Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span
Anticipating social and non-social incentives recruits shared brain structures and promotes behavior. However, little is known about possible age-related behavioral changes, and how the human substantia nigra (SN) signals positive and negative social information. Therefore, we recorded intracranial...
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| Format: | Article |
| Language: | English |
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Elsevier
2021-12-01
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| Series: | NeuroImage |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811921009691 |
| _version_ | 1819097009299128320 |
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| author | Alexandra Sobczak Stefan Repplinger Eva M. Bauch Norbert Brueggemann Christina Lohse Hermann Hinrichs Lars Buentjen Juergen Voges Tino Zaehle Nico Bunzeck |
| author_facet | Alexandra Sobczak Stefan Repplinger Eva M. Bauch Norbert Brueggemann Christina Lohse Hermann Hinrichs Lars Buentjen Juergen Voges Tino Zaehle Nico Bunzeck |
| author_sort | Alexandra Sobczak |
| collection | DOAJ |
| description | Anticipating social and non-social incentives recruits shared brain structures and promotes behavior. However, little is known about possible age-related behavioral changes, and how the human substantia nigra (SN) signals positive and negative social information. Therefore, we recorded intracranial electroencephalography (iEEG) from the SN of Parkinson's Disease (PD) patients (n = 12, intraoperative, OFF medication) in combination with a social incentive delay task including photos of neutral, positive or negative human gestures and mimics as feedback. We also tested a group of non-operated PD patients (n = 24, ON and OFF medication), and a sample of healthy young (n = 51) and older (n = 52) adults with behavioral readouts only. Behaviorally, the anticipation of both positive and negative social feedback equally accelerated response times in contrast to neutral social feedback in healthy young and older adults. Although this effect was not significant in the group of operated PD patients – most likely due to the small sample size – iEEG recordings in their SN showed a significant increase in alpha-beta power (9–20 Hz) from 300 to 600 ms after cue onset again for both positive and negative cues. Finally, in non-operated PD patients, the behavioral effect was not modulated by medication status (ON vs OFF medication) suggesting that other processes than dopaminergic neuromodulation play a role in driving invigoration by social incentives. Together, our findings provide novel and direct evidence for a role of the SN in processing positive and negative social information via specific oscillatory mechanisms in the alpha-beta range, and they suggest that anticipating social value in simple cue-outcome associations is intact in healthy aging and PD. |
| first_indexed | 2024-12-22T00:08:16Z |
| format | Article |
| id | doaj.art-e9f67544069b42259cf477465e5222e6 |
| institution | Directory Open Access Journal |
| issn | 1095-9572 |
| language | English |
| last_indexed | 2024-12-22T00:08:16Z |
| publishDate | 2021-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage |
| spelling | doaj.art-e9f67544069b42259cf477465e5222e62022-12-21T18:45:31ZengElsevierNeuroImage1095-95722021-12-01245118696Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life spanAlexandra Sobczak0Stefan Repplinger1Eva M. Bauch2Norbert Brueggemann3Christina Lohse4Hermann Hinrichs5Lars Buentjen6Juergen Voges7Tino Zaehle8Nico Bunzeck9Department of Psychology, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany; Corresponding authors at: Department of Psychology, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany.Departments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University, Leipziger Straße 44, Magdeburg 39120, Germany; International Graduate School ABINEP, Otto-von-Guericke-University, Leipziger Straße 44, Magdeburg 39120, GermanyDepartment of Psychology, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, GermanyInternational Graduate School ABINEP, Otto-von-Guericke-University, Leipziger Straße 44, Magdeburg 39120, Germany; Department of Neurology, University Medical Center Schleswig-Holstein, Ratzeburger Allee 160, Lübeck 23562, Germany; Institute of Neurogenetics, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany; Center of Brain, Behavior and Metabolism, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, GermanyDepartment of Neurology, University Medical Center Schleswig-Holstein, Ratzeburger Allee 160, Lübeck 23562, GermanyDepartments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University, Leipziger Straße 44, Magdeburg 39120, GermanyDepartments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University, Leipziger Straße 44, Magdeburg 39120, GermanyDepartments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University, Leipziger Straße 44, Magdeburg 39120, GermanyDepartments of Neurology and Stereotactic Neurosurgery, Otto-von-Guericke University, Leipziger Straße 44, Magdeburg 39120, Germany; Center for Behavioral Brain Sciences (CBBS), 39106, MagdeburgDepartment of Psychology, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany; Center of Brain, Behavior and Metabolism, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany; Corresponding authors at: Department of Psychology, University of Lübeck, Ratzeburger Allee 160, Lübeck 23562, Germany.Anticipating social and non-social incentives recruits shared brain structures and promotes behavior. However, little is known about possible age-related behavioral changes, and how the human substantia nigra (SN) signals positive and negative social information. Therefore, we recorded intracranial electroencephalography (iEEG) from the SN of Parkinson's Disease (PD) patients (n = 12, intraoperative, OFF medication) in combination with a social incentive delay task including photos of neutral, positive or negative human gestures and mimics as feedback. We also tested a group of non-operated PD patients (n = 24, ON and OFF medication), and a sample of healthy young (n = 51) and older (n = 52) adults with behavioral readouts only. Behaviorally, the anticipation of both positive and negative social feedback equally accelerated response times in contrast to neutral social feedback in healthy young and older adults. Although this effect was not significant in the group of operated PD patients – most likely due to the small sample size – iEEG recordings in their SN showed a significant increase in alpha-beta power (9–20 Hz) from 300 to 600 ms after cue onset again for both positive and negative cues. Finally, in non-operated PD patients, the behavioral effect was not modulated by medication status (ON vs OFF medication) suggesting that other processes than dopaminergic neuromodulation play a role in driving invigoration by social incentives. Together, our findings provide novel and direct evidence for a role of the SN in processing positive and negative social information via specific oscillatory mechanisms in the alpha-beta range, and they suggest that anticipating social value in simple cue-outcome associations is intact in healthy aging and PD.http://www.sciencedirect.com/science/article/pii/S1053811921009691Substantia nigraIntracranial EEGDopamineSocial reward learningParkinson |
| spellingShingle | Alexandra Sobczak Stefan Repplinger Eva M. Bauch Norbert Brueggemann Christina Lohse Hermann Hinrichs Lars Buentjen Juergen Voges Tino Zaehle Nico Bunzeck Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span NeuroImage Substantia nigra Intracranial EEG Dopamine Social reward learning Parkinson |
| title | Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| title_full | Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| title_fullStr | Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| title_full_unstemmed | Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| title_short | Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| title_sort | anticipating social incentives recruits alpha beta oscillations in the human substantia nigra and invigorates behavior across the life span |
| topic | Substantia nigra Intracranial EEG Dopamine Social reward learning Parkinson |
| url | http://www.sciencedirect.com/science/article/pii/S1053811921009691 |
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