Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque

Leon, Matthew I.; Shadlen, Michael N.

doi:10.1016/s0896-6273(00)80854-5

Cited by 412 publications

(345 citation statements)

References 49 publications

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“…Also, the expectation of rewardmodulated electrophysiological responses of striatal neurons in primates and the saccadic eye movement investigated occurred earlier and faster in the rewarded direction as opposed to nonrewarded directions (Kawagoe et al, 1998). It is likely that rewardrelated signals are transmitted to the striatum by glutamatergic projections from cortical and limbic regions (McGeorge and Faull, 1989) such as the amygdala, prefrontal, or orbitofrontal cortex, which are involved in processing of the incentive properties of stimuli Watanabe, 1996;DeCoteau et al, 1997;Gallagher et al, 1999;Leon and Shadlen, 1999;Tremblay and Schultz, 1999). Input of these structures converges in the NAc on medium-sized striatal projection neurons involving NMDA and non-NMDA receptors (Albin et al, 1992).…”

Section: Intra-nac Nmda Receptors and Reward Expectancymentioning

confidence: 99%

NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

2000

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Expectancy of future reward is an important factor guiding the speed of instrumental behavior. The present study sought to explore whether signals transmitted via the NMDA subtype of glutamate receptors and via dopamine D 2 receptors in the nucleus accumbens (NAc) are critical for the determination of reaction times (RTs) of instrumental responses by the expectancy of future reward. A simple RT task for rats demanding conditioned lever release was used in which the upcoming reward magnitude (5 or 1 pellet) was signaled in advance by discriminative stimuli. In trained rats, RTs of conditioned responses with expectancy of a high reward magnitude were found to be significantly shorter. The shortening of RTs by stimuli predictive of high reward to be obtained was dose-dependently impaired by bilateral intra-NAc infusion of the competitive NMDA antagonist DL-2-amino-5-phosphonovaleric acid (APV) (1, 2, or 10 g in 0.5 l/side), but not by infusion of the preferential dopamine D 2 antagonist haloperidol (5 and 12.5 g in 0.5 l/side) or by infusion of vehicle (0.5 l/side). In conclusion, the data reveal that in well trained animals stimulation of intra-NAc NMDA, but not of dopamine D 2 , receptors, is critically involved in guiding the speed of instrumental responses according to stimuli predictive of the upcoming reward magnitude.Key words: nucleus accumbens; goal-directed behavior; reward; dopamine; glutamate; reaction time; rat Reward expectancy is an important factor of guidance in adaptive motor behavior. Accordingly, the speed of instrumental responses has been found to be a function of the expected reward magnitude because reaction times (RTs) of rats were shortened by expectancy of signaled high reward (Brown and Bowman, 1995). Likewise, RTs of reaching movements (Hollerman et al., 1998) or saccadic eye movements (Kawagoe et al., 1998) of primates decreased as a function of the relative attractiveness of the expected reward.The nucleus accumbens (NAc) as an interface between limbic and motor structures (Groenewegen et al., 1996) may play a key role in the control of goal-directed actions by reward (Mogenson et al., 1980). It is generally assumed that the NAc subserves motivated behaviors such as feeding, sexual behavior, or exploratory locomotion elicited by primary reward and by conditioned stimuli associated with reward Everitt, 1990;Mitchell and Gratton, 1994;Watanabe, 1996). For instance, lesions of the NAc abolished conditioned place preference (Everitt et al., 1991), suggesting that environmental cues predictive for reward no longer control behavior. Furthermore, neurons in the striatum show reward expectation-related activations triggered by reward-predicting stimuli (Apicella et al., 1991;Schultz et al., 1992;Kawagoe et al., 1998). Depending on the expected type of reinforcer, behaviorrelated neuronal activity of striatal neurons is influenced differentially, implying that these neurons incorporate information about the expected behavioral outcome (Hollerman et al., 1998). Although these data suggest that ...

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Section: Intra-nac Nmda Receptors and Reward Expectancymentioning

confidence: 99%

NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

2000

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“…However, reasonable candidates include dopaminergic (DA) neurons in the ventral tegemental area (VTA) and the substantia nigra pars compacta (SNc) that might influence activity in visual cortex via direct projections to early areas of visual cortex (Berger et al 1988(Berger et al , 1991Devoto and Flore 2006). However, these projections are generally thought to be sparse, so it is likely that indirect DA signals relayed through the striatum and then to frontal and parietal cortex play an important role in regulating value-related changes in early visual cortex (Barraclough et al 2004;Ding and Hikosaka 2006;Dorris and Glimcher 2004;Gläscher et al 2009;Glimcher 2003;Hikosaka et al 2008;Hollerman and Schultz 1998;Ikeda and Hikosaka 2003;Lau and Glimcher 2007;Leon and Shadlen 1999;Luk and Wallis 2009;Platt and Glimcher 1999;Schultz and Dickinson 2000;Seo et al 2007;Sugrue et al 2004;Wallis and Miller 2003;Watanabe 1996). Indeed, many of the cortical targets of reward signals-such as oculomotor neurons in frontal and parietal cortex-are ideally situated to send modulatory feedback signals to earlier sensory areas so that the cortical representation of high-value stimulus features can be enhanced (Bisley and Goldberg 2003;Ding and Hikosaka 2006;Gold and Shadlen 2007;Serences and Yantis 2006;Shadlen and Newsome 2001).…”

Section: Value and Population Responses In Human Visual Cortexmentioning

confidence: 99%

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Serences

Saproo

2010

Journal of Neurophysiology

104

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Serences JT, Saproo S. Population response profiles in early visual cortex are biased in favor of more valuable stimuli. J Neurophysiol 104: 76 -87, 2010. First published April 21, 2010 doi:10.1152/jn.01090.2009. Voluntary and stimulus-driven shifts of attention can modulate the representation of behaviorally relevant stimuli in early areas of visual cortex. In turn, attended items are processed faster and more accurately, facilitating the selection of appropriate behavioral responses. Information processing is also strongly influenced by past experience and recent studies indicate that the learned value of a stimulus can influence relatively late stages of decision making such as the process of selecting a motor response. However, the learned value of a stimulus can also influence the magnitude of cortical responses in early sensory areas such as V1 and S1. These early effects of stimulus value are presumed to improve the quality of sensory representations; however, the nature of these modulations is not clear. They could reflect nonspecific changes in response amplitude associated with changes in general arousal or they could reflect a bias in population responses so that high-value features are represented more robustly. To examine this issue, subjects performed a two-alternative forced choice paradigm with a variableinterval payoff schedule to dynamically manipulate the relative value of two stimuli defined by their orientation (one was rotated clockwise from vertical, the other counterclockwise). Activation levels in visual cortex were monitored using functional MRI and feature-selective voxel tuning functions while subjects performed the behavioral task. The results suggest that value not only modulates the relative amplitude of responses in early areas of human visual cortex, but also sharpens the response profile across the populations of feature-selective neurons that encode the critical stimulus feature (orientation). Moreover, changes in space-or feature-based attention cannot easily explain the results because representations of both the selected and the unselected stimuli underwent a similar feature-selective modulation. This sharpening in the population response profile could theoretically improve the probability of correctly discriminating high-value stimuli from low-value alternatives.

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“…These results might be expected given that prefrontal dopamine transmission plays a general role in guiding behavior elicited by external stimuli. Both ventral tegmental area (VTA) dopaminergic and prefrontal cortical neurons are responsive to reward-predicting stimuli (Leon and Shadlen 1999;Pratt and Mizumori 2001;Roesch and Olson 2003;Tobler et al 2005;Tremblay and Schultz 1999). In addition, extracellular levels of dopamine increase in the prefrontal cortex in response to reward cues and stressors including predator odor (Bassareo et al 2002;Bassareo and Di Chiara 1997;Merali et al 2004;Morrow et al 2000).…”

Section: Conditioned Locomotor Arousalmentioning

confidence: 99%

Acute Stress and Nicotine Cues Interact to Unveil Locomotor Arousal and Activity-Dependent Gene Expression in the Prefrontal Cortex

Schiltz

Kelley

Landry

2007

Biological Psychiatry

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Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque

Cited by 412 publications

References 49 publications

NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Acute Stress and Nicotine Cues Interact to Unveil Locomotor Arousal and Activity-Dependent Gene Expression in the Prefrontal Cortex

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Effect of Expected Reward Magnitude on the Response of Neurons in the Dorsolateral Prefrontal Cortex of the Macaque

Cited by 412 publications

References 49 publications

NMDA, But Not Dopamine D2, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

NMDA, But Not Dopamine D2, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

Population Response Profiles in Early Visual Cortex Are Biased in Favor of More Valuable Stimuli

Acute Stress and Nicotine Cues Interact to Unveil Locomotor Arousal and Activity-Dependent Gene Expression in the Prefrontal Cortex

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Product

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NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude

NMDA, But Not Dopamine D₂, Receptors in the Rat Nucleus Accumbens Are Involved in Guidance of Instrumental Behavior by Stimuli Predicting Reward Magnitude