Macaque anterior cingulate cortex deactivation impairs performance and alters lateral prefrontal oscillatory activities in a rule-switching task

Abstract

In primates, both the dorsal anterior cingulate cortex (dACC) and the dorsolateral prefrontal cortex (dlPFC) are key regions of the frontoparietal cognitive control network. To study the role of the dACC and its communication with the dlPFC in cognitive control, we recorded the local field potentials from the dlPFC before and during the reversible deactivation of the dACC, in macaque monkeys engaging in uncued switches between two stimulus-response rules. Cryogenic dACC deactivation impaired response accuracy during rule-maintenance, but not rule-switching, which coincided with a reduction in the correct-error difference in dlPFC beta activities specifically during maintenance of the more challenging rule. During both rule switching and maintenance, dACC deactivation prolonged the animals' reaction time and reduced task-related theta/alpha activities in the dlPFC; it also weakened dlPFC theta-gamma 2 phase-amplitude modulation. Thus, the dACC and its interaction with the dlPFC plays a critical role in the maintenance of a new, challenging rule. been implicated in attention and cognitive control (Tsujimoto et al., 2006;Tsujimoto et al., 2010;Voloh et al., 2015;Voloh and Womelsdorf, 2017;Womelsdorf et al., 2010). While less studied than theta, prefrontal beta oscillations (13-30Hz) has been suggested to orchestrate cell assemblies that maintain information in short-term memory (Kopell et al., 2011), predict reaction time (Buschman et al., 2012Ma et al., 2018), and reflect action outcome (Skoblenick et al., 2016). In between the theta and the beta bands, the alpha rhythms (9-12Hz) may help inhibit attention to irrelevant information (Buschman et al., 2012;Puig and Miller, 2015).Here, we found that cryogenic dACC deactivation impaired the animals' task performance in a manner consistent with an impairment of rule-maintenance, but not ruleswitching. This was manifested by a lower plateau in response accuracy rather than a delay in the implementation of the new rule. Correlated with this performance impairment was a reduction in the absolute difference in dlPFC fixation-period beta activities between correct and error trials, particularly for antisaccades. We also observed increased saccadic reaction time with both rules and across post-switch stages, which coincided with a reduction in task-related theta/alpha activities (5-15Hz) found for both rules in the dlPFC. Lastly, while theta-gamma phaseamplitude modulation in the dlPFC became stronger in the second halves of the sessions, during both on-and off-task periods, dACC deactivation reversed this pattern and resulted in a decrease in this cross-frequency interaction. Together our findings suggest a critical role of the dACC and its interaction with the dlPFC in the maintenance of new rules in a feedback-based rule-switching task. RESULTS dACC Deactivation Impaired Behavioral Performance on the Rule-Switch Task

Ultrasound modulation of macaque prefrontal cortex selectively alters credit assignment–related activity and behavior

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Translating Expectation into Visual Selection through a Beta-Synchronous Fronto-Parietal Neural Subnetwork

“…One prominent, well-documented source of theta rhythmic activity in the FEF is the anterior cingulate cortex. The anterior cingulate generates theta rhythmic output following the onset of learned attention cues (Voloh et al, 2015), synchronizes to the FEF at theta during topdown guided working memory performance (Babapoor-Farrokhran et al, 2017), and is causally involved in generating prefrontal theta activity (Ma et al, 2019). These insights make it possible that the behaviorally relevant beta-synchronous neuronal subnetwork identified in the new study is under the influence of anterior, medial prefrontal activity and thereby gains access to the expected values of possible visual target features and task rules needed to succeed with attentional control.…”

Transcranial Ultrasound Stimulation in Anterior Cingulate Cortex Impairs Information Sampling and Learning in Loss Contexts

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