Pathological laughter and crying: insights from lesion network-symptom-mapping

Author:

Klingbeil Julian1ORCID,Wawrzyniak Max1ORCID,Stockert Anika1ORCID,Brandt Max-Lennart1,Schneider Hans-Ralf1ORCID,Metelmann Moritz1,Saur Dorothee1

Affiliation:

1. Language and Aphasia Laboratory, Department of Neurology, University of Leipzig Medical Centre, 04103 Leipzig, Germany

Abstract

Abstract The study of pathological laughter and crying (PLC) allows insights into the neural basis of laughter and crying, two hallmarks of human nature. PLC is defined by brief, intense and frequent episodes of uncontrollable laughter or crying provoked by trivial stimuli. It occurs secondary to CNS disorders such as stroke, tumours or neurodegenerative diseases. Based on case studies reporting various lesions locations, PLC has been conceptualized as dysfunction in a cortico-limbic-subcortico-thalamo-ponto-cerebellar network. To test whether the heterogeneous lesion locations are indeed linked in a common network, we applied ‘lesion network-symptom-mapping’ to 70 focal lesions identified in a systematic literature search for case reports of PLC. In lesion network-symptom-mapping normative connectome data (resting state functional MRI, n = 100) is used to identify the brain regions that are likely affected by diaschisis based on the lesion locations. With lesion network-symptom-mapping we were able to identify a common network specific for PLC when compared with a control cohort (n = 270). This bilateral network is characterized by positive connectivity to the cingulate and temporomesial cortices, striatum, hypothalamus, mesencephalon and pons, and negative connectivity to the primary motor and sensory cortices. In the most influential pathophysiological model of PLC, a centre for the control and coordination of facial expressions, respiration and vocalization in the periaqueductal grey is assumed, which is controlled via two pathways: an emotional system that exerts excitatory control of the periaqueductal grey descending from the temporal and frontal lobes, basal ganglia and hypothalamus; and a volitional system descending from the lateral premotor cortices that can suppress laughter or crying. To test whether the positive and negative PLC subnetworks identified in our analyses can indeed be related to an emotional system and a volitional system, we identified lesions causing emotional (n = 15) or volitional facial paresis (n = 46) in a second literature search. Patients with emotional facial paresis show preserved volitional movements but cannot trigger emotional movements in the affected hemiface, while the reverse is true for volitional facial paresis. Importantly, these lesions map differentially onto the PLC subnetworks: the ‘positive PLC subnetwork’ is part of the emotional system and the ‘negative PLC subnetwork’ overlaps with the volitional system for the control of facial movements. Based on this network analysis we propose a two-hit model of PLC: a combination of direct lesion and indirect diaschisis effects cause PLC through the loss of inhibitory cortical control of a dysfunctional emotional system.

Funder

Deutsche Forschungsgemeinschaft

Clinician Scientist Program of the University of Leipzig Medical Faculty

University of Leipzig Medical Faculty

James S. McDonnell Foundation

Understanding Human Cognition

Publisher

Oxford University Press (OUP)

Subject

Clinical Neurology

Reference89 articles.

1. Pseudobulbar affect: The spectrum of clinical presentations, etiologies and treatments;Miller;Expert Rev Neurother,2011

2. The differential diagnosis of pseudobulbar affect (PBA). Distinguishing PBA among disorders of mood and affect. Proceedings of a roundtable meeting;Arciniegas;CNS Spectr,2005

3. The epidemiology and pathophysiology of pseudobulbar affect and its association with neurodegeneration;King;Degener Neurol Neuromuscul Dis,2013

4. Neural correlates of laughter and humour;Wild;Brain,2003

5. Original papers: Some problems in neurology;Wilson;J Neurol Psychopathol,1924

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