Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation

Abstract

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.

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Figure 1: Behavioural task, fMRI and subject performance.
Figure 2: Individual and population neuronal responses.
Figure 3: Effect of previous trial on dACC firing and RT.
Figure 4: Abolition of behavioural adaptation after a targeted dACC lesion.

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Acknowledgements

This work was supported by grants from the National Science Foundation (IOB 0645886), the National Institutes of Health (NEI 1R01EY017658-01A1, NIDA 1R01NS063249, NIMH Conte Award MH086400 and R25 NS065743), the Klingenstein Foundation, the Howard Hughes Medical Institute, the Sackler Scholar Programme in Psychobiology, the Centers for Disease Control (5 R01 DP000339), the Benson-Henry Institute at Massachusetts General Hospital for Mind–Body Medicine, the David Judah Fund, the McIngvale Fund, and the Center for Functional Neuroimaging Technologies (P41RR14075).

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E.N.E., W.F.A., Z.M.W. and D.D.D. designed the study. G.B. administered and interpreted the fMRI scans. E.N.E. performed the surgical procedures, and S.A.S., M.K.M., S.R.P. and W.F.A. obtained the neuronal recordings. S.A.S. and M.K.M. analysed the data and wrote the manuscript. All authors edited the manuscript.

Corresponding author

Correspondence to Emad N. Eskandar.

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The authors declare no competing financial interests.

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This file contains Supplementary Figures 1-9, Supplementary Methods, Supplementary Table 1, a Supplementary Discussion and Supplementary Notes 1-4. (PDF 1942 kb)

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Sheth, S., Mian, M., Patel, S. et al. Human dorsal anterior cingulate cortex neurons mediate ongoing behavioural adaptation. Nature 488, 218–221 (2012). https://doi.org/10.1038/nature11239

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