Markers of limbic system damage following SARS-CoV-2 infection

Marine Thomasson; Philippe Voruz; Alexandre Cionca; Isabele Jacot de Alcântara; Anthony Nuber-Champier; Gilles Allali; Lamyae Benzakour; Patrice H Lalive; Karl-Olof Lövblad; Olivia Braillard; Mayssam Nehme; Matteo Coen; Jacques Serratrice; Jean-Luc Reny; Jérôme Pugin; Idris Guessous; Basile N Landis; Alessandra Griffa; Dimitri Van De Ville; Frederic Assal; Julie A Péron

doi:10.1093/braincomms/fcad177

Markers of limbic system damage following SARS-CoV-2 infection

Brain Commun. 2023 Jun 13;5(4):fcad177. doi: 10.1093/braincomms/fcad177. eCollection 2023.

Authors

Marine Thomasson^{1

2}, Philippe Voruz^{1

2

3}, Alexandre Cionca¹, Isabele Jacot de Alcântara^{1

2}, Anthony Nuber-Champier¹, Gilles Allali⁴, Lamyae Benzakour⁵, Patrice H Lalive^{2

3}, Karl-Olof Lövblad^{3

6}, Olivia Braillard⁷, Mayssam Nehme⁷, Matteo Coen⁸, Jacques Serratrice⁸, Jean-Luc Reny^{3

8}, Jérôme Pugin^{3

9}, Idris Guessous^{3

7}, Basile N Landis^{3

10}, Alessandra Griffa^{4

11

12}, Dimitri Van De Ville^{3

11}, Frederic Assal^{2

3}, Julie A Péron^{1

2}

Affiliations

¹ Clinical and Experimental Neuropsychology Laboratory, Faculty of Psychology, University of Geneva, Geneva 1205, Switzerland.
² Neurology Department, Department of Clinical Neurosciences, Geneva University Hospitals, Geneva 1205, Switzerland.
³ Faculty of Medicine, University of Geneva, Geneva 1011, Switzerland.
⁴ Leenaards Memory Centre, Lausanne University Hospital and University of Lausanne, Lausanne 1205, Switzerland.
⁵ Psychiatry Department, Geneva University Hospitals, Geneva 1205, Switzerland.
⁶ Diagnostic and Interventional Neuroradiology Department, Geneva University Hospitals, Geneva 1205, Switzerland.
⁷ Division and Department of Primary Care Medicine, Geneva University Hospitals, Geneva 1205, Switzerland.
⁸ Division of General Internal Medicine, Department of Medicine, Geneva University Hospitals and Geneva University, Geneva 1205, Switzerland.
⁹ Intensive Care Department, Geneva University Hospitals, Geneva 1205, Switzerland.
¹⁰ Rhinology-Olfactology Unit, Otorhinolaryngology Department, Geneva University Hospitals, Geneva 1205, Switzerland.
¹¹ Institute of Bioengineering, Centre for Neuroprosthetics, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne 1015, Switzerland.
¹² Department of Radiology and Medical Informatics, University of Geneva, Geneva 1205, Switzerland.

Abstract

Alterations of the limbic system may be present in the chronic phase of SARS-CoV-2 infection. Our aim was to study the long-term impact of this disease on limbic system-related behaviour and its associated brain functional connectivity, according to the severity of respiratory symptoms in the acute phase. To this end, we investigated the multimodal emotion recognition abilities of 105 patients from the Geneva COVID-COG Cohort 223 days on average after SARS-CoV-2 infection (diagnosed between March 2020 and May 2021), dividing them into three groups (severe, moderate or mild) according to respiratory symptom severity in the acute phase. We used multiple regressions and partial least squares correlation analyses to investigate the relationships between emotion recognition, olfaction, cognition, neuropsychiatric symptoms and functional brain networks. Six to 9 months following SARS-CoV-2 infection, moderate patients exhibited poorer recognition abilities than mild patients for expressions of fear (P = 0.03 corrected), as did severe patients for disgust (P = 0.04 corrected) and irritation (P < 0.01 corrected). In the whole cohort, these performances were associated with decreased episodic memory and anosmia, but not with depressive symptoms, anxiety or post-traumatic stress disorder. Neuroimaging revealed a positive contribution of functional connectivity, notably between the cerebellum and the default mode, somatosensory motor and salience/ventral attention networks. These results highlight the long-term consequences of SARS-Cov-2 infection on the limbic system at both the behavioural and neuroimaging levels.

Keywords: MRI; emotion; functional connectivity; neuropsychological deficits; post-COVID syndrome.