Original Research ARTICLE

Front. Syst. Neurosci., 31 August 2011 | http://dx.doi.org/10.3389/fnsys.2011.00067

Multi-neuronal recordings in the basal ganglia in normal and dystonic rats

Mark S. Baron1*, Kunal D. Chaniary2, Ann C. Rice1 and Steven M. Shapiro1
  • 1 Department of Neurology, Virginia Commonwealth University, Richmond, VA, USA
  • 2 Department of Biomedical Engineering, Virginia Commonwealth University, Richmond, VA, USA

Classical rate-based pathway models are invaluable for conceptualizing direct/indirect basal ganglia pathways, but cannot account for many aspects of normal and abnormal motor control. To better understand the contribution of patterned basal ganglia signaling to normal and pathological motor control, we simultaneously recorded multi-neuronal and EMG activity in normal and dystonic rats. We used the jaundiced Gunn rat model of kernicterus as our experimental model of dystonia. Stainless steel head fixtures were implanted on the skulls and EMG wires were inserted into antagonistic hip muscles in nine dystonic and nine control rats. Under awake, head-restrained conditions, neuronal activity was collected from up to three microelectrodes inserted in the principal motor regions of the globus pallidus (GP), subthalamic nucleus, and entopeduncular nucleus (EP). In normal animals, most neurons discharged in regular or irregular patterns, without appreciable bursting. In contrast, in dystonic animals, neurons discharged in slow bursty or irregular, less bursty patterns. In normal rats, a subset of neurons showed brief discharge bursts coinciding with individual agonist or antagonist EMG bursts. In contrast, in dystonics, movement related discharges were characterized by more prolonged bursts which persist over multiple dystonic co-contraction epics. The pattern of movement related decreases in discharge activity however did not differ in dystonics compared to controls. In severely dystonic rats, exclusively, simultaneously recorded units often showed abnormally synchronized movement related pauses in GP and bursts in EP. In conclusion, our findings support that slow, abnormally patterned neuronal signaling is a fundamental pathophysiological feature of intrinsic basal ganglia nuclei in dystonia. Moreover, from our findings, we suggest that excessive movement related silencing of neuronal signaling in GP profoundly disinhibits EP and in turn contributes to sustained, unfocused dystonic muscle contractions.

Keywords: dystonia, basal ganglia, globus pallidus, subthalamus, entopeduncular nucleus, microelectrode recording, rats

Citation: Baron MS, Chaniary KD, Rice AC and Shapiro SM (2011) Multi-neuronal recordings in the basal ganglia in normal and dystonic rats. Front. Syst. Neurosci. 5:67. doi: 10.3389/fnsys.2011.00067

Received: 23 April 2011; Accepted: 01 August 2011;
Published online: 31 August 2011.

Edited by:

Charles J. Wilson, University of Texas at San Antonio, USA

Reviewed by:

Atsushi Nambu, National Institute for Physiological Sciences, Japan
Hitoshi Kita, The University Tennessee Health Science Center, USA

Copyright: © 2011 Baron, Chaniary, Rice and Shapiro. This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

*Correspondence: Mark S. Baron, Department of Neurology, Virginia Commonwealth University, 6th Floor Sanger Hall, Box 980599, Richmond, VA 23220, USA. e-mail: mbaron@mcvh-vcu.edu