Journal
JOURNAL OF NEUROSCIENCE
Volume 40, Issue 10, Pages 2166-2177Publisher
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.2480-19.2020
Keywords
basal ganglia; deep brain stimulation; hyperdirect pathway; nonhuman primate; Parkinson's disease; primary motor cortex
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Funding
- NIH NINDS [R01NS037019, R37NS077657, P50 NS098573, R01NS110613]
- MnDRIVE (Minnesota's Discovery, Research and Innovation Economy) Brain Conditions Program, Engdahl Family Foundation
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Deep brain stimulation (DBS) of the subthalamic nucleus (STN) and globus pallidus internus (GPi) is an effective treatment for parkinsonian motor signs. Though its therapeutic mechanisms remain unclear, it has been suggested that antidromic activation of the primary motor cortex (M1) plays a significant role in mediating its therapeutic effects. This study tested the hypothesis that antidromic activation of M1 is a prominent feature underlying the therapeutic effect of STN and GPi DBS. Single-unit activity in M1 was recorded using high-density microelectrode arrays in two parkinsonian nonhuman primates each implanted with DBS leads targeting the STN and GPi. Stimulation in each DBS target had similar therapeutic effects, however, antidromic activation of M1 was only observed during STN DBS. Although both animals undergoing STN DBS had similar beneficial effects, the proportion of antidromic-classified cells in each differed, 30 versus 6%. Over 4 h of continuous STN DBS, antidromic activation became less robust, whereas therapeutic benefits were maintained. Although antidromic activation waned over time, synchronization of spontaneous spiking in M1 was significantly reduced throughout the 4 h. Although we cannot discount the potential therapeutic role of antidromic M1 activation at least in the acute phase of STN DBS, the difference in observed antidromic activation between animals, and target sites, raise questions about its hypothesized role as the primary mechanism underlying the therapeutic effect of DBS. These results lend further support that reductions in synchronization at the level of M1 are an important factor in the therapeutic effects of DBS.
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