Single-Cell and Population Coding of Expected Reward Probability in the Orbitofrontal Cortex of the Rat

Duuren, Esther van; Plasse, G; Lankelma, J.; Joosten, R; Feenstra, M. G. P.; Pennartz, Cyriel M. A.

doi:10.1523/jneurosci.0005-09.2009

Cited by 76 publications

(68 citation statements)

References 49 publications

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“…However, OFC cells are known to exhibit a wide range of firing-rate modulations in relation to task events, and a subset of OFC cells shows firing-rate sensitivity to actual and predicted reward ( Schoenbaum et al, 1998;Wallis and Miller, 2003;PadoaSchioppa and Assad, 2006;van Duuren et al, 2008van Duuren et al, , 2009). Because strong theta-band phase locking during the waiting period becomes a reliable predictor of reward with learning, we predict that this property is predominantly expressed by those cells that show outcome selectivity in their firing rates.…”

Section: Phase Locking By Neuronal Groups With Different Task-relatedmentioning

confidence: 99%

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

Wingerden¹,

Vinck²,

Lankelma³

et al. 2010

J. Neurosci.

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The expectancy of a rewarding outcome following actions and cues is coded by a network of brain structures including the orbitofrontal cortex. Thus far, predicted reward was considered to be coded by time-averaged spike rates of neurons. However, besides firing rate, the precise timing of action potentials in relation to ongoing oscillations in local field potentials is thought to be of importance for effective communication between brain areas.We performed multineuron and field potential recordings in orbitofrontal cortex of rats performing olfactory discrimination learning to study the temporal structure of coding predictive of outcome. After associative learning, field potentials were marked by theta oscillations, both in advance and during delivery of reward. Orbitofrontal neurons, especially those coding information about upcoming reward with their firing rate, phase locked to these oscillations in anticipation of reward. When established associations were reversed, phase locking collapsed in the anticipatory task phase, but returned when reward became predictable again after relearning. Behaviorally, the outcome anticipation phase was marked by licking responses, but the frequency of lick responses was dissociated from the strength of theta-band phase locking. The strength of theta-band phase locking by orbitofrontal neurons robustly follows the dynamics of associative learning as measured by behavior and correlates with the rat's current outcome expectancy. Theta-band phase locking may facilitate communication of outcome-related information between reward-related brain areas and offers a novel mechanism for coding value signals during reinforcement learning.

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Section: Phase Locking By Neuronal Groups With Different Task-relatedmentioning

confidence: 99%

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

Wingerden¹,

Vinck²,

Lankelma³

et al. 2010

J. Neurosci.

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“…This suggests that gamma-band synchronization does in general not signal odor identity or outcome-specific information associated with the olfactory input but is involved in a process that is similarly triggered by sampling of the SϪ odor and the Sϩ odor. Different subgroups of cells phase-lock to gamma and theta oscillations in different behavioral periods OFC cells are known to exhibit a wide range of firing-rate modulations in relation to task events, such as odor presentation or reward delivery (Schoenbaum et al, 1998;Wallis and Miller, 2003;PadoaSchioppa and Assad, 2006;van Duuren et al, 2008van Duuren et al, , 2009. Given the presence of gamma-band synchronization in odor processing stages in primary olfactory cortices, we expected that OFC cells responding with changes in firing rates to odor cues (i.e., showing odor selectivity) would show enhanced gamma-band phase-locking compared with other cell groups.…”

Section: Power Of Gamma-band Oscillations Is Learning Dependent But Nmentioning

confidence: 99%

“…We propose that OFC gamma-band synchronization during odor sampling reflects inhibitory control over M-cells, whose firing activity represents action values after a decision has been made (van Duuren et al, 2008(van Duuren et al, , 2009). This increased inhibitory control occurs when the rat has to withhold its behavioral response.…”

Section: Functional Implications Of Orbitofrontal Gamma-band Synchronmentioning

confidence: 99%

“…Thus, we investigated gamma oscillatory activity in the rat orbitofrontal cortex (OFC), a prefrontal structure implicated in making behavioral adjustments to changing reward contingencies and control over prepotent, impulsive responses to incentive stimuli (Jones and Mishkin, 1972;Winstanley et al, 2004) (but see Chudasama et al, 2007;Man et al, 2009). OFC neurons have been shown to flexibly encode representations of stimulus-outcome and action-outcome associations (Schoenbaum et al, 1998;Tremblay and Schultz, 1999;Wallis and Miller, 2003;Padoa-Schioppa and Assad, 2006;van Duuren et al, 2008van Duuren et al, , 2009. Although gamma oscillatory activity has been reported previously for human, monkey, and rat OFC (Nishida et al, 2004;Liu et al, 2005;Sun et al, 2006), the question arises whether gamma oscillations exert similar functions in emotional decision-making and valuation as suggested by studies on sensory processing.…”

Section: Introductionmentioning

confidence: 96%

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Learning-Associated Gamma-Band Phase-Locking of Action–Outcome Selective Neurons in Orbitofrontal Cortex

Wingerden¹,

Vinck²,

Lankelma³

et al. 2010

J. Neurosci.

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Gamma oscillations (30 -100 Hz) correlate to a variety of neural functions, including sensory processing, attention, and action selection. However, they have barely been studied in relation to emotional processing and valuation of sensory signals and actions. We conducted multineuron and local field potential recordings in the orbitofrontal cortex (OFC) of rats performing a task in which they made go or no-go decisions based on two olfactory stimuli predicting appetitive or aversive outcomes.Gamma power was strongest during the late phase of odor sampling, just before go/no-go movement, and increased with behavioral learning. Learning speed was correlated to the slope of the gamma power increment. Spikes of OFC neurons were consistently timed to the gamma rhythm during odor sampling, regardless of the associated outcome. However, only a specific subgroup of cells showed consistent phase timing. These cells showed action-outcome selective activity, not during stimulus sampling but during subsequent movement responses. During sampling, this subgroup displayed a suppression in firing rate but a concurrent increment in the consistency of spike timing relative to gamma oscillations.In addition to gamma rhythm, OFC field potentials were characterized by theta oscillations during odor sampling. Neurons phaselocked to either theta or gamma rhythms but not to both, suggesting that they become associated with separate rhythmic networks involving OFC. Altogether, these results suggest that OFC gamma-band synchronization reflects inhibitory control over a subpopulation of neurons that express information about the emotional valence of actions after a motor decision, which suggests a novel mechanism for response inhibition.

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“…Experiments in human and animal subjects have identified candidate brain areas for performing these different computations [1][2][3][4][5], including the orbitofrontal cortex (OFC) and ventral striatum (vStr) [6][7][8][9][10][11][12][13][14][15].…”

Section: Introductionmentioning

confidence: 99%

A functional difference in information processing between orbitofrontal cortex and ventral striatum during decision-making behaviour

Stott¹,

Redish

2014

Phil. Trans. R. Soc. B

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Both orbitofrontal cortex (OFC) and ventral striatum (vStr) have been identified as key structures that represent information about value in decision-making tasks. However, the dynamics of how this information is processed are not yet understood. We recorded ensembles of cells from OFC and vStr in rats engaged in the spatial adjusting delay-discounting task , a decision-making task that involves a trade-off between delay to and magnitude of reward. Ventral striatal neural activity signalled information about reward before the rat's decision, whereas such reward-related signals were absent in OFC until after the animal had committed to its decision. These data support models in which vStr is directly involved in action selection, but OFC processes decision-related information afterwards that can be used to compare the predicted and actual consequences of behaviour.

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Single-Cell and Population Coding of Expected Reward Probability in the Orbitofrontal Cortex of the Rat

Cited by 76 publications

References 49 publications

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

Learning-Associated Gamma-Band Phase-Locking of Action–Outcome Selective Neurons in Orbitofrontal Cortex

A functional difference in information processing between orbitofrontal cortex and ventral striatum during decision-making behaviour

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