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The Journal of Neuroscience, April 15, 2001, 21(8):2851-2860

Modulation of Hippocampal and Amygdalar-Evoked Activity of Nucleus Accumbens Neurons by Dopamine: Cellular Mechanisms of Input Selection

Stan B. Floresco¹, Charles D. Blaha², Charles R. Yang³, and Anthony G. Phillips¹

¹ Department of Psychology, University of British Columbia Vancouver, British Columbia, Canada V6T 1Z4, ² Department of Psychology, Macquarie University, Sydney, New South Wales, Australia 2109, and ³ Eli Lilly Company, Neuroscience Research, Lilly Corporate Center, Indianapolis, Indiana 46285-0510

Inputs from multiple sites in the telencephalon, including the hippocampus and basolateral amygdala (BLA), converge on neurons in the nucleus accumbens (NAc), and dopamine (DA) is believed to play an essential role in the amplification and gating of these different limbic inputs. The present study used extracellular single-unit recordings of NAc neurons in combination with chronoamperometric sampling of mesoaccumbens DA efflux to assess the importance of DA in the integration of different limbic inputs to the NAc. Tetanic stimulation of the fimbria potentiated hippocampal-evoked firing activity of NAc neurons and increased DA extracellular levels. Systemic administration of the D₁ receptor antagonist SCH23390 or the NMDA receptor antagonist CPP abolished the potentiation of hippocampal-evoked activity and produced a D₂ receptor-mediated suppression of evoked firing. In neurons that received converging input from the hippocampus and BLA, fimbria tetanus potentiated hippocampal-evoked firing activity and suppressed BLA-evoked activity in the same neurons. Both D₁ and NMDA receptors participated in the potentiation of fimbria-evoked activity, whereas the suppression of BLA-evoked activity was blocked by either D₁ receptor antagonism with SCH23390 or the adenosine A₁ antagonist 8-cyclopentyl-1,2-dimethylxanthine. Coincidental tetanus of both the fimbria and BLA resulted in potentiation of both inputs, indicating that DA and adenosine-mediated suppression of BLA-evoked firing was activity-dependent. These data suggest that increases in mesoaccumbens DA efflux by hippocampal afferents to the NAc play a critical role in an input selection mechanism, which can ensure preferential responding to the information conveyed from the hippocampus to the ventral striatum.

Key words: nucleus accumbens; hippocampus; basolateral amygdala; dopamine; NMDA; adenosine; gating

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Copyright © 2001 Society for Neuroscience  0270-6474/01/2182851-10$05.00/0

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