Know thyself: Exploring interoceptive sensitivity in Parkinson's disease

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Highlights

  • PD patients showed lower IS than

  • PD reported higher scores in scales assessing depression, anhedonia and apathy.

  • No significant correlations were detected between IS and motor, non-motor, affective and emotion symptoms.

  • Future studies are encouraged to evaluate the role of interoception in PD.

Abstract

Background

Although Parkinson's disease (PD) is defined by its motor symptoms, it is now well recognised that cognitive, affective and emotion domains are also impaired. The pathophysiology of these disabling non-motor symptoms (NMS) remains unclear; recently the involvement of limbic areas, including the insula, in the neurodegenerative process has been suggested to have a key role. These areas, and the insula in particular, are also been suggested as key regions for interoception; interoceptive sensitivity (IS) is a measure of the accuracy of perception of sensations from inside the body related to the function of internal organs.

Objectives

To evaluate IS in PD patients by means of a well-established task: the heartbeat perception task. Moreover, we evaluated possible correlations between IS and psychological, affective and disease-related characteristics as well as fatigue perception in PD patients.

Methods

Twenty PD patients and 20 healthy subjects (HS) were included and underwent the heartbeat perception task. An extensive evaluation of motor, non-motor, affective and emotion domains was carried out.

Results

PD patients showed lower IS than HS (0.58 ± 0.2 vs 0.72 ± 0.1; p = 0.04). PD reported higher scores in scales assessing depression (Hamilton depression scale: 8.7 ± 5.8 vs 6.2 ± 7.5; p = 0.04); anhedonia (Snaith–Hamilton Pleasure Scale: 26.8 ± 9.7 vs 15.4 ± 2.9; p = < 0.001) and apathy (Apathy Evaluation Scale: 35.8 ± 8.6 vs 27.8 ± 6.8; p = 0.008). No significant correlations were detected between IS and motor, non-motor, affective and emotion symptoms.

Conclusions

PD patients have reduced interoceptive sensitivity. Future studies are encouraged to evaluate the importance of interoception in understanding the pathophysiology of affective/emotional symptoms in PD.

Introduction

Parkinson's disease (PD) is far from just a motor disorder. The importance of non-motor symptoms has been increasingly recognised, particularly in how they significantly add to the burden of PD for patients and impair quality of life. [1] Despite the clinical importance of NMS, the pathophysiology of these symptoms remains unclear.

Limbic areas including insula, amygdala, anterior cingulate cortex are key regions in emotional processing. All these regions, in particular the insula, are involved in the process of interoception, the perception of sensations from inside the body, including the perception of physical sensations related to the function of internal organs. [2] It is proposed that subjective “feeling states” are dependent on the process of interoception: the representation and contextualisation of somatic and visceral responses elicited by emotional stimuli. [3].

In PD many components of the emotional processing are altered, [4] however there is still a lack of clarity on the neurobiological basis of these deficits. Nevertheless, the role of alpha-synuclein deposition and subsequent degeneration of the insula has been highlighted, and suggested as an anatomical region where degeneration could explain a number of NMS, including depression, anxiety, apathy, anhedonia and fatigue. [5].

When studying these aspects of emotion, researchers face two main problems: first, studies are conducted in laboratory and clinical settings and these contexts significantly differ from real life, therefore the generalizability of findings obtained from this research is limited. [6] Second, the diagnosis of these symptoms relies mainly on self-report questionnaires, the validity of which can be called into question when assessing disorders characterized by an inability or an alteration in identifying and judging one's own affective and emotional states. [7] The difficulty in evaluating affective and emotional disorders in PD patients has been also demonstrated in several studies showing a lack of agreement between patients and their caregivers when scoring the severity of these symptoms. [8], [9].

For these reasons, it would be very useful to find an objective measure which would correlate to the severity of NMS such as fatigue perception, affective and emotional symptoms, which could complement and implement the assessment scales in the diagnosis and follow-up of these aspects of the disease. If deficits in interoceptive processing might reflect disease-related insula degeneration and this might underlie a proportion of NMS, then measurement of interoceptive sensitivity (IS) could be a useful biomarker to study. In healthy individuals, higher IS is associated with the experience of more intense emotional states [10] and higher activation of brain areas thought to play a key role in emotional processing (insular cortex, anterior cingulate cortex, ventro-medial and dorsolateral prefrontal cortex and the somatosensory cortex). [2].

Moreover, the literature currently suggests an association between a number of neuropsychiatric problems and reduced IS, including major depression, somatoform disorder, functional neurological symptoms and eating disorders. A disturbed interoceptive awareness of the state of the body has been hypothesized to be linked to symptoms of chronic fatigue and chronic pain [11], [12], [13]. One explanation for this might be that a “noisy” interoceptive signal could result in an inaccurate perception of internal state, which might in turn generate symptoms such as fatigue and pain in the absence of a specific cause.

We hypothesized that due to the neurodegenerative processes in limbic areas (involved in the interoceptive sensitivity) patients with PD may present a disturbed IS which could make them prone to symptoms such as pain, fatigue, emotional/affective disorders. Therefore, we aimed to evaluate using a validated and widely used measure of IS - the heartbeat perception task – whether patients with PD would have disturbed IS compared to healthy subjects, and whether disturbed IS could be related to the presence and severity of NMS, especially affection/emotion symptoms, pain and fatigue perception.

Section snippets

Participants

We recruited 20 consecutive PD patients from the movement disorder outpatient clinics of the National Hospital for Neurology and Neurosurgery, London. Inclusion criteria were a diagnosis of PD according to UK Brain Bank criteria, [14] with treatment and clinical condition stable for at least 4 weeks prior to the study. Exclusion criteria were any major concurrent neurological, cardiac or psychiatric disorders; clinically significant cognitive deficits or score < 26 on the Montreal Cognitive

Results

Twenty PD patients (13 males, mean age 61.4 ± 9.8 years) and 20 healthy controls (HC) (8 male, mean age 56.5 ± 10.8) were included in the study. Demographic and clinical data of the study populations are shown in Table 1, Table 2.

Baseline heartbeats were not significantly different between PD patients and HC (3 min baseline measure: 236.4 ± 46.2 vs 220.6 ± 41.6, p = 0.1). A Mann-Whitney U test revealed that healthy controls had a significantly higher IS compared to patients as measured by the heartbeat

Discussion

This is the first work showing that interoceptive sensitivity, as measured by a heartbeat perception task, is reduced in PD. We have demonstrated that PD patients have a lower IS compared to healthy individuals. However, we found no correlation between IS and a range of self-report measures of affective status, fatigue and non-motor symptoms in general.

Interoception is the body-to-brain axis of sensation concerning the state of the internal body and the organs. It is a key process for

Funding statement

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Competing interest statement

Dr. Ricciardi, Dr. Ferrazzano, Dr. Demartini, Dr. Erro, Dr. Ganos and Prof Berardelli report no disclosures.

Dr. Morgante is member of the advisory boards of UCB pharma, Allergan and Lundbeck, has received honoraria from Allergan, Medtronic, UCB pharma, Lundbeck, Chiesi pharma, and serves in the editorial board of Frontiers Neurology.

Prof Kailash P Bhatia: Funding for travel from GlaxoSmithKline, Orion Corporation, Ipsen, and Merz Pharmaceuticals, LLC; serves on the editorial boards of Movement

Authors' role

  • 1.

    Drafting/revising the manuscript for content, including medical writing for content

  • 2.

    Study concept or design

  • 3.

    Analysis or interpretation of data

  • 4.

    Acquisition of data

  • 5.

    Statistical analysis

  • 6.

    Study supervision or coordination

    LR: 1, 2, 3, 4, 5, 6

    GF: 4

    BD: 3, 4, 5

    FM: 1, 6

    RE:1

    CG:1

    KB:1

    AB:1

    MJE: 1, 2, 3, 6

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