State University of New York, 1975
Neurophysiology - motor control
Specific research interests include: 1) brain mechanisms underlying the control of voluntary movements, 2) recovery of motor function following brain injury and 3) neural injury and dysfunction associated with SIV/HIV infection.
Modern neurophysiological techniques are used to investigate the function of neurons in the cerebral cortex and brainstem. The electrical discharges of single neurons are recorded during various movement tasks. Computerized analysis techniques are used to reveal the functional contribution of a neuron to muscle activation.
Recent work has focused on the use of brain electrical stimulation and its mechanism. Electrical stimulation of the brain was one of the first experimental methods applied to understanding brain organization and function and it continues as a highly useful method both in research and clinical applications. Intracortical microstimulation (ICMS) involves applying electrical stimuli through a microelectrode suitable for recording the action potentials of single neurons. ICMS can be categorized into single-pulse stimulation; high-frequency, short-duration stimulation; and high-frequency, long-duration stimulation. For clinical and experimental reasons, considerable interest focuses on the mechanism of neural activation by electrical stimuli.
Recent data from our lab suggest that action potentials evoked in cortical neurons by high-frequency electrical stimulation do not sum with the natural, behaviorally related background activity; rather, high-frequency stimulation eliminates and replaces natural activity. We refer to this as "neural hijacking". This mechanism is illustrated in Figure 1. We propose that a major component of the mechanism underlying neural hijacking is excitation of axons by ICMS and elimination of natural spikes by antidromic collision with stimulus-driven spikes evoked at high frequency. Evidence also supports neural hijacking as an important mechanism underlying the action of deep brain stimulation in the subthalamic nucleus and its therapeutic effect in treating Parkinson's disease.
Figure 1. Proposed mechanism of neural hijacking associated with high-frequency, long-duration intracranial microstimulation (HFLD-ICMS) of motor cortex. High-frequency stimulation activates axon terminals in the vicinity of stimulation (dotted line) as well as some corticospinal output cells directly (neurons A and B). Stimulation of axon terminals results in antidromic activation (neuron C) in which the stimulus-evoked spikes collide with and eliminate the background naturally occurring spikes. This mechanism of elimination by collision potentially occurs with all afferent inputs to motor cortex, including those from secondary cortical motor areas as well as thalamic inputs (neuron D). The stimulus-driven spikes elicited in axon terminals also conduct orthodromically to activate output cells (A and B).
At the higher stimulus strengths generally used with HFLD-ICMS, some corticospinal output cells are probably also activated directly. In either case, natural activity has been eliminated and replaced with spikes that are entirely stimulus driven. Neural Net refers to the spinal cord network mediating non-monosynaptic input to motoneurons from cortex and other sources. Brainstem (BS) pathways include reticulospinal and rubrospinal. From Cheney, Griffin and Van Acker (2013) Neural Hijacking: Action of High Frequency Electrical Stimulation on Cortical Circuits. The Neuroscientist 19: 434-441.
Park, M.C., Belhaj-Saif, A. and Cheney, P.D. Consistent features in the forelimb representation of primary motor cortex of rhesus macaques. J. Neurosci. 21: 2784-2792, 2001.
Cheney, P.D. Electrophysiological Methods for Mapping Brain Motor Circuits. In: Brain Mapping: The Methods, Second Edition, A. W. Toga and J. C. Mazziotta (Eds.), New York, NY: Academic Press, 2002.
Park, M.C., Belhaj-Saif, A. and Cheney, P.D. Distribution and properties of poststimulus effects in proximal and distal forelimb muscles from primary motor cortex in rhesus macaques. J. Neurophysiol. 92: 2968-2984, 2004.
Marcario, J.K., Manaye, K.F., SantaCruz, K.S., Mouton, P.R., Berman, N.E.J., and Cheney, P.D. Severe subcortical degeneration in macaques infected with neurovirulent simian immunodeficiency virus. J. Neurovirol. 10: 387-399, 2004.
Cheney, P.D., Belhaj-Saïf, A. and Boudrias, M.H. Principles of Corticospinal System Organization and Function. In: Handbook of Clinical Neurophysiology, Vol. 4, Clinical Neurophysiology of Motor Neuron Diseases, A. Eisen, Editor, New York, NY: Elsevier Science, pp. 59-96, 2004.
Boudrias, M.H, Belhaj-Saïf and Cheney, P.D. Output Properties of Supplementary Motor Area (SMA) in Rhesus Macaques. Cerebral Cortex 16: 632-638, 2006.
Marcario, J.K., Riazi, M., Adany, A., Kenjale, H., Fleming, H.K., Marquis, M., Nemon, O., Mayo, M., Yankee, T., Narayan, O., and Cheney, P.D. Effect of morphine on the neuropathogenesis of SIVmac infection in Indian rhesus macaques. J. Neuroimmune Pharmacology 3: 12-25, 2008.
Griffin, D.M., Hudson, H.M., Belhaj-Saif, A., McKiernan, B.J. and Cheney, P.D. Do Corticomotoneuronal Cells Predict Target Muscle EMG Activity? J. Neurophysiol. 99: 1169-1186, 2008.
Cheney, P.D., Riazi, M. and Marcario, J.K. Behavioral and Neurophysiological Hallmarks of SIV Infection in Macaque Monkeys. J. Neurovirol. 14: 301-308, 2008.
Griffin, D.M., Hudson, H.M., Belhaj-Saif, A. and Cheney, P.D. Stability of output effects from motor cortex to forelimb muscles in primates. J. Neurosci., 29: 1915-1927, 2009.
Hudson, H.M., Griffin, D.M., Belhaj-Saif, A., Lee, SP and Cheney, P.D. Methods for chronic recording of EMG activity from large numbers of hindlimb muscles in awake rhesus macaques. J. Neurosci. Methods 189: 153-161, 2010
Griffin, D.M., Hudson, H.M., Belhaj-Saif, A. and Cheney, P.D. Hijacking cortical motor output with repetitive microstimulation. J. Neurosci. 31: 13088-13096, 2011.
Cheney, P.D., Griffin, D.M. and Van Acker, G.M. Neural hijacking: action of high frequency electrical stimulation on cortical circuits. The Neuroscientist 19: 434-441, 2013, September 2013. Epub ahead of print. PMID: 2296864. DOI: 10.1177/1073858412458368.
Van Acker, G.M. III, Amundsen, S.L., Messamore, W.G., Zhang, H.Y., Luchies, C.H., Kovac, A. and Cheney, P.D. Optimal RL-ICMS parameters applied to the primary motor cortex for evoking forelimb movements to static spatial end-points. J. Neurophysiol. 110: 1180-1189, 2013. Sept 2013 published,; June 2013, Epub ahead of print. PMID: 23741044
Jo, J. Zhang, H., Cheney, P.D., Yang, X. Photoacoustic detection of functional responses in the motor cortex of awake behaving monkey during forelimb movement. J. Biomed. Optics 17: 1-3, November 2012. Epub. PMID: 23089667. DOI: 10.1117/1.JBO.17.11.110503.
Hudson, H.M., Griffin, D.M., Belhaj-Saif, A. and Cheney, P.D. Cortical output to fast and slow muscles of the ankle in the rhesus macaque. Front Neural Circuits 7: 1-11, March 2013, Epub. PMID 23459919. DOI: 10.3389/fncir.2013.00033.
Griffin, D.M., Hudson, H.M., Belhaj-Saif, A. and Cheney, P.D. EMG activation patterns associated with high frequency, long-duration intracortical microstimuation of primary motor cortex. J. Neurosci. 34: 1647-1656, 2014.
Van Acker, G.M. III, Amundsen, S.L., Messamore, W.G., Zhang, H.Y., Luchies, A. and Cheney, P.D. Equilibrium-based movement end-points elicited from primary motor cortex using repetitive microstimulation. J Neurosci. 34(47):15722-15734. 2014 doi: 10.1523/JNEUROSCI.0214-14.2014. PMID: 25411500
Hudson, H.M., Griffin, D.M., Belhaj-Saif, A. and Cheney, P.D. Properties of primary motor cortex output to hindlimb muscles in the primate. J Neurophysiol. 113 (3): 937-949, 2015. PMID: 25411454
Paul D. Cheney, Ph.D.
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