Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation

Abstract

Functional imaging, single-cell recording and targeted surgical lesions were used in human patients undergoing cingulotomy to show that the dorsal anterior cingulate cortex provides a continuously updated prediction of expected cognitive demand. The dorsal anterior cingulate cortex (dACC) plays an important part in regulating cognitive control in both humans and non-human primates, but its precise function remains a matter of debate. Various hypotheses have been proposed, including reward-based decision making, monitoring for conflict between competing responses, and predicting task difficulty. This paper combines functional imaging, single-cell recording and targeted surgical lesions in human patients preparing for cingulotomy, and shows that the dACC provides a continuously updated prediction of expected cognitive demand. The authors propose that it helps to optimize future behavioural responses by hastening or delaying responses as appropriate to the upcoming cognitive load. The ability to optimize behavioural performance when confronted with continuously evolving environmental demands is a key element of human cognition. The dorsal anterior cingulate cortex (dACC), which lies on the medial surface of the frontal lobes, is important in regulating cognitive control. Hypotheses about its function include guiding reward-based decision making1, monitoring for conflict between competing responses2 and predicting task difficulty3. Precise mechanisms of dACC function remain unknown, however, because of the limited number of human neurophysiological studies. Here we use functional imaging and human single-neuron recordings to show that the firing of individual dACC neurons encodes current and recent cognitive load. We demonstrate that the modulation of current dACC activity by previous activity produces a behavioural adaptation that accelerates reactions to cues of similar difficulty to previous ones, and retards reactions to cues of different difficulty. Furthermore, this conflict adaptation, or Gratton effect2,4, is abolished after surgically targeted ablation of the dACC. Our results demonstrate that the dACC provides a continuously updated prediction of expected cognitive demand to optimize future behavioural responses. In situations with stable cognitive demands, this signal promotes efficiency by hastening responses, but in situations with changing demands it engenders accuracy by delaying responses.