Contrasting effects of reward expectation on sensory and motor memories in primate prefrontal neurons
Abstract
The value of reward obtained with successful behavior is important for guiding purposeful behavior. The lateral prefrontal cortex (LPFC) has been implicated in working memory that guides goal-directed behavior. However, mechanism that integrates the reward value into the working memory for goal-directed behavior is not understood. To help clarify this issue, we examined the effect of reward expectation on the neuronal process in the LPFC associated with memory-based sensorimotor processing. By temporally dissociating visuospatial sensory and saccade-directional motor memories in the LPFC, we here show that reward expectation significantly enhanced the directional selectivity of sensory working memory but did not affect the directional selectivity of motor memory. The enhancement of sensory working memory in the neuronal population was sustained during the delay but extinguished soon after the motor memory appeared. These results suggest that the expectation of high reward value primarily affects the sensory working memory that may be used for behavioral guidance rather than preparation for forthcoming saccades. It thus appears that the LPFC is a neuronal substrate for working memory used to guide a reward-oriented behavior, rather than reflecting an efficient control of motor action in motivated states.
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Lateral and ventromedial prefrontal cortices show reduced activation with extended training.
“For example, lateral and ventromedial prefrontal cortices, which both encode the value of expected outcomes [67–68, 37] do show reduced activation with extended training [69–70].”
From Cortical and basal ganglia contributions to habit learning and automaticity (2010) · cites this paper as [69]
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Cites
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
Cellular basis of working memory
Goldman-Rakic, P. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90304-6 · Cited by 2,663 · see citing works
Emotion, cognition, and behavior
Dolan, R. J. (2002) · Science · doi:10.1126/science.1076358 · Cited by 1,979 · 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
The functional neuroanatomy of emotion and affective style
Davidson, R. J., & Irwin, W. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(98)01265-0 · Cited by 1,684 · see citing works
Goal-directed instrumental action: contingency and incentive learning and their cortical substrates
Balleine, B. W., & Dickinson, A. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00033-1 · Cited by 1,541 · see citing works
Primary and secondary saccades to goals defined by instructions
Hallett, P. E. (1978) · Vision Research · doi:10.1016/0042-6989(78)90218-3 · Cited by 1,262 · see citing works
Fuster, J. M. (1973) · Journal of Neurophysiology · doi:10.1152/jn.1973.36.1.61 · Cited by 995 · see citing works
Motivational control of goal-directed action
Dickinson, A., & Balleine, B. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199951 · Cited by 995 · see citing works
Neural Economics and the Biological Substrates of Valuation
Montague, P. R., & Berns, G. S. (2002) · Neuron · doi:10.1016/s0896-6273(02)00974-1 · Cited by 994 · see citing works
Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque
Kim, J.-N., & Shadlen, M. N. (1999) · Nature Neuroscience · doi:10.1038/5739 · Cited by 950 · see citing works
Bruce, C. J., Goldberg, M. E., Bushnell, M. C., & Stanton, G. B. (1985) · Journal of Neurophysiology · doi:10.1152/jn.1985.54.3.714 · Cited by 926 · see citing works
Intelligence and the Frontal Lobe: The Organization of Goal-Directed Behavior
Duncan, J., Emslie, H., Williams, P., Johnson, R., & Freer, C. (1996) · Cognitive Psychology · doi:10.1006/cogp.1996.0008 · Cited by 902 · see citing works
Two routes to emotional memory: Distinct neural processes for valence and arousal
Kensinger, E. A., & Corkin, S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0306408101 · Cited by 848 · cited 3× · see citing works
“Recent human imaging studies show that the LPFC appears to be an important region for integrating motivation with cognitive operations such as working memory (Gray et al., 2002; Perlstein et al., 2002; Pochon et al., 2002; Kensinger and Corkin, 2004).”
BackgroundDecision-making processes following damage to the prefrontal cortex
Manes, F., Sahakian, B., Clark, L., Rogers, R., Antoun, N., Aitken, M., & Robbins, T. (2002) · Brain · doi:10.1093/brain/awf049 · Cited by 799 · see citing works
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
Reward expectancy in primate prefrental neurons
Watanabe, M. (1996) · Nature · doi:10.1038/382629a0 · Cited by 684 · cited 4× · see citing works
“The directional activities of a subset of LPFC neurons are modulated by the amount of reward expected at the end of the trials (Watanabe, 1996; Leon and Shadlen, 1999; Kobayashi et al., 2002).”
BackgroundInfluentialPrefrontal neuronal activity in rhesus monkeys performing a delayed anti-saccade task
Funahashi, S., Chafee, M. V., & Goldman, P. S. (1993) · Nature · doi:10.1038/365753a0 · Cited by 662 · see citing works
The antisaccade: a review of basic research and clinical studies
Everling, S., & Fischer, B. (1998) · Neuropsychologia · doi:10.1016/s0028-3932(98)00020-7 · Cited by 600 · 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
Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex
Roesch, M. R., & Olson, C. R. (2004) · Science · doi:10.1126/science.1093223 · Cited by 535 · see citing works
Leon, M. I., & Shadlen, M. N. (1999) · Neuron · doi:10.1016/s0896-6273(00)80854-5 · Cited by 449 · see citing works
The 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
From Perception to Action: Temporal Integrative Functions of Prefrontal and Parietal Neurons
Quintana, J. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.3.213 · Cited by 369 · see citing works
Roesch, M. R., & Olson, C. R. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00019.2003 · Cited by 309 · see citing works
T HE N EUROBIOLOGY OF V ISUAL -S ACCADIC D ECISION M AKING
Glimcher, P. W. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.010302.081134 · Cited by 291 · see citing works
The Neurobiology of Motivation and Reward
Stellar, J. R., & Stellar, E. (1985) · Springer eBooks · doi:10.1007/978-1-4615-8032-4 · Cited by 252 · see citing works
Neuronal switching of sensorimotor transformations for antisaccades
Zhang, M., & Barash, S. (2000) · Nature · doi:10.1038/35050097 · Cited by 247 · see citing works
Dissociation in human prefrontal cortex of affective influences on working memory-related activity
Perlstein, W. M., Elbert, T. R., & Stenger, V. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.241650598 · Cited by 246 · see citing works
Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task
Gottlieb, J. P., & Goldberg, M. E. (1999) · Nature Neuroscience · doi:10.1038/13209 · Cited by 245 · see citing works
15th annual meeting of the society for neuroscience
(1985) · Peptides · doi:10.1016/0196-9781(85)90125-1 · Cited by 240 · see citing works
The sensory nature of mnemonic representation in the primate prefrontal cortex
Constantinidis, C., Franowicz, M. N., & Goldman-Rakic, P. S. (2001) · Nature Neuroscience · doi:10.1038/85179 · Cited by 233 · see citing works
Behavioral planning in the prefrontal cortex
Tanji, J., & Hoshi, E. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00192-6 · Cited by 224 · see citing works
Influence of Reward Expectation on Visuospatial Processing in Macaque Lateral Prefrontal Cortex
Kobayashi, S., Lauwereyns, J., Koizumi, M., Sakagami, M., & Hikosaka, O. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00472.2001 · Cited by 206 · see citing works
Hoshi, E., Shima, K., & Tanji, J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.2355 · Cited by 204 · see citing works
Takeda, K., & Funahashi, S. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00249.2001 · Cited by 201 · see citing works
Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex
Watanabe, M., Hikosaka, K., Sakagami, M., & Shirakawa, S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-06-02391.2002 · Cited by 159 · see citing works
The role of the medial prefrontal cortex in achieving goals
Matsumoto, K., & Tanaka, K. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.005 · Cited by 123 · see citing works
Persistent LIP Activity in Memory Antisaccades: Working Memory For a Sensorimotor Transformation
Zhang, M., & Barash, S. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00504.2003 · Cited by 104 · see citing works
Sawaguchi, T., & Yamane, I. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.5.2070 · Cited by 90 · see citing works
Hasegawa, R., Sawaguchi, T., & Kubota, K. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.1.322 · Cited by 87 · see citing works
Population Vector Analysis of Primate Prefrontal Activity during Spatial Working Memory
Takeda, K. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh093 · Cited by 78 · see citing works
Neuronal Representation of Response-Outcome in the Primate Prefrontal Cortex
Tsujimoto, S. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg090 · Cited by 54 · see citing works
Accuracy of visually and memory-guided antisaccades in man
Krappmann, P. (1998) · Vision Research · doi:10.1016/s0042-6989(98)00101-1 · Cited by 51 · see citing works
34th Annual Meeting of Society for Neuroscience
Calzavara, R., Mailly, P., Bennett, S. R., Kim, K. J., Yung, Y. W., & Haber, S. N. (2004) · HAL · Cited by 40 · see citing works
Cognitive and Motivational Operations in Primate Prefrontal Neurons
Watanabe, M. (1998) · Reviews in the Neurosciences · doi:10.1515/revneuro.1998.9.4.225 · Cited by 38 · see citing works
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- Authors
- Amemori, K.-I., & Sawaguchi, T.
- Affiliations
- Hokkaido University (JP)
- Corresponding author
- Amemori, Ken-ichi
- ORCID
- Amemori, Ken-ichi
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2005-10-12
- Volume
- 16
- Issue
- 7
- Pages
- 1002-1015
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2152080080
- Cited by
- 39
- References
- 47
- Citations by year
- 2024: 1 · 2023: 2 · 2022: 1 · 2017: 2 · 2016: 1 · 2015: 3 · 2014: 2 · 2012: 3
- FWCI
- 2.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- reward anticipation, lateral prefrontal cortex, working memory, motor memory, saccade direction, direction selectivity, goal-directed behavior, visuospatial memory
- MeSH terms
- Animals, Cues, Evoked Potentials, Visual, Eye Movements, Female, Fixation, Ocular, Macaca, Male, Memory, Short-Term, Motion Perception, Motivation, Neurons, Reward, Space Perception, Task Performance and Analysis, Prefrontal Cortex
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