Amphetamine-induced behavioral activation is associated with variable changes in basal ganglia output neurons recorded from awake, behaving rats

Joshua M. Gulley, Jamie L. Reed, Masaaki Kuwajima, George V. Rebec

Research output: Contribution to journalArticle

Abstract

Systemic or intra-striatal administration of d-amphetamine (AMPH) elicits a dose-dependent pattern of behavioral activation and neuronal firing in the striatum. To determine if the AMPH-induced striatal firing pattern is expressed in the substantia nigra pars reticulata (SNr), a main target of striatal efferents and the primary output nucleus of the basal ganglia, we recorded the activity of 214 SNr units in alert, behaving rats responding to either systemic (1.0 or 5.0 mg/kg, sc) or intra-striatal (20 μg/μl/min) AMPH. Both routes of administration increased behavior but the strongest effects occurred after systemic injection. A dose of 1.0 mg/kg progressively increased locomotion, head movements, and sniffing, whereas after 5.0 mg/kg behavioral responding became progressively more focused and stereotyped. The collective response of SNr neurons was a net increase in firing rate that was most apparent after the low systemic dose and intra-striatal infusion. Further analysis revealed significant unit populations that were either excited, inhibited or showed no change. Although excitations predominated over inhibitions in all cases, a sizable population of units was unresponsive: ∼25% to systemic AMPH and almost half to intra-striatal infusion. Subsequent injection of haloperidol (0.5 or 1.0 mg/kg, sc), a dopamine receptor antagonist, reversed both the behavioral and electrophysiological effects of AMPH. Thus, as in striatum, dopamine appears to play a critical role in AMPH-induced changes in SNr activity. Interestingly, however, SNr activity did not closely parallel the striatal response, suggesting that patterns of neuronal responding to AMPH in striatum are not reliably relayed to SNr.

Original languageEnglish (US)
Pages (from-to)108-118
Number of pages11
JournalBrain Research
Volume1012
Issue number1-2
DOIs
StatePublished - Jun 25 2004
Externally publishedYes

Keywords

  • Behaving rat
  • Drugs of abuse: amphetamine and other stimulants
  • Electrophysiology
  • Neural basis of behavior
  • Stereotypy
  • Striatum
  • Substantia nigra pars reticulata

ASJC Scopus subject areas

  • Neuroscience(all)
  • Molecular Biology
  • Clinical Neurology
  • Developmental Biology

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