC) in WM is well established (Friedman and Goldman-Rakic 1994; Petrides et al 1993b) and most neuroimaging studies of WM in schizophrenia demonstrate aberrant DLPFC activation (Manoach et al 1999b; Weinberger and Berman 1996).”
BackgroundNeuronal mechanisms of executive control by the prefrontal cortex
Funahashi, S. (2001) · Neuroscience Research · doi:10.1016/s0168-0102(00)00224-8 · Cited by 493 · see citing works
“Neurophysiological studies using spatial working memory tasks such as the delayed-response task have revealed that many neurons in the prefrontal cortex exhibit delay-period activity (Fuster, 1973; Niki, 1974; Niki and Watanabe, 1976; Kojima and Goldman-Rakic, 1982, 1984; Funahashi et al., 1989; Watanabe, 1996; Carlso…”
BackgroundMethodPharmacology and behavioral pharmacology of the mesocortical dopamine system
Tzschentke, T. M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00033-2 · Cited by 481 · see citing works
Barch, D. M., & Dowd, E. C. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq068 · Cited by 478 · see citing works
Neurons in the frontal lobe encode the value of multiple decision variables
Kennerley, S. W., Dahmubed, A. F., Lara, A. H., & Wallis, J. D. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21100 · Cited by 453 · see citing works
“Moreover, OFC activity is correlated with the preference ranking of different rewards (Arana et al., 2003; Tremblay & Schultz, 1999; Watanabe, 1996) and the combination of reward preference and magnitude (Padoa-Schioppa & Assad, 2006, 2008).”
BackgroundLeon, M. I., & Shadlen, M. N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80854-5 · Cited by 449 · see citing works
Role of the lateral prefrontal cortex in executive behavioral control.
Tanji, J., & Hoshi, E. (2008) · Physiological Reviews · doi:10.1152/physrev.00014.2007 · Cited by 495 · see citing works
Prospective coding for objects in primate prefrontal cortex
Rainer, G., Rao, S. C., & Miller, E. K. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05493.1999 · Cited by 432 · see citing works
“(Watanabe, 1996) and actions (Quintana and Fuster, 1992; Asaad”
BackgroundRule-dependent neuronal activity in the prefrontal cortex
White, I. M., & Wise, S. P. (1999) · Experimental Brain Research · doi:10.1007/s002210050740 · Cited by 429 · see citing works
“Several recent studies have extended the pioneering work by examining the role of PF in processing information about stimuli, responses, rewards, errors, and other behaviorally significant events (Hasegawa et al. 1998; Lecas 1995; Miller et al. 1996; Rao et al. 1997; Rolls and Baylis 1994; Rolls et al. 1996a, 1996b; S…”
BackgroundThe neural system that bridges reward and cognition in humans: An fMRI study
Pochon, J.-B., Lévy, R., Fossati, P., Lehéricy, S., Poline, J.-B., Pillon, B., Bihan, D. L., & Dubois, B. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082111099 · Cited by 431 · see citing works
A neural correlate of response bias in monkey caudate nucleus
Lauwereyns, J., Watanabe, K., Coe, B. C., & Hikosaka, O. (2002) · Nature · doi:10.1038/nature00892 · Cited by 415 · see citing works
Neuronal representations of cognitive state: reward or attention?
Maunsell, J. H. R. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.04.003 · Cited by 404 · see citing works
Exposure to appetitive food stimuli markedly activates the human brain
Wang, G.-J., Volkow, N. D., Telang, F., Jayne, M., Ma, J., Rao, M., Zhu, W., Wong, C. T., Pappas, N. R., Geliebter, A., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.11.026 · Cited by 402 · see citing works
“This association is consistent with the known role of the OFC in processing expectation of food reward (Watababe, 1996).”
ResultBasal ganglia orient eyes to reward
Hikosaka, O., Nakamura, K., & Nakahara, H. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00458.2005 · Cited by 377 · see citing works
Mechanisms of motivation–cognition interaction: challenges and opportunities
Braver, T. S., Krug, M. K., Chiew, K. S., Kool, W., Westbrook, J. A., Clement, N. J., Adcock, R. A., Barch, D. M., Botvinick, M., Carver, C. S., et al. (2014) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-014-0300-0 · Cited by 400 · see citing works
“The integration of these signals reflects more than just additive contributions of cognitive demands and reward value, but actually enhances functional coding within PFC, such as by maximizing signal-to-noise ratio, enhancing discriminability of visuospatial signals, and increasing the amount of information transmitte…”
Neuronal correlates of goal-based motor selection in the prefrontal cortex.
Matsumoto, K., Suzuki, W., & Tanaka, K. (2003) · Science · doi:10.1126/science.1084204 · Cited by 384 · see citing works
Lee, H. B., Simpson, G. V., Logothetis, N. K., & Rainer, G. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.025 · Cited by 388 · see citing works
“…pation of the expected stimulus, action, or reward and structuring information flow among different brain (Asaad et al., 1998; Rainer et al., 1999; Watanabe, 1996), regions (Diesmann et al., 1999; Salinas and Sejnowwhereas activity early during the delay tends to reflect ski, 2001). retrospective…”
BackgroundAmygdala–frontal interactions and reward expectancy
Holland, P. C., & Gallagher, M. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.007 · Cited by 390 · see citing works
Lateral hypothalamic orexin/hypocretin neurons: A role in reward-seeking and addiction
Aston‐Jones, G., Smith, R. J., Sartor, G. C., Moorman, D. E., Massi, L., Tahsili‐Fahadan, P., & Richardson, K. A. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.106 · Cited by 386 · see citing works
“It receives highly processed information from several brain areas and is involved in complex cognitive and behavioral processes (Bubser and Schmidt, 1990; Granon et al., 1994; Kolb, 1984; Muir et al., 1996; Watanabe, 1996).”
Manoach, D. S., Press, D. Z., Thangaraj, V., Searl, M. M., GOFF, D. C., Halpern, E. F., Saper, C. B., & Warach, S. J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00318-7 · Cited by 384 · see citing works
“In monkeys performing spatial-delayed response tasks, DLPFC neurons involved in retaining information in WM are responsive to reward; they show more activity during delay periods when a preferred reward is anticipated than when it is not (Watanabe 1996).”
BackgroundInfluence of Reward Expectation on Behavior-Related Neuronal Activity in Primate Striatum
Hollerman, J. R., Tremblay, L., & Schultz, W. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.2.947 · Cited by 380 · see citing works
“Allrelated sustained activity in a spatial delayed response task (Watanabe 1996).”
BackgroundCell-Type-Specific Activity in Prefrontal Cortex during Goal-Directed Behavior
Pinto, L., & Dan, Y. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.021 · Cited by 323 · see citing works
Effects of Expectations for Different Reward Magnitudes on Neuronal Activity in Primate Striatum
Cromwell, H. C., & Schultz, W. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01014.2002 · Cited by 357 · see citing works
“These activations can be dependent on the reward type (Watanabe 1996) or magnitude (Leon and Shadlen 1999).”
BackgroundCultural objects modulate reward circuitry
Erk, S., Spitzer, M., Wunderlich, A. P., Galley, L., & Walter, H. (2002) · Neuroreport · doi:10.1097/00001756-200212200-00024 · Cited by 359 · see citing works
The motivation and pleasure dimension of negative symptoms: Neural substrates and behavioral outputs
Kring, A. M., & Barch, D. M. (2014) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2013.06.007 · Cited by 352 · see citing works
“…cognitive control enhancements that occur with the provision of incentives in both animals (Kobayashi et al., 2006; Krawczyk et al., 2007; Sakagami and Watanabe, 2007; Watanabe, 1996), and humans (Beck et al., 2010; Jimura et al., 2010; Savine and Braver, 2010; Tsujimoto and Sawaguchi, 2005).”
Reward Encoding in the Monkey Anterior Cingulate Cortex
Amiez, C., Joseph, J., & Procyk, E. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj046 · Cited by 351 · see citing works
“with several fixed rewards — has been already described in structures interconnected with the ACC, including prefrontal cortex (Watanabe, 1996; Leon and Shadlen, 1999; Hikosaka and Watanabe, 2000; Watanabe et al., 2002; Wallis and Miller, 2003), parietal cortex (Platt and Glimcher, 1999; Sugrue et al.”
BackgroundHikosaka, K. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.263 · Cited by 345 · see citing works
“Reward Expectancy-related Neuronal Activity in the LPFC To compare characteristics of delay activity of OFC and LPFC neurons in relation to the response outcome, we introduce here reward expectancy-related neuronal activities of the LPFC which were reported previously (Watanabe, 1996).”
BackgroundMethodResultInfluentialWorking Memory in the Prefrontal Cortex
Funahashi, S. (2017) · Brain Sciences · doi:10.3390/brainsci7050049 · Cited by 339 · see citing works
Seo, H., & Lee, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2369-07.2007 · Cited by 324 · see citing works
“Previous studies have found that the DLPFC might provide several different types of signals necessary for updating the value functions during the matching pennies task used in the present study (Barraclough et al., 2004; Seo et al., 2007).”
BackgroundInfluentialD1- Versus D2-Receptor Modulation of Visuospatial Working Memory in Humans
Müller, U., von Cramon, D. Y., & Pollmann, S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02720.1998 · Cited by 325 · see citing works
“frontal neurons (Watanabe, 1996) are preferentially activated by”
ResultRole of lateral hypothalamic orexin neurons in reward processing and addiction
Aston‐Jones, G., Smith, R. J., Moorman, D. E., & Richardson, K. A. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.060 · Cited by 330 · see citing works
“It receives highly processed information from several brain areas, and is involved in complex cognitive and behavioral processes (Bubser and Schmidt, 1990; Granon et al., 1994; Kolb, 1984; Muir et al., 1996; Watanabe, 1996).”
Reward prediction in primate basal ganglia and frontal cortex
Schultz, W., Tremblay, L., & Hollerman, J. R. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00071-9 · Cited by 318 · see citing works
Well–being and affective style: neural substrates and biobehavioural correlates
Davidson, R. J. (2004) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2004.1510 · Cited by 446 · see citing works
“More recently (Sutton & Davidson 1997) we showed that scores on a self-report measure designed to operationalize Gray’s concepts of the BIS/BAS scales (Carver & White 1994) were even more strongly predicted by electrophysiological measures of prefrontal asymmetry than were scores on the PANAS (see figure 2).”
MethodInfluential
- Authors
- Watanabe, M.
- Corresponding author
- Watanabe, Masataka
- ORCID
- Watanabe, Masataka
- Venue
- Nature
- Published
- 1996-08
- Volume
- 382
- Issue
- 6592
- Pages
- 629-632
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2025931876
- Cited by
- 684
- References
- 24
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 4 · 2023: 8 · 2022: 10 · 2021: 10 · 2020: 10 · 2019: 8 · 2018: 8 · 2017: 19 · 2016: 17 · 2015: 37 · 2014: 23 · 2013: 19 · 2012: 22
- FWCI
- 11.08
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- 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 › Neural dynamics and brain function
- Keywords
- reward expectancy, prefrontal cortex, delay activity, working memory, goal-directed behavior, reward outcome, delayed response task, primate neurophysiology
- MeSH terms
- Animals, Brain Mapping, Conditioning, Classical, Food Preferences, Macaca, Neurons, Reward, Prefrontal Cortex
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