The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism.

Wiest C
Torrecillos F
Pogosyan A
Bange M
Muthuraman M
Groppa S
Hulse N
Hasegawa H
Ashkan K
Baig F
Morgante F
Pereira EA
Mallet N
Magill PJ
Brown P
Sharott A
Tan H

Can we use recordings from deep brain stimulation electrodes to better understand the balance of brain cell activity in people with Parkinson's? This work suggests we can. We first studied rats to find a measurement that reflected the activity balance, and then showed in people that this measurement also separates different medication and stimulation conditions. This measurement could be used to improve stimulation for therapy.

Scientific Abstract

Periodic features of neural time-series data, such as local field potentials (LFPs), 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.

Top panel: left, picture of rodent with implanted electrode, centre, drawing of brain anatomy, right, figure with two columns of coloured dots; bottom panel, left, drawing of electrodes in a human brain, signals goings to a screen, right, figure with two columns with coloured dots
Top panel: Local field potentials and single neuron spiking were recorded from anaesthetised parkinsonian rats and aperiodic exponents distinguished periods of different excitatory/inhibitory input to STN. Bottom panel: LFPs were recorded from externalised electrodes from people with Parkinson’s and aperiodic exponents separated different medication states.

2023. eLife, 12:e82467

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