Locomotor-Related Presynaptic Modulation of Primary Afferents in the Lamprey

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Abstract
Presynaptic modulation of sensory afferent transmission during rhythmic motor activity was investigated in the lamprey spinal cord in vitro. Intracellular recordings were performed from the somata and axons of the glutamatergic sensory neurons from the skin (dorsal cells) during locomotor activity induced by N-methyl-D-aspartate (NMDA). Dorsal cells were phasically depolarized during each ipsilateral ventral root burst. In some soma recordings no or only small amplitude depolarizations were seen, although intracellular recording of their axons revealed the existence of large depolarizations, suggesting that the input synapses are located on the axons. The amplitude of the depolarizations increased during intracellular injection of hyperpolarizing current. The amplitude of the depolarizations increased when the frequency of the locomotor rhythm was increased by elevating the NMDA concentration. The depolarizations were not blocked by specific GABA(A) (bicuculline) or GABA(B) (phaclofen and saclofen) antagonists. To investigate whether the phasic depolarization may influence the monosynaptic excitatory transmission to giant interneurons, the amplitude of the monosynaptic excitatory postsynaptic potential (EPSP) was compared between the onset of the ipsilateral locomotor burst and the burst mid-point. The compound monosynaptic EPSP evoked from dorsal column was significantly smaller during the peak depolarization than at burst onset. The reduction of the amplitude of the EPSPs was not associated with any change of the membrane potential or input resistance of the giant interneurons, suggesting that this effect is mediated by a presynaptic mechanism. Phase-dependent effects were also seen on burst and cycle duration following dorsal column stimulation. Thus, the locomotor-related depolarizations in dorsal cell axons may represent a mechanism for a phasic gain control of sensory transmission during fictive locomotion.