Natasha C Hughes, Danika L Paulo, Michael Zargari, Derek J Doss, Saramati Narasimhan, Robert Shults, Rui Li, Benoit M Dawant, Kaltra Dhima, Hakmook Kang, Travis J Hassell, Tyler J Ball, Dario J Englot, Sarah K Bick
{"title":"术中神经放电与帕金森病的运动和认知特征相关。","authors":"Natasha C Hughes, Danika L Paulo, Michael Zargari, Derek J Doss, Saramati Narasimhan, Robert Shults, Rui Li, Benoit M Dawant, Kaltra Dhima, Hakmook Kang, Travis J Hassell, Tyler J Ball, Dario J Englot, Sarah K Bick","doi":"10.3171/2025.1.JNS241414","DOIUrl":null,"url":null,"abstract":"<p><strong>Objective: </strong>During deep brain stimulation (DBS) surgery for Parkinson's disease (PD), intraoperative microelectrode recordings (MERs) are frequently used to determine electrode positioning within the subthalamic nucleus (STN) and globus pallidus internus (GPi). Various patient characteristics might be associated with abnormal STN and GPi firing activity and thus influence electrode placement. In this study, the authors aimed to elucidate the relationship between preoperative dopamine responsiveness or changes in cognitive status and STN or GPi multiunit activity.</p><p><strong>Methods: </strong>This retrospective cohort study included patients with PD undergoing awake STN (n = 74) or GPi (n = 63) DBS surgery with intraoperative MER at a single institution from 2013 to 2021. To control for the lead position, contralateral motor outcomes of each lead were graded using 1-year neurological follow-up notes. Multiunit neural firing activity for each lead was recorded from MER at the location corresponding to lead active contact at the 1-year follow-up assessment. Linear regression models, controlling for disease duration and age, were used to identify associations between multiunit neural firing rates and preoperative dopamine responsiveness, determined by the difference between preoperative motor scores when on medication minus preoperative motor scores when off medication, and between multiunit activity and the pre- to postoperative change in Mini-Mental State Examination scores.</p><p><strong>Results: </strong>Seventy-four patients with 130 STN leads (mean age 61.2 ± 10.4 years) and 63 patients with 110 GPi leads (mean age 62.8 ± 8.6 years) were included. In STN leads with maximum contralateral motor improvement, increased dopamine responsiveness was associated with both the intraoperative firing rate (p = 0.01) and disease duration (p = 0.01). These relationships were not significant in the GPi leads or when looking at leads for which patients experienced suboptimal motor improvement (p > 0.05). In the GPi leads, an increased intraoperative firing rate in electrodes with maximum symptom improvement was associated with declining cognitive status (p = 0.045).</p><p><strong>Conclusions: </strong>These findings suggest patient characteristics that correlate with neural firing rates and influence intraoperative MER, final electrode placement, and patient outcomes, while improving understanding of STN and GPi pathophysiologic mechanisms in PD. Future investigations into other characteristics that might affect STN and GPi intraoperative neurophysiology are warranted.</p>","PeriodicalId":16505,"journal":{"name":"Journal of neurosurgery","volume":" ","pages":"1-10"},"PeriodicalIF":3.5000,"publicationDate":"2025-05-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Intraoperative neural firing correlates with motor and cognitive features in Parkinson's disease.\",\"authors\":\"Natasha C Hughes, Danika L Paulo, Michael Zargari, Derek J Doss, Saramati Narasimhan, Robert Shults, Rui Li, Benoit M Dawant, Kaltra Dhima, Hakmook Kang, Travis J Hassell, Tyler J Ball, Dario J Englot, Sarah K Bick\",\"doi\":\"10.3171/2025.1.JNS241414\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Objective: </strong>During deep brain stimulation (DBS) surgery for Parkinson's disease (PD), intraoperative microelectrode recordings (MERs) are frequently used to determine electrode positioning within the subthalamic nucleus (STN) and globus pallidus internus (GPi). Various patient characteristics might be associated with abnormal STN and GPi firing activity and thus influence electrode placement. In this study, the authors aimed to elucidate the relationship between preoperative dopamine responsiveness or changes in cognitive status and STN or GPi multiunit activity.</p><p><strong>Methods: </strong>This retrospective cohort study included patients with PD undergoing awake STN (n = 74) or GPi (n = 63) DBS surgery with intraoperative MER at a single institution from 2013 to 2021. To control for the lead position, contralateral motor outcomes of each lead were graded using 1-year neurological follow-up notes. Multiunit neural firing activity for each lead was recorded from MER at the location corresponding to lead active contact at the 1-year follow-up assessment. Linear regression models, controlling for disease duration and age, were used to identify associations between multiunit neural firing rates and preoperative dopamine responsiveness, determined by the difference between preoperative motor scores when on medication minus preoperative motor scores when off medication, and between multiunit activity and the pre- to postoperative change in Mini-Mental State Examination scores.</p><p><strong>Results: </strong>Seventy-four patients with 130 STN leads (mean age 61.2 ± 10.4 years) and 63 patients with 110 GPi leads (mean age 62.8 ± 8.6 years) were included. In STN leads with maximum contralateral motor improvement, increased dopamine responsiveness was associated with both the intraoperative firing rate (p = 0.01) and disease duration (p = 0.01). These relationships were not significant in the GPi leads or when looking at leads for which patients experienced suboptimal motor improvement (p > 0.05). In the GPi leads, an increased intraoperative firing rate in electrodes with maximum symptom improvement was associated with declining cognitive status (p = 0.045).</p><p><strong>Conclusions: </strong>These findings suggest patient characteristics that correlate with neural firing rates and influence intraoperative MER, final electrode placement, and patient outcomes, while improving understanding of STN and GPi pathophysiologic mechanisms in PD. Future investigations into other characteristics that might affect STN and GPi intraoperative neurophysiology are warranted.</p>\",\"PeriodicalId\":16505,\"journal\":{\"name\":\"Journal of neurosurgery\",\"volume\":\" \",\"pages\":\"1-10\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2025-05-23\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of neurosurgery\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.3171/2025.1.JNS241414\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"CLINICAL NEUROLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of neurosurgery","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3171/2025.1.JNS241414","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"CLINICAL NEUROLOGY","Score":null,"Total":0}
Intraoperative neural firing correlates with motor and cognitive features in Parkinson's disease.
Objective: During deep brain stimulation (DBS) surgery for Parkinson's disease (PD), intraoperative microelectrode recordings (MERs) are frequently used to determine electrode positioning within the subthalamic nucleus (STN) and globus pallidus internus (GPi). Various patient characteristics might be associated with abnormal STN and GPi firing activity and thus influence electrode placement. In this study, the authors aimed to elucidate the relationship between preoperative dopamine responsiveness or changes in cognitive status and STN or GPi multiunit activity.
Methods: This retrospective cohort study included patients with PD undergoing awake STN (n = 74) or GPi (n = 63) DBS surgery with intraoperative MER at a single institution from 2013 to 2021. To control for the lead position, contralateral motor outcomes of each lead were graded using 1-year neurological follow-up notes. Multiunit neural firing activity for each lead was recorded from MER at the location corresponding to lead active contact at the 1-year follow-up assessment. Linear regression models, controlling for disease duration and age, were used to identify associations between multiunit neural firing rates and preoperative dopamine responsiveness, determined by the difference between preoperative motor scores when on medication minus preoperative motor scores when off medication, and between multiunit activity and the pre- to postoperative change in Mini-Mental State Examination scores.
Results: Seventy-four patients with 130 STN leads (mean age 61.2 ± 10.4 years) and 63 patients with 110 GPi leads (mean age 62.8 ± 8.6 years) were included. In STN leads with maximum contralateral motor improvement, increased dopamine responsiveness was associated with both the intraoperative firing rate (p = 0.01) and disease duration (p = 0.01). These relationships were not significant in the GPi leads or when looking at leads for which patients experienced suboptimal motor improvement (p > 0.05). In the GPi leads, an increased intraoperative firing rate in electrodes with maximum symptom improvement was associated with declining cognitive status (p = 0.045).
Conclusions: These findings suggest patient characteristics that correlate with neural firing rates and influence intraoperative MER, final electrode placement, and patient outcomes, while improving understanding of STN and GPi pathophysiologic mechanisms in PD. Future investigations into other characteristics that might affect STN and GPi intraoperative neurophysiology are warranted.
期刊介绍:
The Journal of Neurosurgery, Journal of Neurosurgery: Spine, Journal of Neurosurgery: Pediatrics, and Neurosurgical Focus are devoted to the publication of original works relating primarily to neurosurgery, including studies in clinical neurophysiology, organic neurology, ophthalmology, radiology, pathology, and molecular biology. The Editors and Editorial Boards encourage submission of clinical and laboratory studies. Other manuscripts accepted for review include technical notes on instruments or equipment that are innovative or useful to clinicians and researchers in the field of neuroscience; papers describing unusual cases; manuscripts on historical persons or events related to neurosurgery; and in Neurosurgical Focus, occasional reviews. Letters to the Editor commenting on articles recently published in the Journal of Neurosurgery, Journal of Neurosurgery: Spine, and Journal of Neurosurgery: Pediatrics are welcome.