The origin of rhythmic fast subthreshold depolarizations in thalamic relay cells of rats under urethane anaesthesia

Abstract

Intracellular recordings were performed in relay neurons of the dorsal thalamus in rats under urethane anaesthesia. In 77 out of 127 neurons of the ventro-posterolateral and ventral lateral nuclei, but not in neurons of the ventro-posteromedial and posterior nuclei, a highly rhythmic pattern of subthreshold depolarization was present at rest. The average frequency of these rhythmic depolarizations in ventro-posterolateral cell was 23.36±11.48 Hz (range: 6–60 Hz); in ventral lateral relay cells higher frequencies were observed (65.86±17.42 Hz; range: 17–95 Hz). The rhythmic subthreshold events were identified as excitatory postsynaptic potentials generated by the regular firing of prethalamic afferents located in dorsal column and deep cerebellar nuclei. Indeed, in cells of the ventro-posterolateral nucleus these spontaneous potentials had a waveform similar to that synaptic potentials trigged by somatosensory stimulation. They increased in amplitude with membrane hyperpolarization and their rhythmic occurrence was not affected by the injection of large inward currents. Moreover, they persisted after capsular transection, but they could no more be recorded in ventro-posterolateral cells after lesion of dorsal column nuclei. Finally, it was found that prethalamic afferents within the deep cerebellar nuclei discharged spontaneously in a rhythmic manner within the same frequency band as that of the rhythmic synaptic potentials recorded in ventral lateral cells. On the basis of these results, it is concluded that the rhythmic subthreshold depolarization observed in thalamic neurons of animals under urethane anaesthesia are not generated intrinsically but that they represent excitatory postsynaptic potentials of prethalamic origin. The rhythmic nature of these synaptic potentials demonstrates that neurons of the dorsal column and deep cerebellar nuclei are capable of encoding rhythmically their output. In the context of results already published on the origin of fast oscillations in the brain, this intriguing observation should deserve further attention as much as a similar rhythm has previously been reported for retinal ganglion cells in non-anaesthetized or lightly anaesthetized animals.