Single unit and beta oscillatory activities in subthalamic nucleus are modulated during visual choice preference

Abstract

Parkinson's disease is a neurodegenerative disease affecting the supply of dopamine to basal ganglia nuclei, leading to pathological beta band (13-35 Hz) oscillations in the subthalamic nucleus (STN). STN and beta activity are recognized in motoric functions but their role in cognitive functions remains elusive. We examined single unit and beta local field potential (LFP) activity in the STN during a visual choice preference task in PD patients (n = 12) undergoing deep brain stimulation surgery. Patients viewed 2 of 5 possible animal picture-pairs and were instructed to choose their favorite ("fav") picture by clicking the left or right mouse key. A block of trials consisted of 50-75 picture-pair presentations. Single unit histograms and LFP spectrograms were aligned to picture presentation and point of decision for pairs that included the fav and non-fav pictures, respectively. A total of 58 neurons from 26 blocks of trials were analyzed. Thirty of 58 neurons showed a selective change in spiking activity 0.20-0.65 s to fav picture presentation, which preceded the shortest recorded reaction time (=0.7 s), and 17/58 neurons showed no significant response in our task. Beta LFP significantly desynchronized in response to fav but not non-fav pictures in all trials, and in 14/26 blocks of trials, the desynchronization was followed by a "beta burst" and ramp-up to baseline activity. Neurons with choice preference responses were found throughout the dorsoventral extent of the STN. STN single units and beta activity are modulated during visual choice preference, and this suggests a role for STN beta activity in cognitive processing.

Anticipatory human subthalamic area beta-band power responses to dissociable tastes correlate with weight gain

“…Reassuringly, Buot et al (2012) found that they could elicit higher magnitude, event-related potentials in the STN to unpleasant vs neutral whether a motor or passive response was required following the image, but the magnitude was larger when paired with a motor response ( Baunez et al, 2005 ). Further, subthalamic beta-band power responses to rewards have been demonstrated in contexts where no motor action was required ( Oswal et al, 2012 ; Al-Ozzi et al, 2020 ). Here, we demonstrate that when trials are time-locked to the taste cue vs the button press, the magnitude of the beta-band power decrease and beta-band rebound are significantly greater for the former, further suggesting role of anticipatory taste processing.…”

Clinical neurophysiology of Parkinson’s disease and parkinsonism

“…Several studies have investigated the properties of STN neurons in PD patients across the spectrum of motor and non-motor activities ( Yin et al, 2021 , Eisinger et al, 2018 ). In particular, there has been much interest in the relationship between beta oscillations in the STN and PD motor symptoms ( Brown, 2006 , Little and Brown, 2014 )(discussed further in section 11.1), and the role of STN beta oscillations in various non-motor or cognitive functional domains ( Al-Ozzi et al, 2021 , Eisinger et al, 2018 , Spitzer and Haegens, 2017 , Alanazi et al, 2021 ). Beta oscillations in the LFP are involved in many cortical processes such as learning and memory, attention and decision making, and it is thought that cortical and subcortical beta activities are of different origins ( Spitzer and Haegens, 2017 ).…”

“…However, the oscillation model suggests that beta oscillations in the STN derives from cortical beta activities ( Brown, 2003 , Hutchison et al, 2004 ). This may explain STN beta modulation during a visual choice preference task where patients had to choose a favorite from pairs of animal pictures ( Al-Ozzi et al, 2021 ). Thus, beta oscillations the STN can also play a role in cognition and may be related to cognitive aspects of PD such as apathy.…”

Mate preference and brain oscillations: Initial romantic attraction is associated with decreases in alpha‐ and lower beta‐band power

“…In contrast, changes in neural oscillations induced by processing individual preference stimuli are less well understood, and the results reported in the current literature are vague. For instance, among the few studies examining the processing of individual preference stimuli, some studies have reported that individual preference stimuli (such as favorite foods) can induce decreases in the power of the lower beta band (13–20 Hz; Al‐Ozzi, Botero‐Posada, Lopez Rios, & Hutchison, 2021; Tashiro et al, 2019), while other studies have reported that individual preference stimuli (i.e., preferred faces) cause a decrease in alpha power (but not beta power) through event‐related desynchronization (ERD; Kang, Kim, Cho, & Kim, 2015). Therefore, the currently ambiguous question regarding whether the processing of individual preference stimuli is related to alpha‐ERD or beta‐ERD responses needs to be further investigated.…”