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Article ; Online: Volatility Facilitates Value Updating in the Prefrontal Cortex.

Massi, Bart / Donahue, Christopher H / Lee, Daeyeol

2018 Volume 99, Issue 3, Page(s) 598–608.e4

Abstract: Adaptation of learning and decision-making might depend on the regulation of activity in the prefrontal cortex. Here we examined how volatility of reward probabilities influences learning and neural activity in the primate prefrontal cortex. We found ... ...

Abstract	Adaptation of learning and decision-making might depend on the regulation of activity in the prefrontal cortex. Here we examined how volatility of reward probabilities influences learning and neural activity in the primate prefrontal cortex. We found that animals selected recently rewarded targets more often when reward probabilities of different options fluctuated across trials than when they were fixed. Additionally, neurons in the orbitofrontal cortex displayed more sustained activity related to the outcomes of their previous choices when reward probabilities changed over time. Such volatility also enhanced signals in the dorsolateral prefrontal cortex related to the current but not the previous location of the previously rewarded target. These results suggest that prefrontal activity related to choice and reward is dynamically regulated by the volatility of the environment and underscore the role of the prefrontal cortex in identifying aspects of the environment that are responsible for previous outcomes and should be learned.
MeSH term(s)	Animals ; Decision Making/physiology ; Learning/physiology ; Macaca mulatta ; Male ; Prefrontal Cortex/physiology ; Reward
Language	English
Publishing date	2018-07-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2018.06.033
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Article ; Online: A Direct Path to Action Initiation.

Donahue, Christopher H / Kreitzer, Anatol C

Neuron

2015 Volume 88, Issue 2, Page(s) 240–241

Abstract: In this issue of Neuron, Sippy et al. (2015) provide the clearest evidence to date that information is differentially encoded in the direct and indirect pathways of the striatum. The results support the classical notion that the direct pathway plays a ... ...

Abstract	In this issue of Neuron, Sippy et al. (2015) provide the clearest evidence to date that information is differentially encoded in the direct and indirect pathways of the striatum. The results support the classical notion that the direct pathway plays a critical role in initiating actions.
MeSH term(s)	Animals ; Corpus Striatum/cytology ; Corpus Striatum/physiology ; Goals ; Neurons/physiology ; Psychomotor Performance/physiology ; Reward
Language	English
Publishing date	2015-10-21
Publishing country	United States
Document type	Comment ; Journal Article
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2015.10.013
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Article ; Online: Dynamic routing of task-relevant signals for decision making in dorsolateral prefrontal cortex.

Donahue, Christopher H / Lee, Daeyeol

Nature neuroscience

2015 Volume 18, Issue 2, Page(s) 295–301

Abstract: Neurons in the dorsolateral prefrontal cortex (DLPFC) encode a diverse array of sensory and mnemonic signals, but little is known about how this information is dynamically routed during decision making. We analyzed the neuronal activity in the DLPFC of ... ...

Abstract	Neurons in the dorsolateral prefrontal cortex (DLPFC) encode a diverse array of sensory and mnemonic signals, but little is known about how this information is dynamically routed during decision making. We analyzed the neuronal activity in the DLPFC of monkeys performing a probabilistic reversal task where information about the probability and magnitude of reward was provided by the target color and numerical cues, respectively. The location of the target of a given color was randomized across trials and therefore was not relevant for subsequent choices. DLPFC neurons encoded signals related to both task-relevant and irrelevant features, but only task-relevant mnemonic signals were encoded congruently with choice signals. Furthermore, only the task-relevant signals related to previous events were more robustly encoded following rewarded outcomes. Thus, multiple types of neural signals are flexibly routed in the DLPFC so as to favor actions that maximize reward.
MeSH term(s)	Animals ; Behavior, Animal/physiology ; Choice Behavior/physiology ; Macaca mulatta ; Male ; Memory, Short-Term/physiology ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Probability Learning ; Psychomotor Performance/physiology ; Reward ; Visual Perception/physiology
Language	English
Publishing date	2015-01-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1420596-8
ISSN	1546-1726 ; 1097-6256
ISSN (online)	1546-1726
ISSN	1097-6256
DOI	10.1038/nn.3918
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Zs.A 4891: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Flexible combination of reward information across primates.

Farashahi, Shiva / Donahue, Christopher H / Hayden, Benjamin Y / Lee, Daeyeol / Soltani, Alireza

Nature human behaviour

2019 Volume 3, Issue 11, Page(s) 1215–1224

Abstract: A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation ...

Abstract	A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation allows flexible combination of reward information required in uncertain or changing environments. We hypothesized that the level of uncertainty in the reward environment should determine the strategy used for valuation and choice. To test this hypothesis, we examined choice between risky options in humans and rhesus macaques across three tasks with different levels of uncertainty. We found that whereas humans and monkeys adopted a multiplicative strategy under risk when probabilities are known, both species spontaneously adopted an additive strategy under uncertainty when probabilities must be learned. Additionally, the level of volatility influenced relative weighting of certain and uncertain reward information, and this was reflected in the encoding of reward magnitude by neurons in the dorsolateral prefrontal cortex.
MeSH term(s)	Adolescent ; Animals ; Choice Behavior ; Comprehension ; Decision Making ; Female ; Humans ; Macaca mulatta/psychology ; Male ; Probability ; Reward ; Risk ; Uncertainty ; Young Adult
Language	English
Publishing date	2019-09-09
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	2397-3374
ISSN (online)	2397-3374
DOI	10.1038/s41562-019-0714-3
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Article ; Online: Motor thalamus supports striatum-driven reinforcement.

Lalive, Arnaud L / Lien, Anthony D / Roseberry, Thomas K / Donahue, Christopher H / Kreitzer, Anatol C

eLife

2018 Volume 7

Abstract: Reinforcement has long been thought to require striatal synaptic plasticity. Indeed, direct striatal manipulations such as self-stimulation of direct-pathway projection neurons (dMSNs) are sufficient to induce reinforcement within minutes. However, it's ... ...

Abstract	Reinforcement has long been thought to require striatal synaptic plasticity. Indeed, direct striatal manipulations such as self-stimulation of direct-pathway projection neurons (dMSNs) are sufficient to induce reinforcement within minutes. However, it's unclear what role, if any, is played by downstream circuitry. Here, we used dMSN self-stimulation in mice as a model for striatum-driven reinforcement and mapped the underlying circuitry across multiple basal ganglia nuclei and output targets. We found that mimicking the effects of dMSN activation on downstream circuitry, through optogenetic suppression of basal ganglia output nucleus substantia nigra reticulata (SNr) or activation of SNr targets in the brainstem or thalamus, was also sufficient to drive rapid reinforcement. Remarkably, silencing motor thalamus-but not other selected targets of SNr-was the only manipulation that reduced dMSN-driven reinforcement. Together, these results point to an unexpected role for basal ganglia output to motor thalamus in striatum-driven reinforcement.
MeSH term(s)	Animals ; Basal Ganglia/physiology ; Electric Stimulation ; Female ; Glutamates/metabolism ; Male ; Mice ; Motor Activity/physiology ; Neostriatum/physiology ; Optogenetics ; Receptors, N-Methyl-D-Aspartate/metabolism ; Reinforcement, Psychology ; Serotonergic Neurons/metabolism ; Synaptic Transmission/physiology ; Thalamus/physiology
Chemical Substances	Glutamates ; Receptors, N-Methyl-D-Aspartate
Language	English
Publishing date	2018-10-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2687154-3
ISSN	2050-084X ; 2050-084X
ISSN (online)	2050-084X
ISSN	2050-084X
DOI	10.7554/eLife.34032
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Article ; Online: Cortical signals for rewarded actions and strategic exploration.

Donahue, Christopher H / Seo, Hyojung / Lee, Daeyeol

Neuron

2013 Volume 80, Issue 1, Page(s) 223–234

Abstract: In stable environments, decision makers can exploit their previously learned strategies for optimal outcomes, while exploration might lead to better options in unstable environments. Here, to investigate the cortical contributions to exploratory behavior, ...

Abstract	In stable environments, decision makers can exploit their previously learned strategies for optimal outcomes, while exploration might lead to better options in unstable environments. Here, to investigate the cortical contributions to exploratory behavior, we analyzed single-neuron activity recorded from four different cortical areas of monkeys performing a matching-pennies task and a visual search task, which encouraged and discouraged exploration, respectively. We found that neurons in multiple regions in the frontal and parietal cortex tended to encode signals related to previously rewarded actions more reliably than unrewarded actions. In addition, signals for rewarded choices in the supplementary eye field were attenuated during the visual search task and were correlated with the tendency to switch choices during the matching-pennies task. These results suggest that the supplementary eye field might play a unique role in encouraging animals to explore alternative decision-making strategies.
MeSH term(s)	Action Potentials/physiology ; Animals ; Behavior, Animal ; Choice Behavior/physiology ; Female ; Macaca mulatta ; Male ; Motor Cortex/physiology ; Neurons/physiology ; Psychomotor Performance/physiology ; Reward ; Saccades/physiology ; Visual Fields/physiology
Language	English
Publishing date	2013-09-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2013.07.040
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Zs.A 2496: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Metaplasticity as a Neural Substrate for Adaptive Learning and Choice under Uncertainty.

Farashahi, Shiva / Donahue, Christopher H / Khorsand, Peyman / Seo, Hyojung / Lee, Daeyeol / Soltani, Alireza

Neuron

2017 Volume 94, Issue 2, Page(s) 401–414.e6

Abstract: Value-based decision making often involves integration of reward outcomes over time, but this becomes considerably more challenging if reward assignments on alternative options are probabilistic and non-stationary. Despite the existence of various models ...

Abstract	Value-based decision making often involves integration of reward outcomes over time, but this becomes considerably more challenging if reward assignments on alternative options are probabilistic and non-stationary. Despite the existence of various models for optimally integrating reward under uncertainty, the underlying neural mechanisms are still unknown. Here we propose that reward-dependent metaplasticity (RDMP) can provide a plausible mechanism for both integration of reward under uncertainty and estimation of uncertainty itself. We show that a model based on RDMP can robustly perform the probabilistic reversal learning task via dynamic adjustment of learning based on reward feedback, while changes in its activity signal unexpected uncertainty. The model predicts time-dependent and choice-specific learning rates that strongly depend on reward history. Key predictions from this model were confirmed with behavioral data from non-human primates. Overall, our results suggest that metaplasticity can provide a neural substrate for adaptive learning and choice under uncertainty.
MeSH term(s)	Adaptation, Psychological/physiology ; Animals ; Behavior, Animal ; Brain/physiology ; Choice Behavior/physiology ; Macaca mulatta ; Male ; Neuronal Plasticity ; Reversal Learning/physiology ; Uncertainty
Language	English
Publishing date	2017-04-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	808167-0
ISSN	1097-4199 ; 0896-6273
ISSN (online)	1097-4199
ISSN	0896-6273
DOI	10.1016/j.neuron.2017.03.044
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Zs.A 2496: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Attaching values to actions: action and outcome encoding in the primate caudate nucleus.

Donahue, Christopher H / Seo, Hyojung

The Journal of neuroscience : the official journal of the Society for Neuroscience

2008 Volume 28, Issue 18, Page(s) 4579–4580

MeSH term(s)	Animals ; Behavior, Animal/physiology ; Caudate Nucleus/cytology ; Macaca mulatta ; Neural Pathways/physiology ; Neurons/physiology
Language	English
Publishing date	2008-04-30
Publishing country	United States
Document type	Comment ; Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	604637-x
ISSN	1529-2401 ; 0270-6474
ISSN (online)	1529-2401
ISSN	0270-6474
DOI	10.1523/JNEUROSCI.0858-08.2008
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Article ; Online: Neural correlates of strategic reasoning during competitive games.

Seo, Hyojung / Cai, Xinying / Donahue, Christopher H / Lee, Daeyeol

Science (New York, N.Y.)

2014 Volume 346, Issue 6207, Page(s) 340–343

Abstract: Although human and animal behaviors are largely shaped by reinforcement and punishment, choices in social settings are also influenced by information about the knowledge and experience of other decision-makers. During competitive games, monkeys increased ...

Abstract	Although human and animal behaviors are largely shaped by reinforcement and punishment, choices in social settings are also influenced by information about the knowledge and experience of other decision-makers. During competitive games, monkeys increased their payoffs by systematically deviating from a simple heuristic learning algorithm and thereby countering the predictable exploitation by their computer opponent. Neurons in the dorsomedial prefrontal cortex (dmPFC) signaled the animal's recent choice and reward history that reflected the computer's exploitative strategy. The strength of switching signals in the dmPFC also correlated with the animal's tendency to deviate from the heuristic learning algorithm. Therefore, the dmPFC might provide control signals for overriding simple heuristic learning algorithms based on the inferred strategies of the opponent.
MeSH term(s)	Algorithms ; Animals ; Competitive Behavior ; Decision Making ; Games, Experimental ; Learning/physiology ; Macaca mulatta ; Neurons/physiology ; Prefrontal Cortex/cytology ; Prefrontal Cortex/physiology ; Reward ; Video Games
Language	English
Publishing date	2014-09-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	128410-1
ISSN	1095-9203 ; 0036-8075
ISSN (online)	1095-9203
ISSN	0036-8075
DOI	10.1126/science.1256254
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Article ; Online: Somatosensory responses in normal aging, mild cognitive impairment, and Alzheimer's disease.

Stephen, Julia M / Montaño, Rebecca / Donahue, Christopher H / Adair, John C / Knoefel, Janice / Qualls, Clifford / Hart, Blaine / Ranken, Doug / Aine, Cheryl J

Journal of neural transmission (Vienna, Austria : 1996)

2009 Volume 117, Issue 2, Page(s) 217–225

Abstract: As a part of a larger study of normal aging and Alzheimer's disease (AD), which included patients with mild cognitive impairment (MCI), we investigated the response to median nerve stimulation in primary and secondary somatosensory areas. We hypothesized ...

Abstract	As a part of a larger study of normal aging and Alzheimer's disease (AD), which included patients with mild cognitive impairment (MCI), we investigated the response to median nerve stimulation in primary and secondary somatosensory areas. We hypothesized that the somatosensory response would be relatively spared given the reported late involvement of sensory areas in the progression of AD. We applied brief pulses of electric current to left and right median nerves to test the somatosensory response in normal elderly (NE), MCI, and AD. MEG responses were measured and were analyzed with a semi-automated source localization algorithm to characterize source locations and timecourses. We found an overall difference in the amplitude of the response of the primary somatosensory source (SI) based on diagnosis. Across the first three peaks of the SI response, the MCI patients exhibited a larger amplitude response than the NE and AD groups (P < 0.03). Additional relationships between neuropsychological measures and SI amplitude were also determined. There was no significant difference in amplitude for the contralateral secondary somatosensory source across diagnostic category. These results suggest that somatosensory cortex is affected early in the progression of AD and may have some consequence on behavioral and functional measures.
MeSH term(s)	Aged ; Aged, 80 and over ; Aging/physiology ; Algorithms ; Alzheimer Disease/physiopathology ; Automation ; Cognition Disorders/physiopathology ; Electric Stimulation ; Evoked Potentials, Somatosensory ; Female ; Humans ; Magnetoencephalography ; Male ; Median Nerve/physiopathology ; Middle Aged ; Neuropsychological Tests ; Signal Processing, Computer-Assisted ; Somatosensory Cortex/physiopathology ; Time Factors ; Touch Perception/physiology
Language	English
Publishing date	2009-12-15
Publishing country	Austria
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	184163-4
ISSN	1435-1463 ; 0300-9564
ISSN (online)	1435-1463
ISSN	0300-9564
DOI	10.1007/s00702-009-0343-5
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