This first comprehensive, laboratory-based assessment of pathological laughing and crying allowed us to address several fundamental questions about the nature of the disorder. Results involving episodes of pathological laughing and crying were in some respects consistent with prior clinical observations, but in other ways surprising. Furthermore, direct assessment of emotion regulation under standardized conditions suggested specific deficits in patients with pathological laughing and crying that support prior theories.
In a sample of 21 patients with a history of pathological laughing and crying, strong emotional outbursts were induced in 19 patients, whereas comparable events occurred in only 2 of 14 subjects with no history of pathological laughing and crying. The fact that objectively identified episodes were induced almost exclusively in patients endorsing pathological laughing and crying, along with the fact that these events were confirmed by patients as being similar to those experienced in daily life, indicates that episodes of pathological laughing and crying can be elicited in a laboratory setting. Further, this suggests that the subjective, behavioural and physiological characteristics of these in-laboratory events are representative of the reactivity that occurs during episodes in the community. In most cases, the triggers of episodes of pathological laughing and crying were related to thoughts or stimuli that might induce crying or laughing in anyone, but in these patients the triggers resulted in rapidly developing, high intensity, uncontrollable outbursts. The specificity and reproducibility of these trigger–event relationships were remarkable in that many of the patients identified triggers during pre-session interviews that then induced episodes when they were brought up during the laboratory session. In the case of laughing, there was a greater tendency for episodes to occur without an obvious precipitant, but this is consistent with the psychology of laughing, which can normally occur in a variety of contexts, sometimes seemingly inappropriate (Askenasy, 1987
As would be expected based on prior clinical descriptions (Poeck, 1969
) as well as a single prior EMG study of pathological laughing and crying (Tanaka and Sumitsuji, 1991
), facial expressions were stronger during episodes of pathological laughing and crying than during films. Physiological reactions were also stronger in episodes of pathological laughing and crying than films, which was consistent with our hypothesis as well as some prior clinical observations (Wilson, 1924
). A finding that was not expected was that episodes were associated with intense reports of subjective emotional experience that were stronger than those induced by films. This finding is notably opposite to the relationship we hypothesized based on much of the pathological laughing and crying literature, which often depicts pathological laughing and crying as being unrelated, or even opposite to how the patient is feeling (Gallagher, 1989
; Minden and Schiffer, 1990
), although some prior authors have anticipated this finding (Wilson, 1924
; Wortzel et al., 2008
The findings regarding subjective emotional experience merit additional comment. Previous studies have rarely, if ever, systematically collected self-report data immediately after observed episodes of pathological laughing and crying. In many cases, we found that patients would begin to have a reaction during a pause in conversation, and it was only in directed questioning after the episode that the patient could describe the thoughts that led to it. If careful probing had not been pursued, one could have easily assumed that the events had no psychological precipitant. At the same time, pathological laughing and crying was not associated with a statistically significant increase in depressive symptomatology. This contrasts with some findings in the literature (House et al., 1989
), but reinforces the general belief that pathological laughing and crying is not a direct consequence of depression. It is also worth noting that the finding regarding subjective experience might not have emerged if we had included patients with cognitive impairment. Whether the results from our study generalize to patients with cognitive impairment would have to be addressed in other studies, but our results raise concern that studies discussing the relationship between episodes of pathological laughing and crying and subjective feelings could reach inaccurate conclusions in patients with cognitive difficulties. Given its importance for a full understanding of pathological laughing and crying, future studies should make every effort to ensure the validity of self-report data. In patients with speech difficulties, written reports could substitute for verbal reports. Control conditions could be used to help assess the validity of self-reports in cognitively impaired patients.
Our findings suggest that pathological laughing and crying, at least in amyotrophic lateral sclerosis, is much more similar to normal emotion than often depicted (Poeck, 1969
), being associated with congruent activity in all major channels of emotional responding, and often being associated with contextually appropriate triggers. This conclusion is consistent with the original description of pathological laughing and crying in the medical literature by Wilson (1924)
as well as some more recent descriptions (Wortzel et al., 2008
). However, it is also possible that the events occurred spontaneously and were assigned an appropriate feeling state and attributed to specific triggers post hoc
. This would be consistent with models of emotion which posit that physiological activation is too non-specific to engender particular subjective feelings of emotion, and that subjective feelings are attributed to physiological activation based on the context (Schacter and Singer, 1962
). As many of the triggers that produced episodes of pathological laughing and crying in the laboratory session were identified prior to that session, we think this explanation is unlikely. However, additional research will be needed to exclude this possibility.
In response to emotion-eliciting films, we found that the largest difference between patients with pathological laughing and crying and those without occurred during attempts to regulate emotion voluntarily. This finding supports the most prevalent mechanistic hypothesis about pathological laughing and crying, which incorporates the neuroanatomy of emotional processing. Normal emotional processing is dependent on a network of brain regions, including subcortical structures that generate coordinated, often automated emotional responses (e.g. brainstem, hypothalamus, amygdala, striatum), paralimbic structures that link these responses to social and motivational information (e.g. orbitofrontal, ventromedial frontal, ventral anterior cingulate and insular cortices) and dorsal brain regions that mediate voluntary regulation of emotion (e.g. dorsal anterior cingulate and dorsolateral prefrontal cortices, hippocampus). The interactions between these regions are modulated by neurochemical systems including the serotonergic, dopaminergic and adrenergic systems (see Wortzel et al., 2008
and Rosen and Levenson, 2009
for more detailed descriptions). This complex set of systems provides many pathways where disruption can lead to aberrant emotional reactivity. One particular mechanism that has been suggested to cause pathological laughing and crying is failure of the dorsolateral frontal regions to regulate lower systems in the brainstem, either because of disconnection from the brainstem or dysfunction in these dorsal systems (Wilson, 1924
; Wortzel et al., 2008
). Functional and structural imaging experiments have indicated that emotion regulation tasks similar to those used in the current study activate dorsal frontal structures (Ochsner and Gross, 2005
; Goldin et al., 2008
; Welborn et al., 2009
; Giuliani et al., 2011
; Kanske et al., 2011
; Kuhn et al., 2010
; Winecoff et al., 2011
). Thus, the inability of patients with pathological laughing and crying to use this mechanism for regulation supports the possibility that failure of these dorsolateral frontal-based mechanisms is responsible for pathological laughing and crying, at least in amyotrophic lateral sclerosis.
Some caveats regarding the specificity of our findings should be noted. Suppression and reappraisal are thought to be functionally and possibly anatomically distinct mechanisms of regulation with suppression being associated with a higher metabolic demand (Gross, 1998
; Goldin et al., 2008
). In our study, only suppression was significantly impaired in pathological laughing and crying. Reactivity during reappraisal showed a similar pattern, with greater reactivity in patients with pathological laughing and crying than non-pathological laughing and crying patients; this difference approached statistical significance. For this reason, it is probably not wise to conclude that the deficits in emotion regulation in patients with pathological laughing and crying are specific to suppression but are likely to extend to other forms of emotion regulation as well.
In contrast to emotion regulation trials, we found that reactivity during passive viewing in patients with pathological laughing and crying did not differ from that of patients without pathological laughing and crying. This provides preliminary evidence that pathological laughing and crying is not a problem of generalized hyperactivity in the emotion systems studied. Similar findings of comparability between patients with pathological laughing and crying and those without in reactivity to the acoustic startle stimulus supports the idea that the basic mechanisms of emotional reactivity mediated by the brainstem are also intact (Koch and Schnitzler, 1997
). Having said this, it is important to note that small sample sizes work against our ability to detect group differences, and this was probably reflected in relatively large CIs for some of our estimated differences. In addition, we found no statistically significant difference in reactivity between patients with pathological laughing and crying and those without the disorder for sad films under any conditions, but reactivity to sad films was generally lower than for amusing films, and this may indicate that the sad films we used were not powerful enough to elicit the pathological laughing- and crying-related regulation abnormalities. Finally, our experimental design did not include counterbalancing films across viewing conditions, thus the possibility that differences between patient groups were specific to individual films rather than specific regulatory conditions cannot be ruled out.
Patients with pathological laughing and crying were significantly more likely to show bulbar signs and/or symptoms at the onset of amyotrophic lateral sclerosis (33%) and near the time of study (95%) than non-pathological laughing and crying patients. This is consistent with traditional neurological teaching (Poeck, 1969
), and with prior studies (Ironside, 1956
; Gallagher, 1989
; Zeilig et al., 1996
; Newsom-Davis et al., 1999
), and provides further indirect evidence of a frontally-based impairment.