Behavioural and neurophysiological correlates of human cataplexy: A video-polygraphic study

Abstract

Objectives

To investigate the behavioural and neurophysiological pattern of cataplexy.

Methods

Seven narcolepsy with cataplexy patients underwent daytime videopolygraphy using humorous movies or/and jokes to trigger cataplectic attacks.

Results

During segmental cataplectic attacks, EMG showed brief and irregular periods of silencing focally involving facial, neck, axial or limb muscles, sometimes coinciding with bursts of rapid eye movements. All patients enacted intentional movements in response to these segmental postural lapses. During global cataplectic attacks, EMG showed suppression of activity alternated with patterned enhancement, enhanced EMG activity in neck muscles preceding that of other cranial, axial and lower limb muscles. This waxing and waning EMG pattern ended with a complete body collapse and persistent muscle atonia. Breathing irregularities, heart rate (HR) instability and EEG desynchronization were observed during global cataplectic attacks without any appreciable blood pressure changes, but with HR deceleration and silencing of sympathetic skin response while in complete atonia. Patients subjectively perceived the involuntary postural lapses as startling and alarming.

Conclusions

Cataplexy in our patients showed many of the features of tonic REM sleep.

Significance

Cataplexy can be construed as a “freezing-like” perturbation of the orienting response with transient impairment of posture and movements resulting in a “patchwork-compromise-behaviour”.

Introduction

Cataplexy is best defined as a transient loss of muscle tone triggered by strong emotions and typically occurring while laughing or joking (Krahn et al., 2005). It is a core symptom of narcolepsy with cataplexy (NC), and is most often present at disease onset (Gélineau, 1880, Okun et al., 2002, American Academy of Sleep Medicine, 2005). Although cataplexy can result in a dramatic and complete loss of postural muscle tone, resulting in a fall with complete paralysis, loss of tone is more often partial, affecting only some muscles. In these cases it may result in head nodding, limb weakness, slurred speech or facial muscle flickering. Facial attacks with tongue protrusion and closure of eyelids (“cataplectic facies”), are often found around disease onset, sometimes without any clear emotional precipitants (Plazzi et al., 2006, Plazzi et al., 2008, Serra et al., 2008). Generalized forms leading to falls are reported by 25% of NC patients (Bassetti and Aldrich, 1996, Sturzenegger and Bassetti, 2004).

Behavioural and polygraphic criteria for cataplexy have recently been suggested for a murine model of narcolepsy, in which cataplexy is obviously not emotionally triggered (Scammel et al., 2009). By contrast, polygraphic or video-polygraphic studies of cataplexy in human narcolepsy are few and have shown a complex mixture of suppression and enhancement of EMG activity in different muscular segments resulting in postural instability if not falls in some cases (Scollo-Lavizzari, 1970, Guilleminault, 1976, Rubboli et al., 2000, Donadio et al., 2008, Serra et al., 2008).

Cataplectic attacks may last from a few seconds to minutes, and their duration can be prolonged by emotional stimuli (i.e. by reiteration of the trigger, intervention of helpers). Attacks of long duration may evolve into a frank REM sleep episode. In rare cases, cataplectic spells may occur in tightly packed clusters, or be almost continuous, a condition known as “status cataplecticus”. This particular condition may appear at the onset of the disease or may be provoked by antidepressant withdrawal (Plazzi et al., 2007, Serra et al., 2008). Unfortunately, it is at risk of being mistaken for a psychogenic symptom (Simon et al., 2004).

Cataplexy has long been thought to represent the abnormal expression of REM sleep, whereby muscular atonia typical of REM sleep occurs inappropriately when awake (American Academy of Sleep Medicine, 2005). Some features of cataplexy, however, do not fully conform to this view (Tucci and Plazzi, 2009). This study is a video-polygraphic analysis of cataplexy in a group of patients with well characterized NC. Our goal was to investigate the behavioural features, the EMG pattern of cranial and skeletal muscles, and autonomic and EEG variables during cataplexy to shed more light on this puzzling symptom.