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1Medical Research Council Anatomical Neuropharmacology Unit, University of Oxford, Oxford OX1 3TH; 2Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, London WC1N 3BG, United Kingdom; and 3Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois 60611-3008
Submitted 9 February 2004; accepted in final form 22 March 2004
The responses of single subthalamic nucleus (STN) neurons to cortical activation are complex and depend on the relative activation of several neuronal circuits, making theoretical extrapolation of single neuron responses to the population level difficult. To understand better the degree of synchrony imposed on STN neurons and associated neuronal networks by cortical activation, we recorded the responses of single units, pairs of neighboring neurons, and local field potentials (LFPs) in STN to discrete electrical stimulation of the cortex in anesthetized rats. Stimulation of ipsilateral frontal cortex, but not temporal cortex, generated synchronized "multiphasic" responses in neighboring units in rostral STN, usually consisting of a brief, short-latency excitation, a brief inhibition, a second excitation, and a long-duration inhibition. Evoked LFPs in STN consistently mirrored unit responses; brief, negative deflections in the LFP coincided with excitations and brief, positive deflections with inhibitions. This characteristic LFP was dissimilar to potentials evoked in cortex and structures surrounding STN and was resistant to fluctuations in forebrain activity. The short-latency excitation and associated LFP deflection exhibited the highest fidelity to low-intensity cortical stimuli. Unit response failures, which mostly occurred in caudal STN, were not associated with LFPs typical of rostral STN. These data suggest that local populations of STN neurons can be synchronized by both direct and indirect cortical inputs. Synchronized ensemble activity is dependent on topography and input intensity. Finally, the stereotypical, multiphasic profile of the evoked LFP indicates that it might be useful for locating the STN in clinical as well as nonclinical settings.
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