A Neuroanatomy of Positive Affect Display - Subcortical Fiber Pathways Relevant for Initiation and Modulation of Smiling and Laughing

Volker A Coenen; Bastian E A Sajonz; Trevor A Hurwitz; Marlies Böck; Jonas A Hosp; Peter C Reinacher; Horst Urbach; Ganna Blazhenets; Philipp T Meyer; Marco Reisert

doi:10.3389/fnbeh.2022.817554

A Neuroanatomy of Positive Affect Display - Subcortical Fiber Pathways Relevant for Initiation and Modulation of Smiling and Laughing

Front Behav Neurosci. 2022 Mar 30:16:817554. doi: 10.3389/fnbeh.2022.817554. eCollection 2022.

Authors

Volker A Coenen^{1

2}, Bastian E A Sajonz¹, Trevor A Hurwitz³, Marlies Böck^{1

2}, Jonas A Hosp⁴, Peter C Reinacher^{1

5}, Horst Urbach⁶, Ganna Blazhenets⁷, Philipp T Meyer⁷, Marco Reisert¹

Affiliations

¹ Department of Stereotactic and Functional Neurosurgery, Faculty of Medicine, University Medical Center Freiburg, University of Freiburg, Freiburg, Germany.
² Center for Deep Brain Stimulation, University of Freiburg, Freiburg, Germany.
³ Department of Psychiatry, University of British Columbia, Vancouver, BC, Canada.
⁴ Department of Neurology and Clinical Neuroscience, Faculty of Medicine, University Medical Center Freiburg, University of Freiburg, Freiburg, Germany.
⁵ Institute for Laser Technology (ILT), Aachen, Germany.
⁶ Department of Neuroradiology, Medical Faculty, University Medical Center Freiburg, University of Freiburg, Freiburg, Germany.
⁷ Department of Nuclear Medicine, Faculty of Medicine, University Medical Center Freiburg, University of Freiburg, Freiburg, Germany.

Abstract

Background: We here report two cases of stimulation induced pathological laughter (PL) under thalamic deep brain stimulation (DBS) for essential tremor and interpret the effects based on a modified neuroanatomy of positive affect display (PAD).

Objective/hypothesis: The hitherto existing neuroanatomy of PAD can be augmented with recently described parts of the motor medial forebrain bundle (motorMFB). We speculate that a co-stimulation of parts of this fiber structure might lead to a non-volitional modulation of PAD resulting in PL.

Methods: We describe the clinical and individual imaging workup and combine the interpretation with normative diffusion tensor imaging (DTI)-tractography descriptions of motor connections of the ventral tegmental area (VTA) (n = 200 subjects, HCP cohort), [[¹⁸F] fluorodeoxyglucose (¹⁸FDG)] positron emission tomography (PET), and volume of activated tissue simulations. We integrate these results with literature concerning PAD and the neuroanatomy of smiling and laughing.

Results: DBS electrodes bilaterally co-localized with the MB-pathway ("limiter pathway"). The FDG PET activation pattern allowed to explain pathological PAD. A conceptual revised neuroanatomy of PAD is described.

Conclusion: Eliciting pathological PAD through chronic thalamic DBS is a new finding and has previously not been reported. PAD is evolution driven, hard wired to the brain and realized over previously described branches of the motorMFB. A major relay region is the VTA/mammillary body complex. PAD physiologically undergoes conscious modulation mainly via the MB branch of the motorMFB (limiter). This limiter in our cases is bilaterally disturbed through DBS. The here described anatomy adds to a previously described framework of neuroanatomy of laughter and humor.

Keywords: deep brain stimulation; essential tremor; laughter; motorMFB; pathological laughter; pseudobulbar affect.