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Brain oscillations reveal impaired novelty detection from early stages of Parkinson's disease.

ABSTRACT: The identification of reliable biomarkers for early diagnosis and progression tracking of neurodegenerative diseases has become an important objective in clinical neuroscience in the last years. The P3a event-related potential, considered as the neurophysiological hallmark of novelty detection, has been shown to be reduced in Parkinson's disease (PD) and proposed as a sensitive measure for illness duration and severity. Our aim for this study was to explore for the first time whether impaired novelty detection could be observed through phase- and time-locked brain oscillatory activity at early PD. Twenty-seven patients with idiopathic PD at early stages (disease duration <5?years and Hoehn and Yahr stage <3) were included. A healthy control group (n?=?24) was included as well. All participants performed an auditory involuntary attention task including frequent and deviant tones while a digital EEG was obtained. A neuropsychological battery was administered as well. Time-frequency representations of power and phase-locked oscillations and P3a amplitudes were compared between groups. We found a significant reduction of power and phase locking of slow oscillations (3-7?Hz) for deviant tones in the PD group compared to controls in the P3a time range (300-550?ms). Also, reduced modulation of late induced (not phase locked) alpha-beta oscillations (400-650?ms, 8-25?Hz) was observed in the PD group after deviant tones onset. The P3a amplitude was predicted by years of evolution in the PD group. Finally, while phase-locked slow oscillations were associated with task behavioral distraction effects, induced alpha-beta activity was related to cognitive flexibility performance. Our results show that novelty detection impairment can be identified in neurophysiological terms from very early stages of PD, and such impairment increases linearly as the disease progresses. Also, induced alpha-beta oscillations underlying novelty detection are related to executive functioning.

SUBMITTER: Solis-Vivanco R

PROVIDER: S-EPMC5988040 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Brain oscillations reveal impaired novelty detection from early stages of Parkinson's disease.

Solís-Vivanco Rodolfo R Rodríguez-Violante Mayela M Cervantes-Arriaga Amín A Justo-Guillén Edith E Ricardo-Garcell Josefina J

NeuroImage. Clinical 20180322

The identification of reliable biomarkers for early diagnosis and progression tracking of neurodegenerative diseases has become an important objective in clinical neuroscience in the last years. The P3a event-related potential, considered as the neurophysiological hallmark of novelty detection, has been shown to be reduced in Parkinson's disease (PD) and proposed as a sensitive measure for illness duration and severity. Our aim for this study was to explore for the first time whether impaired no ...[more]

PMID: 29876277

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Project description:Background:Different oscillations of brain networks could carry different dimensions of brain integration. We aimed to investigate oscillation-specific nodal alterations in patients with Parkinson's disease (PD) across early stage to middle stage by using graph theory-based analysis. Methods:Eighty-eight PD patients including 39 PD patients in the early stage (EPD) and 49 patients in the middle stage (MPD) and 36 controls were recruited in the present study. Graph theory-based network analyses from three oscillation frequencies (slow-5: 0.01-0.027?Hz; slow-4: 0.027-0.073?Hz; slow-3: 0.073-0.198?Hz) were analyzed. Nodal metrics (e.g. nodal degree centrality, betweenness centrality and nodal efficiency) were calculated. Results:Our results showed that (1) a divergent effect of oscillation frequencies on nodal metrics, especially on nodal degree centrality and nodal efficiency, that the anteroventral neocortex and subcortex had high nodal metrics within low oscillation frequencies while the posterolateral neocortex had high values within the relative high oscillation frequency was observed, which visually showed that network was perturbed in PD; (2) PD patients in early stage relatively preserved nodal properties while MPD patients showed widespread abnormalities, which was consistently detected within all three oscillation frequencies; (3) the involvement of basal ganglia could be specifically observed within slow-5 oscillation frequency in MPD patients; (4) logistic regression and receiver operating characteristic curve analyses demonstrated that some of those oscillation-specific nodal alterations had the ability to well discriminate PD patients from controls or MPD from EPD patients at the individual level; (5) occipital disruption within high frequency (slow-3) made a significant influence on motor impairment which was dominated by akinesia and rigidity. Conclusions:Coupling various oscillations could provide potentially useful information for large-scale network and progressive oscillation-specific nodal alterations were observed in PD patients across early to middle stages.

Project description:Introduction Subthalamic Deep Brain Stimulation (STN-DBS) is a safe and well-established therapy for the management of motor symptoms refractory to best medical treatment in patients with Parkinson's disease (PD). Early intervention is discussed especially for Early-onset PD (EOPD) patients that present with an age of onset ≤ 45–50 years and see themselves often confronted with high psychosocial demands. Methods We retrospectively assessed the effect of STN-DBS at 12 months follow-up (12-MFU) in 46 EOPD-patients. Effects of stimulation were evaluated by comparison of disease-specific scores for motor and non-motor symptoms including impulsiveness, apathy, mood, quality of life (QoL), cognition before surgery and in the stimulation ON-state without medication. Further, change in levodopa equivalent dosage (LEDD) after surgery, DBS parameter, lead localization, adverse and serious adverse events as well as and possible additional clinical features were assessed. Results PD-associated gene mutations were found in 15% of our EOPD-cohort. At 12-MFU, mean motor scores had improved by 52.4 ± 17.6% in the STIM-ON/MED-OFF state compared to the MED-OFF state at baseline (p = 0.00; n = 42). These improvements were accompanied by a significant 59% LEDD reduction (p < 0.001), a significant 6.6 ± 16.1 points reduction of impulsivity (p = 0.02; n = 35) and a significant 30 ± 50% improvement of QoL (p = 0.01). At 12-MFU, 9 patients still worked full- and 6 part-time. Additionally documented motor and/or neuropsychiatric features decreased from n = 41 at baseline to n = 14 at 12-MFU. Conclusion The present study-results demonstrate that EOPD patients with and without known genetic background benefit from STN-DBS with significant improvement in motor as well as non-motor symptoms. In line with this, patients experienced a meaningful reduction of additional neuropsychiatric features. Physicians as well as patients have an utmost interest in possible predictors for the putative DBS outcome in a cohort with such a highly complex clinical profile. Longitudinal monitoring of DBS-EOPD-patients over long-term intervals with standardized comprehensive clinical assessment, accurate phenotypic characterization and documentation of clinical outcomes might help to gain insights into disease etiology, to contextualize genomic information and to identify predictors of optimal DBS candidates as well as those in danger of deterioration and/or non-response in the future.

Project description:The disruption of pathologically enhanced beta oscillations is considered one of the key mechanisms mediating the clinical effects of deep brain stimulation on motor symptoms in Parkinson's disease. However, a specific modulation of other distinct physiological or pathological oscillatory activities could also play an important role in symptom control and motor function recovery during deep brain stimulation. Finely tuned gamma oscillations have been suggested to be prokinetic in nature, facilitating the preferential processing of physiological neural activity. In this study, we postulate that clinically effective high-frequency stimulation of the subthalamic nucleus imposes cross-frequency interactions with gamma oscillations in a cortico-subcortical network of interconnected regions and normalizes the balance between beta and gamma oscillations. To this end we acquired resting state high-density (256 channels) EEG from 31 patients with Parkinson's disease who underwent deep brain stimulation to compare spectral power and power-to-power cross-frequency coupling using a beamformer algorithm for coherent sources. To show that modulations exclusively relate to stimulation frequencies that alleviate motor symptoms, two clinically ineffective frequencies were tested as control conditions. We observed a robust reduction of beta and increase of gamma power, attested in the regions of a cortical (motor cortex, supplementary motor area, premotor cortex) and subcortical network (subthalamic nucleus and cerebellum). Additionally, we found a clear cross-frequency coupling of narrowband gamma frequencies to the stimulation frequency in all of these nodes, which negatively correlated with motor impairment. No such dynamics were revealed within the control posterior parietal cortex region. Furthermore, deep brain stimulation at clinically ineffective frequencies did not alter the source power spectra or cross-frequency coupling in any region. These findings demonstrate that clinically effective deep brain stimulation of the subthalamic nucleus differentially modifies different oscillatory activities in a widespread network of cortical and subcortical regions. Particularly the cross-frequency interactions between finely tuned gamma oscillations and the stimulation frequency may suggest an entrainment mechanism that could promote dynamic neural processing underlying motor symptom alleviation.

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Brain oscillations reveal impaired novelty detection from early stages of Parkinson's disease.

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Brain oscillations reveal impaired novelty detection from early stages of Parkinson's disease.

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