Patterns of neuronal firing in the human lateral thalamus during sleep and wakefulness

Abstract

The firing patterns of thalamic neurons in mammals undergo a dramatic change as the animal's state changes between sleep and wakefulness. During sleep the normal tonic firing of thalamic neurons changes into a slower bursting mode characterized by repetitive activation of a low-threshold calcium (Ca2+) current. The present report describes the patterns of thalamic neuronal firing during sleep and wakefulness in one human patient. Extracellular single neuron activity was recorded during functional stereotactic surgery in the thalamus of a patient with chronic pain, who was observed to fall asleep during the recording. Evolutive power spectra of the thalamic slow wave were used in place of cortical encephalography to confirm the patient's states of sleep and wakefulness. Twenty-nine sites were observed in motor and somatosensory thalamus (Vop, Vim, and Vc) that were characterized by the presence of neurons with bursting activity when the patient was asleep. Such bursting was not observed in the patient when she was awakened. At 14 of these sites we were able to discriminate the bursting activity of single units. In each case the cell stopped firing or its bursting was replaced by a tonic firing pattern when the patient was awakened. In three cases the patient began to lapse back into sleep and the neuron resumed firing in a bursting pattern once again. None of these units had a peripheral receptive field (RF), while several other units recorded in nearby regions that did not fire in a bursting pattern during sleep had kinesthetic or cutaneous RFs. Analysis of the intraburst firing pattern revealed increasing interspike intervals (ISI) for successive action potentials in a burst and that the duration of the first ISI in the burst decreased as the number of ISIs increased. This pattern is similar to that reported to occur as a result of a calcium spike. These data have confirmed for the first time that state-dependent changes in thalamic firing exist in the human and that the physiological substrates at the thalamic level that are involved in human sleep are similar to those observed in animals.

Thalamic single‐unit and local field potential activity in Tourette syndrome

“…The main reason was that DBS effect is highly dependent on the electrode localization and targets suitable for some pathologies cannot be generally used in other pathologies. In the literature, nevertheless, bursting activity in various thalamic nuclei [ventralis intermediate (VIM), ventralis caudalis (VC), anterior lateral (AL), central lateral (CL)] and in various pathologies (epilepsy, pain, tinnitus, essential tremor, and other abnormal movements) were described and identified as low‐threshold calcium spike bursts 39–43. The results obtained were very close to ours: in essential tremor the interburst interval ranged between 0.17 and 0.39 seconds in the VO and between 0.36 and 0.58 seconds in the VC in awake patients,41 in epilepsy it ranged between 0.172 and 0.361 seconds in the AL in anaesthetized patients,39 in pain and in patients with other abnormal movements ranged between 0.176 and 0.397 seconds in the CL 40.…”

Gain control mechanisms in the nociceptive system

“…4 The thalamus is often considered the gate to the cortex, eg, during wakefulness vs sleep. 43 The transition from wakefulness to sleep leads to a transient functional deafferentation of the cortex, which may share some of its circuitry and neuropharmacology with chronic pain states induced by nerve damage that leads to a more permanent deafferentation. 1 The cortical reorganization observed after amputation 11 is a clinically relevant example of a spatially precise mechanism of gain control in the brain.…”

On the relation between sensory deafferentation, pain and thalamic activity in Wallenberg's syndrome: A PET‐scan study before and after motor cortex stimulation

“…Single unit bursts recorded in the thalamic nuclei of patients with neuropathic pain fulfilled the criteria of low-threshold calcium spikes (LTS), i.e. peculiar rhythmic activities reflecting a state of hyperpolarisation and inhibition at the cellular level, similar to that observed during slow wave sleep (Llinás and Jahnsen, 1982;Lenz et al, 1989;Jeanmonod et al, 1993Jeanmonod et al, , 1994Jeanmonod et al, , 1996Steriade et al, 1993;Tsoukatos et al, 1997;Weng et al, 2003). Furthermore, a direct link between thalamic bursting and reduced metabolic activity was demonstrated by Hirato et al (1994), who obtained both PET-scan and intrathalamic recordings in patients with central post-stroke pain, and showed that the thalamic regions concerned by bursting activity had also reduced glucose metabolism and reduced sensory responses to external stimuli.…”