Chemogenetic Modulation and Single-Photon Calcium Imaging in Anterior Cingulate Cortex Reveal a Mechanism for Effort-Based Decisions

Hart, Evan E.; Blair, Garrett J.; O’Dell, Thomas J.; Blair, Hugh T.; Izquierdo, Alicia

doi:10.1523/jneurosci.2548-19.2020

Cited by 57 publications

(61 citation statements)

References 83 publications

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“…Numerous studies have shown that the Cg1/ACC and M2 (or supplementary motor area in primate) respond to the relative value of behaviors, with firing rates or BOLD responses corresponding to high value options (Croxson et al 2009; Kennerley et al 2009; Kennerley and Wallis, 2009; Sul et al 2011; Hillman and Bilkey, 2010, 2012; Cowen et al 2012; Porter et al 2019; Hart et al 2020). However, in most previous studies subjects had to choose between, or are at least were presented with, multiple stimuli or options in a given task; quitting not being one of the options (though see Zhao et al 2016).…”

Section: Discussionmentioning

confidence: 99%

“…However, in most previous studies subjects had to choose between, or are at least were presented with, multiple stimuli or options in a given task; quitting not being one of the options (though see Zhao et al 2016). Furthermore, there has generally been an emphasis on the evaluation of the relative value of behaviors in the context of all possible behaviors (Hillman and Bilkey, 2010, 2012; Wallis and Kennerley, 2011; Hart et al 2020) even if there is no overt choice between multiple options (Cowen et al 2012; Porter et al 2019). For example, Hart et al (2020) demonstrated that Cg1 neurons have higher activity when rats are carrying out a sucrose-rewarded progressive lever pressing task with no other option available, compared to when standard rat-chow was concurrently available.…”

Section: Discussionmentioning

confidence: 99%

“…Wang et al (2017) provided some clarity on this discrepancy by showing that muscimol-inactivation of the rat Cg1 impairs performance in a novel “do more get more” task, suggesting that the Cg1 is critical for self-paced effort expenditure. Furthermore, Hart et al (2020) demonstrated that chemogenetic manipulation of the ACC resulted in rats putting less effort into a progressive ratio task only when alternative rat-chow was available. Thus, in the context of quitting behaviors, the ACC/Cg1 may provide a value signal of the current effortful behavior relative to the other available behaviors in a task environment and this value signal influences the decision to persist at the current behavior or quit (Hillman and Bilkey, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Individual Cg1 neurons are known to respond to physical effort costs and reward amounts associated with different actions and their outcomes (Kennerley et al 2009; Hayden and Platt, 2010; Cowen et al 2012; Hillman and Bilkey, 2012; Hosokawa et al 2013; Porter et al 2019). As a whole, the ACC is thought to form a cognitive map of the “task space” that is used to drive decision-making towards actions that carry high relative utility (Kurniawan et al 2013; Haber and Behrens, 2014; Heilbronner and Hayden, 2016; Azab and Hayden, 2017; Mashhoori et al 2018; Hart et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Dorsomedial prefrontal neural ensembles reflect changes in task utility that culminate in task quitting

Porter

2020

Preprint

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When performing a physically demanding behavior, sometimes the optimal choice is to quit the behavior rather than persist and waste time and energy. The dorsomedial prefrontal cortex (dmPFC), consisting of the anterior cingulate cortex and secondary motor area, likely contributes towards such utility assessments. Here, we examined how rodent dmPFC single unit and ensemble level activity corresponded to changes in motivation and quitting in an effortful weight lifting task. Rats carried out two task paradigms: one that became progressively more physically demanding over time and a second fixed effort version. Rats could quit the task at any time. Dorsomedial PFC neurons were highly responsive to each behavioral stage of the task, consisting of rope pulling, reward retrieval, and reward area leaving. Activity was highest early in sessions, commensurate with the highest relative task utility, then decreased until the point of quitting. Neural ensembles showed stable task representations across the entirety of sessions. However, these representations drifted and became more distinct over the course of the session. These results suggest that dmPFC neurons represent behavioral states that are dynamically modified as behaviors lose their utility, culminating in task quitting.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Dorsomedial prefrontal neural ensembles reflect changes in task utility that culminate in task quitting

Porter

2020

Preprint

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“…It has been argued that mPFC is important for evaluating actions and outcomes along multiple dimensions (Skvortsova et al, 2014). The anterior cingulate area of mPFC has been implicated in discriminating the utility of different reward options in effort-based decision-making (Walton et al, 2006;Hart et al, 2020). Consistent with this view the prelimbic area of mPFC has been implicated in the ability to detect actionoutcome contingencies (Balleine and O'Doherty, 2010;Balleine, 2019).…”

Section: Effects Of Mpfc Lesions On Instrumental Behaviormentioning

confidence: 93%

Central Thalamic-Medial Prefrontal Control of Adaptive Responding in the Rat: Many Players in the Chamber

Mair

Francoeur

Gibson

2021

Front. Behav. Neurosci.

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The medial prefrontal cortex (mPFC) has robust afferent and efferent connections with multiple nuclei clustered in the central thalamus. These nuclei are elements in large-scale networks linking mPFC with the hippocampus, basal ganglia, amygdala, other cortical areas, and visceral and arousal systems in the brainstem that give rise to adaptive goal-directed behavior. Lesions of the mediodorsal nucleus (MD), the main source of thalamic input to middle layers of PFC, have limited effects on delayed conditional discriminations, like DMTP and DNMTP, that depend on mPFC. Recent evidence suggests that MD sustains and amplifies neuronal responses in mPFC that represent salient task-related information and is important for detecting and encoding contingencies between actions and their consequences. Lesions of rostral intralaminar (rIL) and ventromedial (VM) nuclei produce delay-independent impairments of egocentric DMTP and DNMTP that resemble effects of mPFC lesions on response speed and accuracy: results consistent with projections of rIL to striatum and VM to motor cortices. The ventral midline and anterior thalamic nuclei affect allocentric spatial cognition and memory consistent with their connections to mPFC and hippocampus. The dorsal midline nuclei spare DMTP and DNMTP. They have been implicated in behavioral-state control and response to salient stimuli in associative learning. mPFC functions are served during DNMTP by discrete populations of neurons with responses related to motor preparation, movements, lever press responses, reinforcement anticipation, reinforcement delivery, and memory delay. Population analyses show that different responses are timed so that they effectively tile the temporal interval from when DNMTP trials are initiated until the end. Event-related responses of MD neurons during DNMTP are predominantly related to movement and reinforcement, information important for DNMTP choice. These responses closely mirror the activity of mPFC neurons with similar responses. Pharmacological inactivation of MD and adjacent rIL affects the expression of diverse action- and outcome-related responses of mPFC neurons. Lesions of MD before training are associated with a shift away from movement-related responses in mPFC important for DNMTP choice. These results suggest that MD has short-term effects on the expression of event-related activity in mPFC and long-term effects that tune mPFC neurons to respond to task-specific information.

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Cholinergic and dopaminergic‐mediated motivated behavior in healthy states and in substance use and mood disorders

Nunes

Kebede

Bağdaş

et al. 2022

J Exper Analysis Behavior

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Acetylcholine is an important neuromodulator of the mesolimbic dopamine (DA) system, which itself is a mediator of motivated behavior. Motivated behavior can be described by two primary components, termed directional and activational motivation, both of which can be examined and dissociated using effort-choice tasks. The directional component refers to motivated behavior directed towards reinforcing stimuli and away from aversive stimuli. Behaviors characterized by increased vigor, persistence, and work output are considered to reflect activational components of motivation. Disruption of DA signaling has been shown to decrease activational components of motivation, while leaving directional features intact. Facilitation of DA release promotes the activational aspects of motivated behavior. In this review, we discuss cholinergic and DA regulation of motivated behaviors. We place emphasis on effortchoice processes and the ability of effort-choice tasks to examine and dissociate changes of motivated behavior in the context of substance use and mood disorders. Furthermore, we consider how altered cholinergic transmission impacts motivated behavior across disease states, and the possible role of cholinergic dysregulation in the etiology of these illnesses. Finally, we suggest that treatments targeting cholinergic activity may be useful in ameliorating motivational disruptions associated with substance use and comorbid substance use and mood disorders.

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Chemogenetic Modulation and Single-Photon Calcium Imaging in Anterior Cingulate Cortex Reveal a Mechanism for Effort-Based Decisions

Abstract: Chemogenetic modulation and single-photon calcium imaging in anterior cingulate cortex reveal a mechanism for effort-based decisions

Cited by 57 publications

References 83 publications

Dorsomedial prefrontal neural ensembles reflect changes in task utility that culminate in task quitting

Dorsomedial prefrontal neural ensembles reflect changes in task utility that culminate in task quitting

Central Thalamic-Medial Prefrontal Control of Adaptive Responding in the Rat: Many Players in the Chamber

Cholinergic and dopaminergic‐mediated motivated behavior in healthy states and in substance use and mood disorders

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