Dopamine depletion can be predicted by the aperiodic component of subthalamic local field potentials

Kim, JinMo; Lee, Jungmin; Kim, Eun‐Ho; Choi, Joon Ho; Rah, Jong‐Cheol; Choi, Ji‐Woong

doi:10.1016/j.nbd.2022.105692

Cited by 27 publications

(38 citation statements)

References 56 publications

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“…Aperiodic exponents of STN-LFPs recorded from awake PD patients are increased ON medication and ON DBS when STN local activity is believed to be decreased according to the classical direct/indirect pathways model (Albin et al, 1989; DeLong, 1990). The increased exponents ON dopaminergic medication in PD are consistent with a recent study that reported higher aperiodic exponents in dopamine-intact compared to lesioned animals (Kim et al, 2022). Furthermore, our results indicate that periodic beta power differs between the two dopaminergic medication states ( Figures 2C ), consistent with previous findings (Kim et al, 2022; Kühn et al, 2006; Neumann et al, 2017; Ray et al, 2008).…”

Section: Discussionsupporting

confidence: 91%

“…The increased exponents ON dopaminergic medication in PD are consistent with a recent study that reported higher aperiodic exponents in dopamine-intact compared to lesioned animals (Kim et al, 2022). Furthermore, our results indicate that periodic beta power differs between the two dopaminergic medication states ( Figures 2C ), consistent with previous findings (Kim et al, 2022; Kühn et al, 2006; Neumann et al, 2017; Ray et al, 2008). Finally, the missing correlation between medication-induced changes of aperiodic exponents and periodic beta power suggests that aperiodic exponents capture changes with medication that are not reflected by beta power alone and might be complimentary in an adaptive DBS algorithm ( Figure 2D and Figure S3 ).…”

Section: Discussionsupporting

confidence: 91%

Section: The Aperiodic Exponent As a Marker Of E/i Balancesupporting

confidence: 93%

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The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism: a cross-species study in vivo

Wiest

Torrecillos

Pogosyan

et al. 2022

Preprint

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Periodic features of neural time series data, such as local field potentials (LFP), are often quantified using power spectra. While the aperiodic exponent of spectra is typically disregarded, it is nevertheless modulated in a physiologically-relevant manner and was recently hypothesised to reflect excitation/inhibition (E/I) balance in neuronal populations. Here, we used a cross-species in vivo electrophysiological approach to test the E/I hypothesis in the context of experimental and idiopathic Parkinsonism. We demonstrate in dopamine-depleted rats that aperiodic exponents and power at 30-100 Hz in subthalamic nucleus (STN) LFPs reflect defined changes in basal ganglia network activity; higher aperiodic exponents tally with lower levels of STN neuron firing and a balance tipped towards inhibition. Using STN-LFPs recorded from awake Parkinson's patients, we show that higher exponents accompany dopaminergic medication and deep brain stimulation (DBS) of STN, consistent with untreated Parkinson's manifesting as reduced inhibition and hyperactivity of STN. These results suggest that the aperiodic exponent of STN-LFPs in Parkinsonism reflects E/I balance, and might be a candidate biomarker for adaptive DBS.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 91%

Section: The Aperiodic Exponent As a Marker Of E/i Balancesupporting

confidence: 93%

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The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism: a cross-species study in vivo

Wiest

Torrecillos

Pogosyan

et al. 2022

Preprint

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“…Recent studies have shown alterations of arhythmic brain activity in PD patients 12,67,68 . Here we show that the arhythmic component of the neurophysiological spectrum can differentiate between individuals and contributes to the association between inter-individual differentiability and motor symptoms.…”

Section: Discussionmentioning

confidence: 99%

The neurophysiological brain-fingerprint of Parkinson’s disease

Castanheira

Wiesman

Hansen

et al. 2023

Preprint

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Brain-fingerprinting is a neuroimaging approach that is expanding the neuroscientific perspective on inter-individual diversity in health and disease. In the present study, we used brain-fingerprinting to advance the neurophysiological characterization of Parkinson's disease (PD). We derived the brain-fingerprints of patients with PD and age-matched healthy controls from the rhythmic and arhythmic spectral features of brief and task-free magnetoencephalography recordings. Using this approach, the individual differentiation of patients against healthy controls is 81% accurate, with the differentiability of patients scaling with the severity of their cognitive and motor symptoms. We show that between-patient differentiation is more challenging (77% accurate) than between healthy controls (90%) because the neurophysiological spectral features of patients with PD are less stable over time. The most distinctive features for differentiating healthy controls map to higher-order regions in the brain functional hierarchy. In contrast, the most distinctive features for patient differentiation map to the somatosensori-motor cortex. We also report that patient brain-fingerprints coincide with the cortical topography of the neurotransmitter systems affected in PD. We conclude that Parkinson's disease affects the spectral brain-fingerprint of patients with remarkable heterogeneity between individuals, and increased variability over short periods of time, compared to age-matched healthy controls. Our study demonstrates the relevance of neurophysiological fingerprinting to clinical neuroscience, and highlights its potential in terms of patient stratification, disease modeling, and the development and evaluation of personalized interventions.

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“…Studies have highlighted its physiological importance, relating it to chronological age, behavioral and cognitive performance, and attention ( Donoghue et al, 2020 ; Thuwal et al, 2021 ; Waschke et al, 2021 ). Other reports correlate it to behavioral readouts in Autism Spectrum Disorder ( Wilkinson and Nelson, 2021 ) and dopamine depletion in Parkinson’s disease ( Kim et al, 2022 ). Moreover, this 1/f component of the signal has been stated to reflect the EIB of neural activity ( Gao et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Glutamatergic and GABAergic Receptor Modulation Present Unique Electrophysiological Fingerprints in a Concentration-Dependent and Region-Specific Manner

Gonzalez-Burgos

Bainier²,

Gross³

et al. 2023

eNeuro

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Brain function depends on complex circuit interactions between excitatory and inhibitory neurons embedded in local and long-range networks. Systemic GABAA-receptor or NMDA-receptor modulation alters the excitatory/inhibitory balance (EIB), measurable with electroencephalography (EEG). However, EEG signatures are complex in localization and spectral composition. We developed and applied analytical tools to investigate the effects of two EIB modulators, MK801 (NMDAR-antagonist) and diazepam (GABAAR-modulator), on periodic and aperiodic EEG features in freely-moving male Sprague-Dawley rats. We investigated how, across three brain regions, EEG features are correlated with EIB modulation. We found that the periodic component was composed of seven frequency bands that presented region- and compound-dependent changes. The aperiodic component was also different between compounds and brain regions. Importantly, the parametrization into periodic and aperiodic components unveiled correlations between quantitative EEG and plasma concentrations of pharmacological compounds. MK-801 exposures were positively correlated with the slope of the aperiodic component. Concerning the periodic component, MK-801 exposures correlated negatively with the peak frequency of low-gamma oscillations but positively with those of high-gamma and high-frequency oscillations. As for the power, theta and low-gamma oscillations correlated negatively with MK-801, whereas mid-gamma correlated positively. Diazepam correlated negatively with the knee of the aperiodic component, positively to beta and negatively to low-gamma oscillatory power, and positively to the modal frequency of theta, low-, mid-, and high-gamma. In conclusion, correlations between exposures and pharmacodynamic effects can be better-understood thanks to the parametrization of EEG into periodic and aperiodic components. Such parametrization could be key in functional biomarker discovery.SIGNIFICANCE STATEMENTExcitatory-inhibitory balance (EIB) is compromised in neurological disorders. Our study demonstrates that pharmacologically-induced effects on EIB can be quantified by decomposing the qEEG PS signal into the oscillatory periodic and the 1/f aperiodic components. MK-801 and diazepam showed distinct signatures across brain regions and EEG components. Specific features of these components are sensitive to relatively small changes in measured exposure. This methodological approach and the features identified as sensitive to EIB modulation could be key for the development of new therapies and functional biomarkers in disorders with excitatory-inhibitory imbalance.

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Dopamine depletion can be predicted by the aperiodic component of subthalamic local field potentials

Cited by 27 publications

References 56 publications

The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism: a cross-species study in vivo

The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism: a cross-species study in vivo

The neurophysiological brain-fingerprint of Parkinson’s disease

Glutamatergic and GABAergic Receptor Modulation Present Unique Electrophysiological Fingerprints in a Concentration-Dependent and Region-Specific Manner

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