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The Journal of Neurophysiology Vol. 81 No. 5 May 1999, pp. 2046-2055
Copyright ©1999 by the American Physiological Society
1Experimental Therapeutics Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892; and 2Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan
Ruskin, David N.,
Debra A. Bergstrom,
Yoshiki Kaneoke,
Bindu N. Patel,
Michael J. Twery, and
Judith R. Walters.
Multisecond Oscillations in Firing Rate in the Basal Ganglia:
Robust Modulation by Dopamine Receptor Activation and Anesthesia. J. Neurophysiol. 81: 2046-2055, 1999.
Multisecond oscillations in firing rate in the basal ganglia:
robust modulation by dopamine receptor activation and anesthesia. Studies of CNS electrophysiology have suggested an important
role for oscillatory neuronal activity in sensory perception,
sensorimotor integration, and movement timing. In extracellular
single-unit recording studies in awake, immobilized rats, we have found
that many tonically active neurons in the entopeduncular nucleus
(n = 15), globus pallidus (n = 31), and
substantia nigra pars reticulata (n = 31) have slow
oscillations in firing rate in the seconds-to-minutes range. Basal
oscillation amplitude ranged up to ±50% of the mean firing rate.
Spectral analysis was performed on spike trains to determine whether
these multisecond oscillations were significantly periodic. Significant
activity in power spectra (in the 2- to 60-s range of periods) from
basal spike trains was found for 56% of neurons in these three nuclei.
Spectral peaks corresponded to oscillations with mean periods of ~30
s in each nucleus. Multisecond baseline oscillations were also found in
21% of substantia nigra dopaminergic neurons. The dopamine agonist
apomorphine (0.32 mg/kg iv, n = 10-15) profoundly
affected multisecond oscillations, increasing oscillatory frequency
(means of spectral peak periods were reduced to ~15 s) and increasing
the regularity of the oscillations. Apomorphine effects on oscillations
in firing rate were more consistent from unit to unit than were its
effects on mean firing rates in the entopeduncular nucleus and
substantia nigra. Apomorphine modulation of multisecond periodic
oscillations was reversed by either D1 or D2
antagonists and was mimicked by the combination of selective D1 (SKF 81297) and D2 (quinpirole) agonists.
Seventeen percent of neurons had additional baseline periodic activity
in a faster range (0.4-2.0 s) related to ventilation. Multisecond
periodicities were rarely found in neurons in anesthetized rats
(n = 29), suggesting that this phenomenon is sensitive
to overall reductions in central activity. The data demonstrate
significant structure in basal ganglia neuron spiking activity at
unexpectedly long time scales, as well as a novel effect of dopamine on
firing pattern in this slow temporal domain. The modulation of
multisecond periodicities in firing rate by dopaminergic agonists
suggests the involvement of these patterns in behaviors and cognitive
processes that are affected by dopamine. Periodic firing rate
oscillations in basal ganglia output nuclei should strongly affect the
firing patterns of target neurons and are likely
involved in coordinating neural activity responsible for motor
sequences. Modulation of slow, periodic oscillations in firing rate may
be an important mechanism by which dopamine influences motor and
cognitive processes in normal and dysfunctional states.
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