Scientific Understanding of Consciousness
Anterior Cingulate Cortex Mediates Behavioral Adaptation
Nature 488, 218–221 (09 August 2012)
Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation
Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114, USA
Sameer A. Sheth, Matthew K. Mian, Shaun R. Patel, Ziv M. Williams & Emad N. Eskandar
Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, Massachusetts 02118, USA
Shaun R. Patel
Department of Neurosurgery, Alpert Medical School, Brown University and Rhode Island Hospital, Providence, Rhode Island 02912, USA
Wael F. Asaad
Department of Psychiatry, Massachusetts General Hospital, Boston, Massachusetts 02114, USA
Darin D. Dougherty & George Bush
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 making, monitoring for conflict between competing responses and predicting task difficulty. 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 effect, 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.
Human cognition is characterized by the ability to parse and evaluate a stream of constantly changing environmental stimuli so as to choose the most appropriate response in evolving conditions. The dACC is thought to be important in regulating cognitive control over goal-directed behaviour. Various theories postulate its involvement in linking reward-related information to action, monitoring for conflict between competing responses or detecting the likelihood of error commission. Despite substantial information from studies using lesions, functional magnetic resonance imaging (fMRI) and event-related potentials, the neurophysiological basis of its regulatory role remains the subject of considerable debate.
We studied dACC function with a combination of fMRI, single-neuronal recordings and observations of behaviour before and after lesion in human subjects undergoing surgical cingulotomy, a procedure in which a precise, stereotactically targeted lesion is created in the dACC. Microelectrode recordings, which are routinely performed during the procedure, allowed us to record from individual dACC neurons. Six subjects participated, and in four of these we also obtained a preoperative fMRI with the same task. In four we recorded behavioural responses using the same task immediately after cingulotomy.
Subjects performed the multi-source interference task, a Stroop-like task in which they viewed a cue consisting of three numbers and had to indicate, by pressing a button, the unique number (‘target’) that differed from the other two numbers (‘distracters’)
We recorded 59 well-isolated single dACC neurons, with an average baseline firing rate of 5.7 ± 0.7 (mean ± s.e.m.) spikes per second.
Current models of dACC function, whether predicated on conflict monitoring, reinforcement learning or reward-based decision making, require that future dACC activity reflect past experience, but modulation of dACC firing on the basis of recent history has not been demonstrated at the single-neuronal level.
Our results support the view that the dACC is specifically responsible for providing a continuously updated account of predicted demand on cognitive resources. The salient influence of current dACC activity on future neuronal activity and behaviour permits the implementation of behavioural adjustments that optimize performance. In situations in which cognitive demands remain constant, this signal facilitates efficiency by accelerating responses. In situations involving rapidly changing demands, it promotes accuracy by retarding responses.
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