Corticostriatal Beta Power Changes Associated with Cognitive Function in Parkinson’s Disease

Abstract

Cognitive impairment (CI) is the most frequent nonmotor symptom in Parkinsons Disease (PD) and is associated with deficits in executive functions such as working memory. Previous studies have demonstrated that caudate beta power underlies learning and working memory. Decreased dopamine in motor cortico-striato-thalamo-cortical (CSTC) circuits results in increased beta power and PD motor symptoms. Analogous changes in cognitive CSTC circuits, including the caudate and dorsolateral prefrontal cortex (DLPFC), may contribute to PD CI. A better understanding of anatomic structures and neurophysiologic changes associated with working memory deficits is needed to develop potential neuromodulatory treatment strategies for PD CI. The objective of our study is to evaluate neurophysiologic changes underlying cognitive dysfunction in PD patients via direct local field potential recordings during deep brain stimulation surgery. Fifteen patients were included, one of which completed 2 minutes of resting state data collection while the other fourteen completed resting state collection and task based data collection with a verbal working memory 2-back task with feedback. LFP signals from DLPFC (50 channels) and caudate (25 channels) were sampled at 1000Hz, demeaned by channel and aligned to task events of encoding and feedback. Correlations of resting state beta power and pre-operative neuropsychological testing as well as caudate volumes were performed. Beta power decreased in both DLPFC and caudate during encoding and was significantly different for correct and incorrect trials, whereas beta power increased in DLPFC and caudate during feedback and was significantly different for correct and incorrect trials. Beta power during encoding was inversely correlated with memory scores on pre-operative neuropsychological testing. Understanding neurophysiologic correlates of cognitive dysfunction within cognitive CSTC circuits will aid in development of novel neuromodulatory therapies for patients with PD CI and other cognitive disorders.

Cortical beta oscillations map to shared brain networks modulated by dopamine

“…Our results motivate to conceptualise the capacity to generate beta oscillations as a feature that arises from a large-scale global brain network that is modulated by dopamine. However, we do not see this concept as contradictory to previous reports of functional correlates of beta activity in the domains of motor control, cognition, memory and emotion 3,6,7,22 . Instead, we believe that the overlap in oscillatory activity across these domains can be conceptualised through a circuit definition of beta activity and its relationship to dopamine signalling.…”

“…Oscillatory neural activity is proposed to orchestrate brain function, by providing multilateral rhythmic synchronisation of neural excitability and action potential firing 1 . One prominent example in the human brain is the beta rhythm (13 – 35 Hz), which has traditionally been described as a phenomenon of the motor domain, primarily localised to motor cortex and important for the pathophysiology of movement disorders, such as Parkinson’s disease (PD) 2,3 . In PD, beta activity, especially in deeper brain structures, such as the basal ganglia, has been associated with the loss of innervation with dopamine 4 , a neurotransmitter critically involved in synaptic plasticity and reinforcement learning at cortico-striatal synapses 5 .…”

“…This relationship is mirrored in rodent and nonhuman primate models of PD, corroborating the role of dopamine as a key neurotransmitter governing beta synchrony. Meanwhile, the putative function of beta modulation in both human and animal literature has been extended within and beyond PD, to diverse domains of cognition 3 , memory 6 and emotions 7 , but only few studies so far have sought to relate these observations to dopamine signalling. For each of these domains, localised synchronisation or desynchronisation phenomena in the beta frequency range have been described in specific brain regions.…”

Transcranial Ultrasound Stimulation Improves Memory Performance of Parkinsonian Mice

“…Research shows that there is a close relationship between working memory and neural oscillations (such as theta frequency band/gamma frequency band) in the cortex/hippocampus/subthalamic nucleus and other brain areas [6], [7]. For example, in Parkinson's patients, the spectral power of beta oscillations in the prefrontal cortex and caudate nucleus decreases during working memory encoding, while the spectral power of these structures increases during feedback [8], [9]. There are also studies proving that changes in neural oscillations in the alpha and theta frequency bands of the parietal lobe are related to sequential working memory in Parkinson's disease.…”

Depression Attenuates Caudate and Dorsolateral Prefrontal Cortex Alpha and Beta Power Response to Reward

“…Previous work has shown that beta band neural oscillations in the caudate and DLPFC increase during reward-related feedback of cognitive tasks in human subjects. [37][38][39] However, whether these corticostriatal reward-related neural oscillations are altered in depression is not known. Moreover, how reward and emotional processing may interact is not well understood.…”