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Pseudobulbar affective disorder, emotion and the brain
  1. Michael Swash1,
  2. Michael R Trimble2
  1. 1 Department of Neurology, Royal London Hospital, Barts and the London School of Medicine and Dentistry, Queen Mary University of London, London, UK
  2. 2 Department of Behavioural Neurology, Institute of Neurology, University College London, London, UK
  1. Correspondence to Professor Michael Swash, Department of Neurology, The Royal London Hospital, London, UK EC2Y 8BL; mswash{at}btinternet.com

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Emotional expression and cognition are unlinked in pseudobulbar affective disorder

In the past half-century, the neuroanatomical regulators of emotion have become better understood. The rediscovery of the limbic areas and their intimate links with the basal ganglia, especially the ventral striatum and associated orbitofrontal cortex, and the special role of the right hemisphere in emotional experience has been central to this understanding.1 However, the complexity of the relationship between these circuits and areas of isocortex and the descending pathways to midbrain and brainstem nuclei in volitional and emotional faciobulbar expression remain less well understood. Emotional disorder is a major feature of frontal brain disease, and complex emotional states and gelastic seizures are well-recognised features of some forms of epilepsy. Uncontrolled, disabling and unstable mood change characteristics of pseudobulbar affective disorder may develop after diffuse traumatic brain injury, in frontal or multi-infarct cerebrovascular disease, multiple sclerosis and degenerative brain diseases, which can lead to depressive illness, bipolar disorder and emotional lability.

The relationship between the experience of emotion and its motor expression was first clearly formulated in 1884–1885 in the James-Lange theory of the emotions.2 This theory suggested that emotional feelings and behaviours stemmed from the motor and sensory activities are characterised by the motor expression itself. Subsequently, Cannon and Bard3 concluded that emotional feelings originate in the dorsal thalamus, modified by cortex, and emotional expression in the hypothalamus; thus, feeling and expression of emotions are separated. The somewhat counterintuitive concept underlying the James-Lange hypothesis was partially accepted by Wilson as the theoretical basis for his seminal review of pathological laughing and crying—pseudobulbar affect—in neurological disorders.4 It is of contemporary interest that Wilson described patients in whom the expressed emotion was not accompanied by the appropriate internal experience (mood incongruent), although the experience was excited by emotionally relevant external stimuli and could not be voluntarily suppressed. However, in other patients, the emotion was congruent and expressed even to excess. Wilson concluded that pathological laughing and crying resulted from disinhibition of brain stem centres from volitional cortical control, leading to the potential dissociation of affective display from subjectively experienced emotional states. This hypothesis required two pathways for faciobulbar movement, one concerned with volitional facial expression and the other with emotional facial movements as, indeed, was recognised by Wilson in supranuclear facial palsies.4 In this issue of the journal, Thakore and Pioro explored disordered emotionality in amyotrophic lateral sclerosis (ALS), noting that crying-predominant pseudobulbar affect was often associated with depression, whereas laughter-predominant pseudobulbar affect was not.5

Although classically associated with lesions involving the brain motor system, more recently pseudobulbar affect has been found to be associated with lesions interrupting pathways from higher cortical association areas to the cerebellum, implying a cerebellar mechanism for modulation of affective display.6 Corticopontocerebellar pathways, projecting via the anterior limb of the internal capsules and through the pontine nuclei, are required in the regulation of emotion and its expression.7 In addition, the cerebellum has itself been recognised as important in the regulation of emotion and related thought implying that the thinking and emotional brain are functionally closely linked.8 On this basis, released involuntary laughter and/or crying in the pseudobulbar affective syndrome result on the basis of incomplete information about the context, resulting in inadequate and chaotic behaviour due to failure of automatic adjustment of the execution of laughter or crying to the cognitive and situational context of a potential emotional stimulus.6 An MRI study of multiple sclerosis associated with pseudobulbar affective disorder found associations with brainstem hypodense lesions and with left inferior temporal and bilateral inferior frontal hyperdense lesions.9

These ideas find support in recent diffusion tensor imaging studies of the brain in ALS and primary lateral sclerosis.10 These have shown reduced fractional anisotropy in the corticospinal and callosal white matter pathways, with increased mean diffusivity in white matter pathways underlying frontotemporal cortex, in transverse pontine fibres and in the middle cerebellar peduncle. There is evidence that the relevant pathways are serotoninergic and dopaminergic and that in pseudobulbar affective disorder, there is reduced binding of these neurotransmitters in the brain. Treatment with serotonin reuptake inhibitors is partially effective in pseudobulbar affective disorder and a combination of dextromethorphan with a small dose of quinidine, which slows hepatic breakdown of dextromethorphan, is effective in partially reducing the frequency of episodes of pathological laughter and crying, without major side effects.11 These findings require a reappraisal of any simple idea that the limbic system alone represents the ‘emotional brain’.

In practice, it is important to recognise that pseudobulbar affective states are not always related to the presence of a complementary underlying emotion. As close friends and relatives, through natural empathetic identification of the patient’s emotional state, may be more disturbed than the patient, careful explanation of the neurological cause of the emotional disorder is required, often with repeated reassurance. Tactics to explore ways to minimise the embarrassment they, the patient and others may feel are important in management. Pseudobulbar affective disorder is a clinical problem that has not received as much attention as it deserves. Unravelling the functional neuroanatomy of laughing and crying, behaviours which are unique to human experience, is an important area of neuroscience.

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Footnotes

  • Contributors MS and MRT contributed equally to this commentary.

  • Competing interests None declared.

  • Provenance and peer review Commissioned; internally peer reviewed.

  • Correction notice This paper has been amended since it was published Online First. Owing to a scripting error, some of the publisher names in the references were replaced with ‘BMJ Publishing Group’. This only affected the full text version, not the PDF. We have since corrected these errors and the correct publishers have been inserted into the references.

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