Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation
IntroductionDeep brain stimulation (DBS) studies in Parkinson's Disease (PD) targeting the subthalamic nucleus (STN) have characterized its spectral properties across cognitive processes. In emotional evaluation tasks, specific alpha frequency (8–12 Hz) event-related de-synchronization (ERD) (r...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-07-01
|
| Series: | Frontiers in Human Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1181635/full |
| _version_ | 1797770953160130560 |
|---|---|
| author | Naeem Muhammad Naeem Muhammad Saurabh Sonkusare Saurabh Sonkusare Saurabh Sonkusare Qiong Ding Linbin Wang Linbin Wang Linbin Wang Alekhya Mandali Yi Jie Zhao Yi Jie Zhao Bomin Sun Dianyou Li Valerie Voon Valerie Voon Valerie Voon Valerie Voon |
| author_facet | Naeem Muhammad Naeem Muhammad Saurabh Sonkusare Saurabh Sonkusare Saurabh Sonkusare Qiong Ding Linbin Wang Linbin Wang Linbin Wang Alekhya Mandali Yi Jie Zhao Yi Jie Zhao Bomin Sun Dianyou Li Valerie Voon Valerie Voon Valerie Voon Valerie Voon |
| author_sort | Naeem Muhammad |
| collection | DOAJ |
| description | IntroductionDeep brain stimulation (DBS) studies in Parkinson's Disease (PD) targeting the subthalamic nucleus (STN) have characterized its spectral properties across cognitive processes. In emotional evaluation tasks, specific alpha frequency (8–12 Hz) event-related de-synchronization (ERD) (reduced power) has been demonstrated. The time-locked stimulation of STN relative to stimuli onset has shown subjective positive valence shifts with 10 Hz but not with 130 Hz. However, neurophysiological effects of stimulation on power modulation have not been investigated. We aim to investigate effects of acute stimulation of the right STN on concurrent power modulation in the contralateral STN and frontal scalp EEG. From our previous study, we had a strong a priori hypothesis that negative imagery without stimulation would be associated with alpha ERD; negative imagery with 130 Hz stimulation would be also associated with alpha ERD given the lack of its effect on subjective valence ratings; negative imagery with 10 Hz stimulation was to be associated with enhanced alpha power given the shift in behavioral valence ratings.MethodsTwenty-four subjects with STN DBS underwent emotional picture-viewing tasks comprising neutral and negative pictures. In a subset of these subjects, the negative images were associated with time-locked acute stimulation at either 10 or 130 Hz. Power of signals was estimated relative to the baseline and subjected to non-parametric statistical testing.ResultsAs hypothesized, in 130 Hz stimulation condition, we show a decrease in alpha power to negative vs. neutral images irrespective of stimulation. In contrast, this alpha power decrease was no longer evident in the negative 10 Hz stimulation condition consistent with a predicted increase in alpha power. Greater beta power in the 10 Hz stimulation condition along with correlations between beta power across the 10 Hz stimulation and unstimulated conditions suggest physiological and cognitive generalization effects.ConclusionAcute alpha-specific frequency stimulation presumably was associated with a loss of this expected decrease or desynchronization in alpha power to negative images suggesting the capacity to facilitate the synchronization of alpha and enhance power. Acute time-locked stimulation has the potential to provide causal insights into the spectral frequencies and temporal dynamics of emotional processing. |
| first_indexed | 2024-03-12T21:30:29Z |
| format | Article |
| id | doaj.art-59c9fbf61e5a4899bbd3e5ba4d109611 |
| institution | Directory Open Access Journal |
| issn | 1662-5161 |
| language | English |
| last_indexed | 2024-03-12T21:30:29Z |
| publishDate | 2023-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-59c9fbf61e5a4899bbd3e5ba4d1096112023-07-27T22:06:59ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612023-07-011710.3389/fnhum.2023.11816351181635Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulationNaeem Muhammad0Naeem Muhammad1Saurabh Sonkusare2Saurabh Sonkusare3Saurabh Sonkusare4Qiong Ding5Linbin Wang6Linbin Wang7Linbin Wang8Alekhya Mandali9Yi Jie Zhao10Yi Jie Zhao11Bomin Sun12Dianyou Li13Valerie Voon14Valerie Voon15Valerie Voon16Valerie Voon17Department of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Psychiatry, University of Cambridge, Cambridge, United KingdomDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Psychiatry, University of Cambridge, Cambridge, United KingdomInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaKey Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaDepartment of Psychiatry, University of Cambridge, Cambridge, United KingdomInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaKey Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Neurosurgery, Centre for Functional Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, ChinaDepartment of Psychiatry, University of Cambridge, Cambridge, United KingdomInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaKey Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, Fudan University, Shanghai, ChinaIntroductionDeep brain stimulation (DBS) studies in Parkinson's Disease (PD) targeting the subthalamic nucleus (STN) have characterized its spectral properties across cognitive processes. In emotional evaluation tasks, specific alpha frequency (8–12 Hz) event-related de-synchronization (ERD) (reduced power) has been demonstrated. The time-locked stimulation of STN relative to stimuli onset has shown subjective positive valence shifts with 10 Hz but not with 130 Hz. However, neurophysiological effects of stimulation on power modulation have not been investigated. We aim to investigate effects of acute stimulation of the right STN on concurrent power modulation in the contralateral STN and frontal scalp EEG. From our previous study, we had a strong a priori hypothesis that negative imagery without stimulation would be associated with alpha ERD; negative imagery with 130 Hz stimulation would be also associated with alpha ERD given the lack of its effect on subjective valence ratings; negative imagery with 10 Hz stimulation was to be associated with enhanced alpha power given the shift in behavioral valence ratings.MethodsTwenty-four subjects with STN DBS underwent emotional picture-viewing tasks comprising neutral and negative pictures. In a subset of these subjects, the negative images were associated with time-locked acute stimulation at either 10 or 130 Hz. Power of signals was estimated relative to the baseline and subjected to non-parametric statistical testing.ResultsAs hypothesized, in 130 Hz stimulation condition, we show a decrease in alpha power to negative vs. neutral images irrespective of stimulation. In contrast, this alpha power decrease was no longer evident in the negative 10 Hz stimulation condition consistent with a predicted increase in alpha power. Greater beta power in the 10 Hz stimulation condition along with correlations between beta power across the 10 Hz stimulation and unstimulated conditions suggest physiological and cognitive generalization effects.ConclusionAcute alpha-specific frequency stimulation presumably was associated with a loss of this expected decrease or desynchronization in alpha power to negative images suggesting the capacity to facilitate the synchronization of alpha and enhance power. Acute time-locked stimulation has the potential to provide causal insights into the spectral frequencies and temporal dynamics of emotional processing.https://www.frontiersin.org/articles/10.3389/fnhum.2023.1181635/fulldeep brain stimulation (DBS)acute stimulationalpha frequencyemotionevent related (de)/synchronization |
| spellingShingle | Naeem Muhammad Naeem Muhammad Saurabh Sonkusare Saurabh Sonkusare Saurabh Sonkusare Qiong Ding Linbin Wang Linbin Wang Linbin Wang Alekhya Mandali Yi Jie Zhao Yi Jie Zhao Bomin Sun Dianyou Li Valerie Voon Valerie Voon Valerie Voon Valerie Voon Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation Frontiers in Human Neuroscience deep brain stimulation (DBS) acute stimulation alpha frequency emotion event related (de)/synchronization |
| title | Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| title_full | Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| title_fullStr | Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| title_full_unstemmed | Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| title_short | Time-locked acute alpha-frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| title_sort | time locked acute alpha frequency stimulation of subthalamic nuclei during the evaluation of emotional stimuli and its effect on power modulation |
| topic | deep brain stimulation (DBS) acute stimulation alpha frequency emotion event related (de)/synchronization |
| url | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1181635/full |
| work_keys_str_mv | AT naeemmuhammad timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT naeemmuhammad timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT saurabhsonkusare timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT saurabhsonkusare timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT saurabhsonkusare timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT qiongding timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT linbinwang timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT linbinwang timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT linbinwang timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT alekhyamandali timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT yijiezhao timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT yijiezhao timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT bominsun timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT dianyouli timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT valerievoon timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT valerievoon timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT valerievoon timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation AT valerievoon timelockedacutealphafrequencystimulationofsubthalamicnucleiduringtheevaluationofemotionalstimulianditseffectonpowermodulation |