Electrophysiological Correlates of a Versatile Executive Control System in the Monkey Anterior Cingulate Cortex

Abstract

When a subject faces conflicting situations, decision-making becomes uncertain. The human dorsal anterior cingulate cortex (dACC) has been repeatedly implicated in the monitoring of such situations, and its neural activity is thought to be involved in behavioral adjustment. However, this hypothesis is mainly based on neuroimaging results and is challenged by animal studies that failed to report any neuronal correlates of conflict monitoring. This discrepancy is thought be due either to methodological or more fundamental cross-species differences. In this study, we eliminated methodological biases and recorded single-neuron activity in monkeys performing a Stroop-like task. We found specific changes in dACC activity during incongruent trials but only in a small subpopulation of cells. Critically, these changes were not related to reaction time and were absent before any incorrect action was taken. A larger fraction of neurons exhibited sustained activity during the whole decision period, whereas another subpopulation of neurons was modulated by reaction time, with a gradual increase in their firing rate that peaked at movement onset. Most of the neurons found in these subpopulations exhibited activity after the delivery of an external negative feedback stimulus that indicated an error had been made. These findings, which are consistent with an executive control role, reconcile various theories of prefrontal cortex function and support the homology between human and monkey cognitive architectures.

Cortical localization of phase and amplitude dynamics predicting access to somatosensory awareness

“…Intriguingly, a recent study observed that neuronal oscillations in a cingulate cortex were locked to heart beats and that this correlation was predictive of conscious sensory perception [Park et al, ]. Further, the activity in these areas has been associated with egocentric bodily sensations [Nagels et al, ], processing of emotions [Paulus et al, ] as well as monitoring of cognitive goals and expectations [Michelet et al, ; Sheth et al, ]. Thereby, modulations of neuronal activity in cingulate cortices might be a crucial constituent in the subjective experience of conscious sensory perception.…”

“…Further, also activity in insula, anterior and posterior cingulate cortices, and thalamus [Boly et al, 2007;Marois et al, 2004;Sadaghiani et al, 2009] predicts whether sensory stimuli will be consciously detected. Thus, in the multi-second time scales of the BOLD signal fluctuations, conscious access is correlated with increased activity levels in the frontoparietal control areas belonging functionally to FP and dorsal attention networks (DAN) but also with the activity-levels in the ventral attention (VAN) and defaultmode network (DMN), which signal the salience or bottom-up attention to the sensory stimuli [Corbetta and Shulman, 2002;Dosenbach et al, 2008;Power et al, 2011] and self-oriented behaviors [Michelet et al, 2015;Nagels et al, 2015;Sheth et al, 2012], respectively.…”

Dorsal Anterior Cingulate Cortex: A Bottom-Up View

“…Several other studies tested conflict coding at the single neuron level and failed to find it (Amiez et al 2006, Cai & Padoa-Schioppa 2012, Hayden et al 2011a, Ito et al 2003, Quilodran et al 2008). A few recent studies have found modest conflict coding in the dACC, but have neither identified a specific population of conflict-sensitive neurons nor explained why other studies have failed to find such signals (Ebitz & Platt 2015, Michelet et al 2015, Sheth et al 2012). The debate has grown strong, and the discrepancy between BOLD measures and single-unit measures has emerged as a great puzzle in the field (Rushworth et al 2004, Shenhav et al 2014).…”

Checking behavior in rhesus monkeys is related to anxiety and frontal activity

“…The alpha level was set at 0.05 for every statistical test. No statistical methods were used to predetermine sample sizes, but these were similar to sample sizes routinely used in the field for similar experiment30.…”

“…Among these cases, baboons25 and chiefly rhesus monkeys161920 and apes182729 were able to use these alternative opportunities in order to improve their performance when lacking enough information to answer directly. Moreover, recent studies have emphasized the close homology existing between human and monkey brain structures involved in cognitive tasks3031. We therefore hypothesized that rhesus monkeys are likely to express voluntary checking behavior based on their own doubts when facing uncertainty about a previous decision, and then use it as an adaptive function to improve their performance.…”