Patch-clamp recordings in a whole-cell mode were performed on dorsal sensory cells enzymatically isolated from the spinal cord of two lamprey species, Ichthyomyzon unicuspis and Lampetra fluviatilis. The voltage- activated currents through calcium channels were analysed. GABA and the specific GABA(B) receptor agonist baclofen reduced the peak amplitude of inward Ba2+current, as a robust alternate charge carrier through voltage- dependent Ca2+channels. These effects were dose-dependent and reversible. GABA(B) receptor antagonists, 2-hydroxysaclofen and δ-amino-n-valeric acid, blocked the reduction of Ba2+currents by GABA and baclofen, while bicuculline, a GABA(A) receptor antagonist, had no blocking action. GABA and baclofen did not modify the dorsal sensory cell membrane conductance, indicating that they did not activate ligand-gated channels. However, GABA, but not baclofen, considerably increased membrane conductance and induced Cl-currents in isolated multipolar neurons (presumably interneurons and/or motoneurons). These findings suggest that GABA and baclofen action of lamprey dorsal sensory cells is mediated by GABA(B) receptors. We concluded that GABA-mediated presynaptic inhibition of lamprey dorsal sensory cell fibers results from GABA(B) receptor activation followed by a decrease of inward voltage-activated calcium currents. Appositions of GABA-immunoreactive boutons to horseradish peroxidase-labeled fibers from the dorsal root were observed at the ultrastructural level in the dorsal column using postembedding immunogold cytochemistry. It seems likely that these appositions represent the morphological substrate of dorsal sensory cell fiber presynaptic inhibition. In very rare cases, ultrastructural features were observed which would be interpreted as synaptic specializations between the GABA-immunoreactive boutons and the primary afferent fibers. The extrasynaptic action of GABA as a basis of presynaptic inhibition of this population of primary afferent neurons is discussed.
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