Theta-activity in anterior cingulate cortex predicts task rules and their adjustments following errors

Abstract

Accomplishing even simple tasks depend on neuronal circuits to configure how incoming sensory stimuli map onto responses. Controlling these stimulus-response (SR) mapping rules relies on a cognitive control network comprising the anterior cingulate cortex (ACC). Single neurons within the ACC convey information about currently relevant SR mapping rules and signal unexpected action outcomes, which can be used to optimize behavioral choices. However, its functional significance and the mechanistic means of interaction with other nodes of the cognitive control network remain elusive and poorly understood. Here, we report that core aspects of cognitive control are encoded by rhythmic theta-band activity within neuronal circuits in the ACC. Throughout task performance, theta-activity predicted which of two SR mapping rules will be established before processing visual target information. Task-selective theta-activity emerged particularly early during those trials, which required the adjustment of SR rules following an erroneous rule representation in the preceding trial. These findings demonstrate a functional correlation of cognitive control processes and oscillatory theta-band activity in macaque ACC. Moreover, we report that spike output of a subset of cells in ACC is synchronized to predictive theta-activity, suggesting that the theta-cycle could serve as a temporal reference for coordinating local task selective computations across a larger network of frontal areas and the hippocampus to optimize and adjust the processing routes of sensory and motor circuits to achieve efficient sensory-motor control.cognitive control | theta-synchronization | attention | oscillation | antisaccade C ognitive control refers to those neuronal processes responsible for assembling task-relevant information, which in turn biases sensory and motor pathways for efficient communication during task processing. Two core functions of cognitive control are (i) the implementation and maintenance of task-relevant stimulusresponse (SR) mapping rules, and (ii) the adjustment and optimization of such representations during task performance according to behavioral outcome. Both functions are subserved by a mosaic of interconnected neuronal groups distributed within frontal cortex (1-4). The anterior cingulate cortex (ACC) is one of the key nodes within this cognitive control network, conveying task relevant information at various time intervals during task processing (5, 6). First, during preparatory periods, ACC neurons convey signals selective for the currently relevant SR mapping rule (7), and allow inferences with respect to changes in SR mapping triggered by either an incorrect response, or an explicit cue to change SR mapping (8). Second, during stimulus processing and delay epochs in working memory paradigms, subsets of neurons encode the expected reward outcome associated with the stimulus (9). Third, following the behavioral response to a target stimulus, neuronal groups in ACC signal whether the behavioral response was incorrect or result...

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

“…Our main finding characterized the statistical relation of two band-limited activity fluctuations comprising a narrow ∼5-to 10-Hz (peak at 7 Hz) theta band and a ∼35-to 55-Hz (peak at 40 Hz) gamma band. Previous studies have documented that a 5-to 10-Hz theta band is a widespread LFP signature in ACC/PFC that increases with specific demands to control goal-directed behavior (22)(23)(24)(25). Our study corroborates these reports (Fig.…”

Brain oscillatory activity associated with task switching and feedback processing

“…Although it still needs to be shown whether these theta modulations reflect analogous cognitive and neural mechanisms, at least partially common mechanisms can be inferred. In general, increases in the theta band seem to be relevant for indexing undesirable or negative outcomes and when further adjustments in the behavior are requested for learning or to improve the performance on subsequent trials (van de Vijver et al, in press;Womelsdorf, Johnston, Vinck, & Everling, 2010). One possibility is that some of these experimental paradigms and, in particular, switch cues and positive feedback signals from our modified WCST engage analogous cognitive control mechanisms reflected in the theta response.…”

Discriminant brain connectivity patterns of performance monitoring at average and single-trial levels

“…Theta dynamics in the MFC relates to focused attention, working memory and action control (Klimesch, 1999;Klimesch et al, 2001;Sauseng et al, 2004;Gevins and Smith, 2000;Buzsáki and Draguhn, 2004), particularly error monitoring and feedback processing in both human (Trujillo and Allen, 2007;Cavanagh, Cohen, and Allen, 2009;Cohen et al, 2008;Wang et al, 2005) and primates (Tsujimoto et al, 2010;Womelsdorf et al, 2010;Kuwabara et al, 2014), and organize cross-regional brain interactions for cognitive control processes (Cohen and Cavanagh, 2011;Cohen et al, 2009). Further studies report the MFC theta as a common temporal neural pattern during endogenous and exogenous monitoring processes (Cavanagh, ZambranoVazquez, and Allen, 2012;Ullsperger et al, 2014).…”