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Volume 16, Number 16, Issue of August 15, 1996 pp. 4971-4982
Copyright ©1996 Society for Neuroscience

Multiple Actions of 1S,3R-ACPD in Modulating Endogenous Synaptic Transmission to Spinal Respiratory Motoneurons

Received Feb. 20, 1996; revised May 22, 1996; accepted May 28, 1996.

Xiao-Wei Dong¹, Didier Morin¹, and Jack L. Feldman^{1, 2}

Systems Neurobiology Laboratory, Departments of ¹ Physiological Science and ² Neurobiology, University of California at Los Angeles, Los Angeles, California 90095-1527

To determine physiological roles of metabotropic glutamate receptors (mGluRs) affecting breathing, we examined the effects of (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD) on synaptic transmission and excitability of phrenic motoneurons (PMNs) in an in vitro neonatal rat brainstem/spinal cord preparation. The effects of 1S,3R-ACPD were multiple, including reduction of inspiratory-modulated synaptic currents and increase of neuronal excitability via an inward current (I_acpd) associated with a decrease of membrane conductance. The mechanism underlying synaptic depression was examined. We found that 1S,3R-ACPD reduced the frequency but not the amplitude of miniature excitatory postsynaptic currents. The current induced by exogenous AMPA was not significantly affected by 1S,3R-ACPD. These results suggest that 1S,3R-ACPD-induced reduction of inspiratory synaptic currents is mediated by presynaptic mGluRs. We also examined the ionic basis for I_acpd. We found that I_acpd had a reversal potential of approximately 100 mV, close to the estimated E_K⁺ (95 mV). Elevating extracellular [K⁺] to 9 mM reduced the I_acpd reversal potential to 75 mV. The K⁺ channel blocker Ba²⁺ induced an inward current with a reversal potential at 93 mV associated with a decrease of membrane conductance, closely resembling the effect of 1S,3R-ACPD. Moreover, Ba²⁺ occluded 1S,3R-ACPD effects. In the presence of Ba²⁺, I_acpd and the 1S,3R-ACPD-induced decrease of membrane conductance were diminished. Our data indicate that the dominant component of I_acpd results from the blockade of a Ba²⁺-sensitive resting K⁺ conductance. We conclude that the activation of mGluRs affects the inspiratory-modulated activity of PMNs via distinct mechanisms at pre- and postsynaptic sites.

Key words: 1S,3R-ACPD; metabotropic glutamate receptors; synaptic transmission; presynaptic; excitability; potassium channels; brainstem; spinal cord; phrenic motoneurons; respiration

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