Causal evidence for cholinergic stabilization of attractor landscape dynamics
Natasha L. Taylor,
Christopher J. Whyte,
Brandon R. Munn,
Catie Chang,
Joseph T. Lizier,
David A. Leopold,
Janita N. Turchi,
Laszlo Zaborszky,
Eli J. Műller,
James M. Shine
Affiliations
Natasha L. Taylor
Brain and Mind Centre, The University of Sydney, Sydney, NSW, Australia; Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia
Christopher J. Whyte
Brain and Mind Centre, The University of Sydney, Sydney, NSW, Australia; Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia
Brandon R. Munn
Brain and Mind Centre, The University of Sydney, Sydney, NSW, Australia; Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia
Catie Chang
Vanderbilt School of Engineering, Vanderbilt University, Nashville, TN, USA
Joseph T. Lizier
Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia; School of Computer Science, The University of Sydney, Sydney, NSW, Australia
David A. Leopold
Neurophysiology Imaging Facility, National Institute of Mental Health, Washington DC, USA; Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda MD, USA
Janita N. Turchi
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda MD, USA
Laszlo Zaborszky
Centre for Molecular & Behavioral Neuroscience, Rutgers, The State University of New Jersey, Newark, NJ, USA
Eli J. Műller
Brain and Mind Centre, The University of Sydney, Sydney, NSW, Australia; Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia
James M. Shine
Brain and Mind Centre, The University of Sydney, Sydney, NSW, Australia; Centre for Complex Systems, The University of Sydney, Sydney, NSW, Australia; Corresponding author
Summary: There is substantial evidence that neuromodulatory systems critically influence brain state dynamics; however, most work has been purely descriptive. Here, we quantify, using data combining local inactivation of the basal forebrain with simultaneous measurement of resting-state fMRI activity in the macaque, the causal role of long-range cholinergic input to the stabilization of brain states in the cerebral cortex. Local inactivation of the nucleus basalis of Meynert (nbM) leads to a decrease in the energy barriers required for an fMRI state transition in cortical ongoing activity. Moreover, the inactivation of particular nbM sub-regions predominantly affects information transfer in cortical regions known to receive direct anatomical projections. We demonstrate these results in a simple neurodynamical model of cholinergic impact on neuronal firing rates and slow hyperpolarizing adaptation currents. We conclude that the cholinergic system plays a critical role in stabilizing macroscale brain state dynamics.
