Prospective Coding of Dorsal Raphe Reward Signals by the Orbitofrontal Cortex

Zhou, Jingfeng; Jia, Chunying; Feng, Qiru; Bao, Junhong; Luo, Minmin

doi:10.1523/jneurosci.4017-14.2015

Cited by 42 publications

(36 citation statements)

References 79 publications

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“…Functional interactions between the OFC and the ventral tegmental area (VTA), ventral striatum, dorsal raphe nucleus, and the basolateral nucleus of the amygdala (BLA) could provide mechanisms that link stable reward to OFC and support predictive coding. VTA error prediction signals depend on OFC (Takahashi et al, 2011), optogenetic excitation of the dorsal raphe increases prospective coding in the OFC (Zhou et al, 2015), and striatal serotonergic manipulations reverse compulsivity caused by OFC damage (Schilman et al, 2010). OFC and BLA interactions are especially relevant to reward associations, the effects of OFC lesions on learning, and the present results linking contingencies to predictive coding.…”

Section: Ofc Dynamicsmentioning

confidence: 99%

Orbitofrontal Cortex Signals Expected Outcomes with Predictive Codes When Stable Contingencies Promote the Integration of Reward History

Riceberg

Shapiro

2017

J. Neurosci.

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Memory can inform goal-directed behavior by linking current opportunities to past outcomes. The orbitofrontal cortex (OFC) may guide value-based responses by integrating the history of stimulus-reward associations into expected outcomes, representations of predicted hedonic value and quality. Alternatively, the OFC may rapidly compute flexible "online" reward predictions by associating stimuli with the latest outcome. OFC neurons develop predictive codes when rats learn to associate arbitrary stimuli with outcomes, but the extent to which predictive coding depends on most recent events and the integrated history of rewards is unclear. To investigate how reward history modulates OFC activity, we recorded OFC ensembles as rats performed spatial discriminations that differed only in the number of rewarded trials between goal reversals. The firing rate of single OFC neurons distinguished identical behaviors guided by different goals. When Ͼ20 rewarded trials separated goal switches, OFC ensembles developed stable and anticorrelated population vectors that predicted overall choice accuracy and the goal selected in single trials. When Ͻ10 rewarded trials separated goal switches, OFC population vectors decorrelated rapidly after each switch, but did not develop anticorrelated firing patterns or predict choice accuracy. The results show that, whereas OFC signals respond rapidly to contingency changes, they predict choices only when reward history is relatively stable, suggesting that consecutive rewarded episodes are needed for OFC computations that integrate reward history into expected outcomes.

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Section: Ofc Dynamicsmentioning

confidence: 99%

Orbitofrontal Cortex Signals Expected Outcomes with Predictive Codes When Stable Contingencies Promote the Integration of Reward History

Riceberg

Shapiro

2017

J. Neurosci.

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“…DRN neurons also respond to broad range of motor and reward-related events (Ranade and Mainen, 2009;Liu et al, 2014;Cohen et al, 2015;Zhou et al, 2015), and longer-term 5-HT effects are also to be expected. These will place sensory processing in the olfactory system under the control of higher-order behavioral states and conditions.…”

Section: Endogenous Control Of Drn Activitymentioning

confidence: 99%

Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex

2016

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Serotonin (5-hydroxytriptamine; 5-HT) is implicated in a variety of brain functions including not only the regulation of mood and control of behavior but also the modulation of perception. 5-HT neurons in the dorsal raphe nucleus (DRN) often fire locked to sensory stimuli, but little is known about how 5-HT affects sensory processing, especially on this timescale. Here, we used an optogenetic approach to study the effect of 5-HT on single-unit activity in the mouse primary olfactory (anterior piriform) cortex. We show that activation of DRN 5-HT neurons rapidly inhibits the spontaneous firing of olfactory cortical neurons, acting in a divisive manner, but entirely spares sensory-driven firing. These results identify a new role for serotonergic modulation in dynamically regulating the balance between different sources of neural activity in sensory systems, suggesting a possible role for 5-HT in perceptual inference.

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“…Brief stimulations (2 -3 sec) support light self-administration, shift sucrose preference, guide olfactory discrimination learning, and rapidly shape the firing pattern of cortical neurons in a closed-loop brain -machine interface (Liu et al 2014). Moreover, activation of DRN Pet-1 neurons, resembling the natural reward of sucrose, directs the formation of the prospective activation patterns in the orbitofrontal cortex (Zhou et al 2015). Pet-1 neurons release both 5-HT and glutamate in the VTA and NAc and the glutamate release requires VGluT3 (Liu et al 2014).…”

Section: Optogenetics Reveal Two Different Roles Of Drn Neurons In Rementioning

confidence: 99%

Reward processing by the dorsal raphe nucleus: 5-HT and beyond

2015

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The dorsal raphe nucleus (DRN) represents one of the most sensitive reward sites in the brain. However, the exact relationship between DRN neuronal activity and reward signaling has been elusive. In this review, we will summarize anatomical, pharmacological, optogenetics, and electrophysiological studies on the functions and circuit mechanisms of DRN neurons in reward processing. The DRN is commonly associated with serotonin (5-hydroxytryptamine; 5-HT), but this nucleus also contains neurons of the neurotransmitter phenotypes of glutamate, GABA and dopamine. Pharmacological studies indicate that 5-HT might be involved in modulating reward-or punishment-related behaviors. Recent optogenetic stimulations demonstrate that transient activation of DRN neurons produces strong reinforcement signals that are carried out primarily by glutamate. Moreover, activation of DRN 5-HT neurons enhances reward waiting. Electrophysiological recordings reveal that the activity of DRN neurons exhibits diverse behavioral correlates in reward-related tasks. Studies so far thus demonstrate the strong power of DRN neurons in reward signaling and at the same time invite additional efforts to dissect the roles and mechanisms of different DRN neuron types in various processes of reward-related behaviors.

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Prospective Coding of Dorsal Raphe Reward Signals by the Orbitofrontal Cortex

Cited by 42 publications

References 79 publications

Orbitofrontal Cortex Signals Expected Outcomes with Predictive Codes When Stable Contingencies Promote the Integration of Reward History

Orbitofrontal Cortex Signals Expected Outcomes with Predictive Codes When Stable Contingencies Promote the Integration of Reward History

Optogenetic Activation of Dorsal Raphe Serotonin Neurons Rapidly Inhibits Spontaneous But Not Odor-Evoked Activity in Olfactory Cortex

Reward processing by the dorsal raphe nucleus: 5-HT and beyond

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