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Articles, Behavioral/Cognitive

Free Energy, Precision and Learning: The Role of Cholinergic Neuromodulation

Rosalyn J. Moran, Pablo Campo, Mkael Symmonds, Klaas E. Stephan, Raymond J. Dolan and Karl J. Friston
Journal of Neuroscience 8 May 2013, 33 (19) 8227-8236; DOI: https://doi.org/10.1523/JNEUROSCI.4255-12.2013
Rosalyn J. Moran
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
2Virginia Tech Carilion Research Institute and Bradley Department of Electrical and Computer Engineering, Virginia Tech, Roanoke, Virginia 24016,
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Pablo Campo
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
3Department of Basic Psychology, Autonoma University of Madrid, 28049 Madrid, Spain,
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Mkael Symmonds
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
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Klaas E. Stephan
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
4Translational Neuromodeling Unit, Institute for Biomedical Engineering, University of Zurich and Swiss Federal Institute of Technology (ETH Zurich), 8092 Zurich, Switzerland, and
5Laboratory for Social and Neural Systems Research, Department of Economics, University of Zurich, CH-8006 Zurich, Switzerland
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Raymond J. Dolan
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
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Karl J. Friston
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
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Abstract

Acetylcholine (ACh) is a neuromodulatory transmitter implicated in perception and learning under uncertainty. This study combined computational simulations and pharmaco-electroencephalography in humans, to test a formulation of perceptual inference based upon the free energy principle. This formulation suggests that ACh enhances the precision of bottom-up synaptic transmission in cortical hierarchies by optimizing the gain of supragranular pyramidal cells. Simulations of a mismatch negativity paradigm predicted a rapid trial-by-trial suppression of evoked sensory prediction error (PE) responses that is attenuated by cholinergic neuromodulation. We confirmed this prediction empirically with a placebo-controlled study of cholinesterase inhibition. Furthermore, using dynamic causal modeling, we found that drug-induced differences in PE responses could be explained by gain modulation in supragranular pyramidal cells in primary sensory cortex. This suggests that ACh adaptively enhances sensory precision by boosting bottom-up signaling when stimuli are predictable, enabling the brain to respond optimally under different levels of environmental uncertainty.

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The Journal of Neuroscience: 33 (19)
Journal of Neuroscience
Vol. 33, Issue 19
8 May 2013
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Free Energy, Precision and Learning: The Role of Cholinergic Neuromodulation
Rosalyn J. Moran, Pablo Campo, Mkael Symmonds, Klaas E. Stephan, Raymond J. Dolan, Karl J. Friston
Journal of Neuroscience 8 May 2013, 33 (19) 8227-8236; DOI: 10.1523/JNEUROSCI.4255-12.2013

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Free Energy, Precision and Learning: The Role of Cholinergic Neuromodulation
Rosalyn J. Moran, Pablo Campo, Mkael Symmonds, Klaas E. Stephan, Raymond J. Dolan, Karl J. Friston
Journal of Neuroscience 8 May 2013, 33 (19) 8227-8236; DOI: 10.1523/JNEUROSCI.4255-12.2013
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