Single neurons in the thalamus and subthalamic nucleus process cardiac and respiratory signals in humans

Author:

De Falco Emanuela12ORCID,Solcà Marco13ORCID,Bernasconi Fosco1,Babo-Rebelo Mariana1ORCID,Young Nicole4,Sammartino Francesco5,Tallon-Baudry Catherine6ORCID,Navarro Vincent7,Rezai Ali R.8,Krishna Vibhor9ORCID,Blanke Olaf110ORCID

Affiliation:

1. Laboratory of Cognitive Neuroscience, School of Life Sciences, Neuro-X Institute and Brain Mind Institute, École Polytechnique Fédérale de Lausanne, Lausanne 1015, Switzerland

2. Department of Neuroscience, Rockefeller Neuroscience Institute–West Virginia University, Morgantown, WV 26505

3. Department of Psychiatry, University Hospital Geneva, Geneva 1205, Switzerland

4. Medical Department, SpecialtyCare, Brentwood, TN 37027

5. Department of Physical Medicine and Rehabilitation, The Ohio State University, Columbus, OH 43210

6. Laboratoire de Neurosciences Cognitives et Computationnelles, Département d’Etudes Cognitives, École normale supérieure-Paris Sciences et Lettres University, Inserm, Paris 75005, France

7. Sorbonne Université, Paris Brain Institute—Institut du Cerveau et de la Moelle épinière, Inserm, CNRS, Assistance Publique - Hôpitaux de Paris, Epilepsy Unit, Hôpital de la Pitié-Salpêtrière, Paris 75013, France

8. Department of Neurosurgery, Rockefeller Neuroscience Institute—West Virginia University, Morgantown, WV 26505

9. Department of Neurosurgery, University of North Carolina at Chapel Hill, Durham, NC 27516

10. Department of Clinical Neurosciences, University Hospital Geneva, Geneva 1205, Switzerland

Abstract

Visceral signals are constantly processed by our central nervous system, enable homeostatic regulation, and influence perception, emotion, and cognition. While visceral processes at the cortical level have been extensively studied using non-invasive imaging techniques, very few studies have investigated how this information is processed at the single neuron level, both in humans and animals. Subcortical regions, relaying signals from peripheral interoceptors to cortical structures, are particularly understudied and how visceral information is processed in thalamic and subthalamic structures remains largely unknown. Here, we took advantage of intraoperative microelectrode recordings in patients undergoing surgery for deep brain stimulation (DBS) to investigate the activity of single neurons related to cardiac and respiratory functions in three subcortical regions: ventral intermedius nucleus (Vim) and ventral caudalis nucleus (Vc) of the thalamus, and subthalamic nucleus (STN). We report that the activity of a large portion of the recorded neurons (about 70%) was modulated by either the heartbeat, the cardiac inter-beat interval, or the respiration. These cardiac and respiratory response patterns varied largely across neurons both in terms of timing and their kind of modulation. A substantial proportion of these visceral neurons (30%) was responsive to more than one of the tested signals, underlining specialization and integration of cardiac and respiratory signals in STN and thalamic neurons. By extensively describing single unit activity related to cardiorespiratory function in thalamic and subthalamic neurons, our results highlight the major role of these subcortical regions in the processing of visceral signals.

Publisher

Proceedings of the National Academy of Sciences

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