Alpha oscillations in the pedunculopontine nucleus correlate with gait performance in parkinsonism

Abstract

The pedunculopontine nucleus, a component of the reticular formation, is topographically organized in animal models and implicated in locomotor control. In Parkinson's disease, pedunculopontine nucleus stimulation is an emerging treatment for gait freezing. Local field potentials recorded from pedunculopontine nucleus electrodes in such patients have demonstrated oscillations in the alpha and beta frequency bands, reactive to self-paced movement. Whether these oscillations are topographically organized or relevant to locomotion is unknown. Here, we recorded local field potentials from the pedunculopontine nucleus in parkinsonian patients during rest and unconstrained walking. Relative gait speed was assessed with trunk accelerometry. Peaks of alpha power were present at rest and during gait, when they correlated with gait speed. Gait freezing was associated with attenuation of alpha activity. Beta peaks were less consistently observed across rest and gait, and did not correlate with gait speed. Alpha power was maximal in the caudal pedunculopontine nucleus region and beta power was maximal rostrally. These results indicate a topographic distribution of neuronal activity in the pedunculopontine nucleus region and concur with animal data suggesting that the caudal subregion has particular relevance to gait. Alpha synchronization, proposed to suppress ‘task irrelevant’ distraction, has previously been demonstrated to correlate with performance of cognitive tasks. Here, we demonstrate a correlation between alpha oscillations and improved gait performance. The results raise the possibility that stimulation of caudal and rostral pedunculopontine nucleus regions may differ in their clinical effects.

Imagined gait modulates neuronal network dynamics in the human pedunculopontine nucleus

“…Alpha band LFP activity in the PPN 33, 35 increases during locomotion 35 . In agreement, LFP alpha power in the caudal PPN increased during limb movement.…”

“…Active gait is accompanied by increased LFP alpha power in the caudal PPN 35 . In agreement, we also find that alpha power was significantly higher relative to beta power in caudal PPN (Fig.…”

“…Local field potential (LFP) recordings from the PPN have reported oscillations in both the alpha (6-12Hz) and beta (12-30Hz) frequency bands 33,[35][36][37] , with relatively higher alpha power in caudal-PPN, and higher beta power in the rostral-PPN 35 . Active gait is accompanied by increased LFP alpha power in the caudal PPN 35 .…”

“…During imagined gait, the effects on alpha and beta LFP power were smaller (Fig 3b), but the overall change in alpha/beta power ratio was similar to that seen during passive movement, with an increase from 1.99 ± 0.40 to 2.58 ± 0.53 (n=22). The LFP results in part from local neuronal activity 35 , and we next tested the relationship between unit activity and LFP oscillations. At rest, 75 of 695 neurons tested were significantly phase locked in the alpha (6-12 Hz) frequency band (Rayleigh test p< 0.01; Fig.…”

“…Limb movement and imagined gait changed the patterns of correlated activity, establishing distinct network states during limb movement and imagined gait. These results suggest that the PPN is not simply a relay station between the basal ganglia and spinal cord CPGs but also plays a role in gait initiation.Alpha band LFP activity in the PPN 33, 35 increases during locomotion 35 . In agreement, LFP alpha power in the caudal PPN increased during limb movement.…”