Antidromic firing occurs spontaneously on thalamic relay neurons: triggering of ectopic action potentials by somatic intrinsic burst discharges.

Possible dynamic relationships between orthodromically conducted somatic bursts and antidromic impulses arising from presynaptic endings of thalamocortical neurons were explored. Evoked or spontaneous bursts were recorded from 125 identified thalamic relay neurons in 36 anesthetized rats using extracellular microelectrodes. Evoked bursts were obtained by electrical stimulation of either the neocortex or the peripheral activation field. Spontaneous antidromic firing appeared only during periods of (or an expected) rapid somatic intrinsic burst discharge. Ectopic axonal impulses occurred either separately, or clustered in doublets or triplets having relatively long-lasting intervals; these slow bursts represented a proportion of about 12% of evoked and 20% of spontaneous whole bursts. Separate ectopic action potentials could also appear several milliseconds after rapid bursts, producing peculiar long last-interval bursts; about 15% of the whole bursts were of this long interval type. The probability that an ectopic axonal impulse will occur after a rapid burst increases with the number of its action potentials, suggesting that the duration of orthodromic burst firing might contribute to the triggering of ectopic impulses. For 52% of the neurons tested, the activation threshold of their axon terminals decreased just before or immediately after rapid somatic bursts. Since no excitability changes were observed in thalamocortical axons of the white matter, the ectopic action potential generators were probably located on presynaptic endings. During a transient deafferentation of thalamic neurons induced by intrathalamic microinjection of a magnesium solution, neither burst activity nor spontaneous antidromic firing were observed, suggesting that thalamic orthodromic burst discharges are required for presynaptic impulse generation. In conclusion, somatic intrinsic bursts traveling orthodromically along thalamocortical axons might be involved in triggering presynaptic impulses on parent and possibly on nearby thalamic cells. Since a spontaneous antidromic action potential is able to trigger a rapid burst [Pinault (1988) Eur. J. Neurosci. Suppl. P. 246; Pinault and Pumain (1989) Neuroscience 31, 625-637], it is postulated that excitatory interactions between presynaptic endings might be involved in intrinsic burst synchronization processes.