Gamma activity and reactivity in human thalamic local field potentials

Abstract

Depth recordings in patients with Parkinson's disease on dopaminergic therapy have revealed a tendency for oscillatory activity in the basal ganglia that is sharply tuned to frequencies of approximately 70 Hz and increases with voluntary movement. It is unclear whether this activity is essentially physiological and whether it might be involved in arousal processes. Here we demonstrate an oscillatory activity with similar spectral characteristics and motor reactivity in the human thalamus. Depth signals were recorded in 29 patients in whom the ventral intermediate or centromedian nucleus were surgically targeted for deep brain stimulation. Thirteen patients with four different pathologies showed sharply tuned activity centred at approximately 70 Hz in spectra of thalamic local field potential (LFP) recordings. This activity was modulated by movement and, critically, varied over the sleep-wake cycle, being suppressed during slow wave sleep and re-emergent during rapid eye movement sleep, which physiologically bears strong similarities with the waking state. It was enhanced by startle-eliciting stimuli, also consistent with modulation by arousal state. The link between this pattern of thalamic activity and that of similar frequency in the basal ganglia was strengthened by the finding that fast thalamic oscillations were lost in untreated parkinsonian patients, paralleling the behaviour of this activity in the basal ganglia. Furthermore, there was sharply tuned coherence between thalamic and pallidal LFP activity at approximately 70 Hz in eight out of the 11 patients in whom globus pallidus and thalamus were simultaneously implanted. Subcortical oscillatory activity at approximately 70 Hz may be involved in movement and arousal.

Striatal cholinergic interneurons generate beta and gamma oscillations in the corticostriatal circuit and produce motor deficits

“…Finely tuned gamma oscillations in the range of 60-90 Hz are a consistent feature of basal ganglia and thalamic recordings (47) that are diminished in PD patients in the absence of dopaminergic replacement (17,18). However, rather than an increase in finely tuned gamma, here we observed a broader-band gamma power increase, which may represent a general increase in neuronal activity (26).…”

“…To further evaluate the changes at specific frequency bands, we calculated the normalized spectrum before, during, and after laser stimulation. We found that optogenetic stimulation of SChIs robustly increased oscillation power across higher frequency bands conventionally defined as alpha (8)(9)(10)(11)(12)(13)(14)(15), beta (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30), low gamma (30-60 Hz), and high gamma (60-100 Hz), but not lower frequency bands of delta (1-4 Hz) or theta (4-8 Hz) (Fig. 2 E and F; n = 7 mice).…”

“…Similarly, acute reduction of dopamine locally in the striatum increases striatal beta oscillations (16). Systemic dopaminergic drugs decrease beta oscillation power and coherence in PD patients (17), and also increase finely tuned gamma oscillations in the basal ganglia and thalamus, although we know little about the functional significance of these finely tuned gamma oscillations in PD (17,18). Because of the dense innervation of the striatum by the midbrain dopaminergic system (19), we have recently proposed that dopamine may modulate basal ganglia beta oscillations by acting on the striatum, in particular via the striatal cholinergic system.…”

“…When compromised, these circuits contribute to neurological and psychiatric disorders, such as Parkinson's disease (PD). In PD, motor deficits correlate with the emergence of exaggerated beta frequency (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) oscillations throughout the CBT network. However, little is known about how specific cell types within individual CBT brain regions support the generation, propagation, and interaction of oscillatory dynamics throughout the CBT circuit or how specific oscillatory dynamics are related to motor function.…”

“…striatum | optogenetics | beta oscillations | coherence | cholinergic interneurons E xaggerated beta oscillations (15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) within the cortico-basal ganglia-thalamic (CBT) neural network are putative electrophysiological correlates of bradykinesia and rigidity in Parkinson's disease (PD) (1)(2)(3)(4). Therapies that effectively manage PD motor symptoms, such as dopamine replacement therapy and deep brain stimulation, are associated with a suppression of the exaggerated beta oscillations (4,5).…”