Medial prefrontal cortex lesions disrupt prepotent action selection signals in dorsomedial striatum

Brockett, Adam T.; Tennyson, Stephen S.; deBettencourt, Coreylyn A.; Kallmyer, Madeline; Roesch, Matthew R.

doi:10.1016/j.cub.2022.06.025

Cited by 9 publications

(10 citation statements)

References 61 publications

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“…Further, neural signals representing accurate response direction during performance of STOP-change tasks have been shown to be weaker and more slowly resolved on STOP trials that follow GO trials, reflecting the higher conflict between the two actions ( Bryden et al, 2012 ; Brockett et al, 2020b , 2022 ). Given this, we hypothesized that OFC inhibition might impact behavior differently broken down by trial sequence ( Bryden et al, 2012 , 2016 , 2019 ; Bryden and Roesch, 2015 ; Tennyson et al, 2018 ; Brockett et al, 2020a , b , 2022 ). To test this hypothesis, we examined gG (g: previous trial GO; G current trial GO), sG (s: previous trial STOP; G current trial GO), and gS (g: previous trial GO; G current trial STOP) trials.…”

Section: Resultsmentioning

confidence: 99%

“…Total trials and total reward trials were computed as well. Similar calculations were made after filtering the data for sequence effects (i.e., when a GO preceded a STOP or GO or when a stop preceded either a STOP or GO) as previously published ( Bryden et al, 2012 , 2016 , 2019 ; Bryden and Roesch, 2015 ; Tennyson et al, 2018 ; Brockett et al, 2020a , b , 2022 ). Planned t tests were conducted, where appropriate to verify the directionality of interactions.…”

Section: Methodsmentioning

confidence: 99%

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Optogenetic Inhibition of the Orbitofrontal Cortex Disrupts Inhibitory Control during Stop-Change Performance in Male Rats

Brockett,

Kumar,

Sharalla

et al. 2024

eNeuro

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Historically, the orbitofrontal cortex (OFC) has been implicated in a variety of behaviors ranging from reversal learning and inhibitory control to more complex representations of reward value and task space. While modern interpretations of the OFC's function have focused on a role in outcome evaluation, these cognitive processes often require an organism to inhibit a maladaptive response or strategy. Single unit recordings from the OFC in rats performing a stop-change task show that the OFC responds strongly to STOP trials. To investigate the role that the OFC plays in stop-change performance we expressed halorhodopsin (eNpHR3.0) in excitatory neurons in the OFC and tested rats on the stop-change task. Previous work suggests that the OFC differentiates between STOP trials based on trial sequence (i.e., gS trials: STOP trials preceded by a GO versus sS trials: STOP trials preceded by a STOP). We found that yellow light activation of the eNpHR3.0 expressing neurons significantly decreased accuracy only on STOP trials that followed GO trials (gS trials). Further, optogenetic inhibition of OFC speeded reaction times on error trials. This suggests that the OFC plays a role in inhibitory control processes, and that this role needs to be accounted for in modern interpretations of OFC function.Significance StatementThe orbitofrontal cortex (OFC) is a highly interconnected brain region thought to be essential for healthy cognitive function. Historically, research has implicated the OFC in the inhibition of inappropriate actions, however, more recent work has focused on its role in guiding value-based decision making. Using a modified version of a canonical inhibitory control task in combination with optogenetics, we show that while important for value-based decision making, disruption of excitatory neurons in the OFC impairs inhibitory control processes as well. This highlights the need for theoretical accounts of OFC function to accommodate its role in both types of cognitive processes.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Optogenetic Inhibition of the Orbitofrontal Cortex Disrupts Inhibitory Control during Stop-Change Performance in Male Rats

Brockett,

Kumar,

Sharalla

et al. 2024

eNeuro

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“…An extensive body of evidence shows that lesions in the rodent mPFC impairs several executive functions similarly as lesions of human PFC. For example, lesions on the rodent mPFC produced deficiencies in working memory ( Ragozzino and Kesner, 2001 ), focused attention ( Kahn et al, 2012 ), decision-making ( Croxson et al, 2014 ), strategy switching ( de Bruin et al, 2001 ; Floresco et al, 2009 ) and inhibitory control ( Brockett et al, 2022 ). Evidence from spatial memory tasks has shown that the mPFC supports strategy progression during spatial learning ( de Bruin et al, 1997 ).…”

Section: The Prefrontal Cortex and Cognitive Control Of Behaviormentioning

confidence: 99%

Large-scale coupling of prefrontal activity patterns as a mechanism for cognitive control in health and disease: evidence from rodent models

Negrón-Oyarzo,

Dib,

Chacana-Véliz

et al. 2024

Front. Neural Circuits

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Cognitive control of behavior is crucial for well-being, as allows subject to adapt to changing environments in a goal-directed way. Changes in cognitive control of behavior is observed during cognitive decline in elderly and in pathological mental conditions. Therefore, the recovery of cognitive control may provide a reliable preventive and therapeutic strategy. However, its neural basis is not completely understood. Cognitive control is supported by the prefrontal cortex, structure that integrates relevant information for the appropriate organization of behavior. At neurophysiological level, it is suggested that cognitive control is supported by local and large-scale synchronization of oscillatory activity patterns and neural spiking activity between the prefrontal cortex and distributed neural networks. In this review, we focus mainly on rodent models approaching the neuronal origin of these prefrontal patterns, and the cognitive and behavioral relevance of its coordination with distributed brain systems. We also examine the relationship between cognitive control and neural activity patterns in the prefrontal cortex, and its role in normal cognitive decline and pathological mental conditions. Finally, based on these body of evidence, we propose a common mechanism that may underlie the impaired cognitive control of behavior.

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“…And yet, the basal ganglia project to multiple regions besides the neocortex which may also trigger motor commands (Figure 1F) (Guo et al, 2017;Mink, 1996;Utter & Basso, 2008;Yin & Knowlton, 2006). Revealing the functional organizations of the motor cortex and the basal ganglia requires conducting representational and causal studies from both structures in subjects performing the same behavioral task (Antzoulatos & Miller, 2011;Brockett et al, 2022;Clarke et al, 2008;Kupferschmidt et al, 2017;Muhammad et al, 2006;Pasupathy & Miller, 2005;Peters et al, 2021;Pimentel-Farfan et al, 2022) The mouse whisker system is an ideal model system to test this functional organization, due to its simplified and well-characterized neural anatomy. Whisker stimulus responses propagate to the contralateral whisker representation of primary somatosensory cortex (S1).…”

Section: Introductionmentioning

confidence: 99%

Dorsolateral striatum, not motor cortex, is a bottleneck for responding to task-relevant stimuli in a learned whisker detection task in mice

Zareian

Lam

Zhang

et al. 2022

Preprint

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A learned sensory-motor behavior engages multiple brain regions, including the neocortex and the basal ganglia. How these brain regions coordinate to affect sensory selection (for target stimuli) and inhibition (for distractor stimuli) remains unknown. Here, we performed laminar electrophysiological recordings and muscimol inactivation in frontal cortex and dorsolateral striatum to determine the representations within and functions of each region during selective detection performance. From the recording experiments, in deep layers of frontal cortex and dorsolateral striatum we observed similar encoding of sensory and motor features. However, muscimol inactivation of each region resulted in drastically different outcomes. Inactivation of target-aligned striatum substantially reduced behavioral responses to all task stimuli without disrupting the ability to respond, suggesting essential roles in sensory selection. In contrast, inactivation of distractor-aligned frontal cortex increased responses to distractor stimuli, indicating essential roles in distractor inhibition. Overall, these data suggest distinct functions of frontal cortex and dorsolateral striatum in this task, despite having similar neuronal representations.

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Medial prefrontal cortex lesions disrupt prepotent action selection signals in dorsomedial striatum

Cited by 9 publications

References 61 publications

Optogenetic Inhibition of the Orbitofrontal Cortex Disrupts Inhibitory Control during Stop-Change Performance in Male Rats

Optogenetic Inhibition of the Orbitofrontal Cortex Disrupts Inhibitory Control during Stop-Change Performance in Male Rats

Large-scale coupling of prefrontal activity patterns as a mechanism for cognitive control in health and disease: evidence from rodent models

Dorsolateral striatum, not motor cortex, is a bottleneck for responding to task-relevant stimuli in a learned whisker detection task in mice

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