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Chronic deep brain stimulation of the human nucleus accumbens region disrupts the stability of inter-temporal preferences

View ORCID ProfileBen J. Wagner, Canan B. Schüller, Thomas Schüller, Juan C. Baldermann, Sina Kohl, Veerle Visser-Vandewalle, Daniel Huys, Milena Marx, Jens Kuhn, View ORCID ProfileJan Peters
doi: https://doi.org/10.1101/2020.12.11.417337
Ben J. Wagner
1Department of Psychology, Biological Psychology, University of Cologne, Germany
2Faculty of Psychology, Chair of Neuroimaging, TU Dresden, Germany
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  • For correspondence: ben_jonathan.wagner@tu-dresden.de
Canan B. Schüller
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
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Thomas Schüller
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
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Juan C. Baldermann
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
4Department of Neurology, University Hospital Cologne, University of Cologne, Cologne, Germany
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Sina Kohl
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
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Veerle Visser-Vandewalle
5Department of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, Germany
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Daniel Huys
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
6Department of Psychiatry and Psychotherapy III, LVR Klinik Bonn, Bonn, Germany
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Milena Marx
7Department of Psychology, Developmental Psychology, University of Heidelberg, Heidelberg, Germany
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Jens Kuhn
3Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany
8Department of Psychiatry, Psychotherapy and Psychosomatic, Johanniter Hospital Oberhausen, Germany
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Jan Peters
1Department of Psychology, Biological Psychology, University of Cologne, Germany
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Abstract

When choosing between rewards that differ in temporal proximity (inter-temporal choice), human preferences are typically stable, constituting a clinically-relevant transdiagnostic trait. Here we show in patients undergoing deep brain stimulation (DBS) of the anterior limb of the internal capsule / nucleus accumbens region for treatment-resistant obsessivecompulsive disorder (OCD), that long-term chronic (but not phasic) DBS disrupts inter-temporal preferences. Hierarchical Bayesian modeling accounting for temporal discounting behavior across multiple time points allowed us to assess both short-term and long-term reliability of inter-temporal choice. In controls, temporal discounting was highly reliable, both long-term (6 months) and short-term (1 week). In contrast, in patients undergoing DBS, short-term reliability was high, but long-term reliability (6 months) was severely disrupted. Control analyses confirmed that this effect was not due to range restriction, the presence of OCD symptoms or group differences in choice stochasticity. Model-agnostic between- and within-subject analyses confirmed this effect. These findings provide initial evidence for long-term modulation of cognitive function via DBS and highlight a potential contribution of the human nucleus accumbens region to inter-temporal preference stability over time.

Significance Statement Choosing between rewards that differ in temporal proximity is in part a stable trait with relevance for many mental disorders, and depends on prefrontal regions and regions of the dopamine system. Here we show that chronic deep brain stimulation (DBS) of the human anterior limb of the internal capsule / nucleus accumbens region for treatment-resistant obsessive compulsive disorder disrupts the stability of inter-temporal preferences. These findings show that chronic stimulation of one of the brain’s central motivational hubs can disrupt preferences thought to depend on this circuit.

Competing Interest Statement

J.K. has occasionally received honoraria from AstraZeneca, Lilly, Lundbeck, and Otsuka Pharma for lecturing at conferences and financial support to travel. He received financial support for investigator-initiated trials from Medtronic Europe SARL (Meerbusch, Germany). The remaining authors reported no biomedical financial interests or potential conflicts of interests.

Footnotes

  • ↵§ Shared first/senior authorship.

  • - Major update of all modeling procedures: data across time points are now modeled via multivariate gaussian distributions - Reliability analyses now based on posterior distributions of test-retest correlation coefficients drawn from these generative models - All control analyses and single-subject data plots now included in the main text - Included links for open data and code

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 23, 2023.
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Chronic deep brain stimulation of the human nucleus accumbens region disrupts the stability of inter-temporal preferences
Ben J. Wagner, Canan B. Schüller, Thomas Schüller, Juan C. Baldermann, Sina Kohl, Veerle Visser-Vandewalle, Daniel Huys, Milena Marx, Jens Kuhn, Jan Peters
bioRxiv 2020.12.11.417337; doi: https://doi.org/10.1101/2020.12.11.417337
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Chronic deep brain stimulation of the human nucleus accumbens region disrupts the stability of inter-temporal preferences
Ben J. Wagner, Canan B. Schüller, Thomas Schüller, Juan C. Baldermann, Sina Kohl, Veerle Visser-Vandewalle, Daniel Huys, Milena Marx, Jens Kuhn, Jan Peters
bioRxiv 2020.12.11.417337; doi: https://doi.org/10.1101/2020.12.11.417337

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