Extracellular potassium accumulation in the frog spinal cord induced by stimulation of the skin and ventrolateral columns

Abstract

1. Changes in extracellular K(+) concentration (Delta[K](e)), dorsal root potentials (DRPs) and single unit activity were studied in the frog spinal cord in response to stimulation of the skin of the hindlimb by touch, pressure, hot water (heat), single electrical pulses and to stimulation of the ventrolateral columns (LC).2. Single electrical pulses, various types of adequate stimulation applied to the skin of the hind limb for 1-2 s as well as single volleys of LC led to a Delta[K](e) of up to 0.2 mmol.l(-1). Stimuli which evoked larger Delta[K](e) also produced larger DRPs in the same frog preparation.3. The briefest heat stimuli, which lasted about 1-2 s, led to more prolonged activity in dorsal horn interneurones than did a single volley or a single tactile stimulus and the Delta[K](e) were longer and larger and had a slower rise time.4. The ;slow' second component of dorsal root depolarization (presumably mediated by K(+)) was observed after electrical and heat stimulation of the skin on the hind limb corresponding to the time course of Delta[K](e).5. The maximum Delta[K](e) induced by nociceptive stimulation occurred in the grey matter of the dorsal horn at a depth of 300-600 mum from the dorsal surface. The maximum response to single stimuli applied to the skin occurred at a depth of 400-800 mum, while that evoked by LC stimulation in the ventral horn at a depth of 1000-1400 mum.6. Repetitive and more prolonged nociceptive stimulation (5-20 s) produced a Delta[K](e) of up to 1 mmol.l(-1). The Delta[K](e) in response to repetitive tactile stimulation does not exceed 0.2 mmol.l(-1). Repetitive stimulation (100 Hz) of LC fibres led to an increase in [K](e) of up to 9-10 mmol.l(-1) in the ventral horn; this level was similar to that achieved in the intermediate region by electrical repetitive stimulation of the skin (100 Hz). Tetanic stimulation of the ventral root led to a Delta[K](e) of only about 0.05 mmol.l(-1) at a depth of 500-700 mum and no measurable Delta[K](e) within the ventral horn.7. Spontaneous Delta[K](e) associated with spontaneous DRPs and VRPs were observed during the decay phase of Delta[K](e) at various intervals from several seconds to one minute after nociceptive or electrical stimulation of the skin, suggesting the occurrence of a longlasting increase in excitability.8. The depolarization of dorsal root fibres evoked by nociceptive stimulation, tetanic stimulation of the LC and single or tetanic stimulation of the skin was followed by a dorsal root hyperpolarization. Its size, as well as that of Delta[K](e), was dependent on the frequency and duration of stimulation and its time course correlated with the dissipation of Delta[K](e) when stimulation was discontinued.9. It is suggested that the extracellular K(+) accumulation could, under physiological conditions, contribute to the modulation of spinal cord transmission, acting both pre-and post-synaptically. Low levels of increased [K](e) were associated with facilitation of impulse transmission while higher increases could result in its inhibition.