Contrasting Roles for Orbitofrontal Cortex and Amygdala in Credit Assignment and Learning in Macaques

Chau, Bolton K.H.; Sallet, Jérôme; Παπαγεωργίου, Γεώργιος Κ.; Noonan, MaryAnn P.; Bell, Andrew; Walton, Mark E.; Rushworth, Matthew F. S.

doi:10.1016/j.neuron.2015.08.018

Cited by 154 publications

(170 citation statements)

References 53 publications

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“…Consistent with this evidence for humans, functional neuroimaging in macaques reveals that the macaque lateral orbitofrontal cortex is activated by non-reward during a reversal task (Chau et al, 2015) (Fig. 2c).…”

Section: Neuroimaging Evidence For a Non-reward System In The Lateralsupporting

confidence: 76%

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A non-reward attractor theory of depression

Rolls

2016

Neuroscience & Biobehavioral Reviews

159

174

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Neuroscience and Biobehavioral Reviews, in press (May 2016) \papers\Emotion\depression\depression16b.docx 2 SummaryA non-reward attractor theory of depression is proposed based on the operation of the lateral orbitofrontal cortex and supracallosal cingulate cortex. The orbitofrontal cortex contains error neurons that respond to non-reward for many seconds in an attractor state that maintains a memory of the nonreward. The human lateral orbitofrontal cortex is activated by non-reward during reward reversal, and by a signal to stop a response that is now incorrect. Damage to the human orbitofrontal cortex impairs reward reversal learning. Not receiving reward can produce depression. The theory proposed is that in depression, this lateral orbitofrontal cortex non-reward system is more easily triggered, and maintains its attractor-related firing for longer. This triggers negative cognitive states, which in turn have positive feedback top-down effects on the orbitofrontal cortex non-reward system. Treatments for depression, including ketamine, may act in part by quashing this attractor. The mania of bipolar disorder is hypothesized to be associated with oversensitivity and overactivity in the reciprocally related reward system in the medial orbitofrontal cortex and pregenual cingulate cortex.

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Section: Neuroimaging Evidence For a Non-reward System In The Lateralsupporting

confidence: 76%

“…This neuron-level evidence is strongly supported by functional neuroimaging evidence, which indicates that the macaque lateral orbitofrontal cortex is activated by non-reward during a reversal task, and that the focus of the activation is the lateral orbitofrontal cortex (Chau et al, 2015).…”

Section: Neurophysiological Evidence For a Non-reward System In The Omentioning

confidence: 58%

A non-reward attractor theory of depression

Rolls

2016

Neuroscience & Biobehavioral Reviews

159

174

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“…For example, previous work has implicated other areas of the PFC as well as the parietal cortex. Specifically, the fMRI BOLD signal in the lateral orbitofrontal cortex of monkeys was observed to correlate with win-stay/lose-shift (contrasted with win-shift/lose-stay) behavior, reflecting successful choices that depended upon proper credit assignment (Chau et al, 2015), and lesions of the lateral orbitofrontal cortex led to a "spread of effect" (Ogden, 1933), whereby credit was misattributed to preceding events (Noonan et al, 2010). In humans, BOLD signals correlated with attribution of credit to attended versus nonattended cues were observed in the medial and orbitofrontal cortices (Akaishi et al, 2016); our study did not directly assess potential differences in the assignment of credit to attended versus nonattended options because there was no direct measure of the locus of attention, and these animals generally learned much more from positive than from negative feedback in this task (Asaad and Eskandar, 2011), limiting our ability to examine substrates of counterfactual reasoning.…”

Section: Discussionmentioning

confidence: 99%

Prefrontal Neurons Encode a Solution to the Credit-Assignment Problem

et al. 2017

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To adapt successfully to our environments, we must use the outcomes of our choices to guide future behavior. Critically, we must be able to correctly assign credit for any particular outcome to the causal features which preceded it. In some cases, the causal features may be immediately evident, whereas in others they may be separated in time or intermingled with irrelevant environmental stimuli, creating a potentially nontrivial credit-assignment problem. We examined the neuronal representation of information relevant for credit assignment in the dorsolateral prefrontal cortex (dlPFC) of two male rhesus macaques performing a task that elicited key aspects of this problem. We found that neurons conveyed the information necessary for credit assignment. Specifically, neuronal activity reflected both the relevant cues and outcomes at the time of feedback and did so in a manner that was stable over time, in contrast to prior reports of representational instability in the dlPFC. Furthermore, these representations were most stable early in learning, when credit assignment was most needed. When the same features were not needed for credit assignment, these neuronal representations were much weaker or absent. These results demonstrate that the activity of dlPFC neurons conforms to the basic requirements of a system that performs credit assignment, and that spiking activity can serve as a stable mechanism that links causes and effects.

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“…Moreover, the study reveals that the human orbitofrontal cortex is very sensitive to social feedback when it must be used to change behaviour . Correspondingly, it has now been shown in macaques using fMRI that the lateral orbitofrontal cortex is activated by non-reward during reversal (Chau, Sallet, Papageorgiou, Noonan, Bell, Walton and Rushworth 2015).…”

Section: Accepted Manuscriptmentioning

confidence: 92%

Non-reward neural mechanisms in the orbitofrontal cortex

Rolls

Deco

2016

Cortex

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Single neurons in the primate orbitofrontal cortex respond when an expected reward is not obtained, and behavior must change. The human lateral orbitofrontal cortex is activated when non-reward, or loss occurs. The neuronal computation of this negative reward prediction error is fundamental for the emotional changes associated with non-reward, and with changing behavior. Little is known about the neuronal mechanism. Here we propose a mechanism, which we formalize into a neuronal network model, which is simulated to enable the operation of the mechanism to be investigated. A single attractor network has a Reward population (or pool) of neurons that is activated by Expected Reward, and maintain their firing until, after a time, synaptic depression reduces the firing rate in this neuronal population. If a Reward Outcome is not received, the decreasing firing in the Reward neurons releases the inhibition implemented by inhibitory neurons, and this results in a second population of Non-Reward neurons to start and continue firing encouraged by the spiking-related noise in the network. If a Reward Outcome is received, this keeps the Reward attractor active, and this through the inhibitory neurons prevents the Non-Reward attractor neurons from being activated. If an Expected Reward has been signalled, and the Reward Attractor neurons are active, their firing can be directly inhibited by a Non-Reward Outcome, and the Non-Reward neurons become activated because the inhibition on them is released. The neuronal mechanism in the orbitofrontal cortex for computing negative reward prediction error are important, for this system may be over-reactive in depression, under-reactive in impulsive behavior, and may influence the dopaminergic 'prediction error' neurons.

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Contrasting Roles for Orbitofrontal Cortex and Amygdala in Credit Assignment and Learning in Macaques

Cited by 154 publications

References 53 publications

A non-reward attractor theory of depression

A non-reward attractor theory of depression

Prefrontal Neurons Encode a Solution to the Credit-Assignment Problem

Non-reward neural mechanisms in the orbitofrontal cortex

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