CENTRAL MODULATION OF STRETCH-RECEPTOR NEURONS DURING FICTIVE LOCOMOTION IN LAMPREY

1. In lamprey, stretch receptor neurons (SRNs), also referred to as ed ge cells, are located along the lateral margin of the spinal cord. The y sense the lateral movements occurring in each swim cycle during loco motion. The isolated lamprey spinal cord in vitro was used to investig ate the activity of SRNs during fictive locomotion induced by bath-app lied N-methyl-D-aspartate (NMDA). Intracellular recordings with potass ium acetate filled electrodes showed that 63% of SRNs had a clear loco motor-related modulation of their membrane potential. 2. Of the modula ted SRNs, two-thirds had periods of alternating excitation and inhibit ion occurring during the ipsilateral and the contralateral ventral roo t bursts, respectively. The phasic hyperpolarization could be reversed into a depolarizing phase after the injection of chloride ions into t he cells; this revealed a chloride-dependent synaptic drive. The remai ning modulated SRNs were inhibited phasically during ipsilateral motor activity. 3. Experiments with barriers partitioning the recording cha mber with the spinal cord into three pools, allowed an inactivation of the locomotor networks within one pool by washing out NMDA from the p ool in which the SRN was recorded. This resulted in a marked reduction , but not an abolishment, of the amplitude of the membrane potential o scillations. Both the excitatory and the inhibitory phases were reduce d, resulting from removal of input from inhibitory and excitatory inte rneurons projecting from the adjacent pools. If the glycine receptor a ntagonist strychnine (1 mu M) was applied in one pool, the phasic hype rpolarizing phase disappeared without affecting the excitatory phase. 4. Bath application of the gamma-aminobutyric acid (GABA)(A) receptor antagonist, bicuculline (50-100 mu M) blocked the spontaneous large un itary inhibitory postsynaptic potentials, which occurred without a cle ar phasic pattern. Bicuculline had no significant effect on the peak t o peak amplitude of the locomotor-related membrane potential oscillati ons. The inhibition in SRNs therefore has a dual origin: glycinergic i nterneurons provide phasic inhibition, while the GABA system can exert a tonic inhibition via GABA(A) receptors. 5. These data show that, in addition to the stretch-evoked excitation, which SRNs receive during each locomotor cycle, most of them also receive excitation from the ce ntral pattern generator network during the ipsilateral contraction, wh ich may ensure a maintained high level of sensitivity to stretch durin g the shortening phase of the locomotor cycle. This arrangement is ana logous to the efferent control of muscle spindles exerted by gamma-mot oneurons in mammals, which as a rule are coactivated with alpha-motone urons to the same muscle (alpha-gamma linkage).