Alteration of interoceptive sensitivity: expanding the spectrum of behavioural disorders in amyotrophic lateral sclerosis.
Behavioural
Cognition
Emotion
HRV
Interoception
Rehabilitation
Journal
Neurological sciences : official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology
ISSN: 1590-3478
Titre abrégé: Neurol Sci
Pays: Italy
ID NLM: 100959175
Informations de publication
Date de publication:
Sep 2022
Sep 2022
Historique:
received:
02
04
2022
accepted:
17
06
2022
pubmed:
26
6
2022
medline:
20
8
2022
entrez:
25
6
2022
Statut:
ppublish
Résumé
Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder with progressive loss of upper and lower motor neurons. Non-motor-symptoms, such as cognitive, emotional, autonomic, and somatosensory alterations, have been also described. Interoception represents the link between the body and brain, since it refers to the ability to consciously perceive the physical condition of the inner body, including one's heartbeat (i.e., interoceptive sensitivity, IS). To evaluate IS in ALS patients by means of a well-established task: the heartbeat perception task. Moreover, we evaluated possible correlations between IS and neuropsychological, affective, and disease-related characteristics. Fifty-five ALS patients (mean-age = 60.3 ± 12.5 years; mean disease-duration = 20.9 ± 18.8 months) and 41 caregivers (CG) underwent the heartbeat perception task and an extensive evaluation of motor, cognitive, body awareness, affective, and emotion domains. ALS patients showed lower IS than CG (0.68 ± 0.24 vs 0.82 ± 0.16; p = 0.003). Significant correlations were found between IS and self-reported measures of alexithymia (subscale of Toronto Alexithymia scale-20 "difficulties in describing feelings"; rho = - .391, p = .003) and interoceptive awareness (subscale of Multidimensional assessment of interoceptive awareness "not worrying about pain"; rho = .405, p = .002). No significant differences were found on questionnaires for depression and anxiety between patients with ALS and their caregivers (p > .05). ALS patients show reduced interoceptive sensitivity that is associated with poorer ability to describe feelings and with lower focalization on pain, regardless of cognitive and motor impairment. Alteration of interoception may represent a specific behavioural sign within the spectrum of emotion processing deficits described in ALS patients.
Sections du résumé
BACKGROUND
BACKGROUND
Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disorder with progressive loss of upper and lower motor neurons. Non-motor-symptoms, such as cognitive, emotional, autonomic, and somatosensory alterations, have been also described. Interoception represents the link between the body and brain, since it refers to the ability to consciously perceive the physical condition of the inner body, including one's heartbeat (i.e., interoceptive sensitivity, IS).
OBJECTIVES
OBJECTIVE
To evaluate IS in ALS patients by means of a well-established task: the heartbeat perception task. Moreover, we evaluated possible correlations between IS and neuropsychological, affective, and disease-related characteristics.
METHODS
METHODS
Fifty-five ALS patients (mean-age = 60.3 ± 12.5 years; mean disease-duration = 20.9 ± 18.8 months) and 41 caregivers (CG) underwent the heartbeat perception task and an extensive evaluation of motor, cognitive, body awareness, affective, and emotion domains.
RESULTS
RESULTS
ALS patients showed lower IS than CG (0.68 ± 0.24 vs 0.82 ± 0.16; p = 0.003). Significant correlations were found between IS and self-reported measures of alexithymia (subscale of Toronto Alexithymia scale-20 "difficulties in describing feelings"; rho = - .391, p = .003) and interoceptive awareness (subscale of Multidimensional assessment of interoceptive awareness "not worrying about pain"; rho = .405, p = .002). No significant differences were found on questionnaires for depression and anxiety between patients with ALS and their caregivers (p > .05).
CONCLUSIONS
CONCLUSIONS
ALS patients show reduced interoceptive sensitivity that is associated with poorer ability to describe feelings and with lower focalization on pain, regardless of cognitive and motor impairment. Alteration of interoception may represent a specific behavioural sign within the spectrum of emotion processing deficits described in ALS patients.
Identifiants
pubmed: 35751711
doi: 10.1007/s10072-022-06231-4
pii: 10.1007/s10072-022-06231-4
pmc: PMC9385786
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5403-5410Informations de copyright
© 2022. The Author(s).
Références
Abrahams S, Leigh PN, Harvey A et al (2000) Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia 38:734–747. https://doi.org/10.1016/S0028-3932(99)00146-3
doi: 10.1016/S0028-3932(99)00146-3
pubmed: 10689049
Beeldman E, Raaphorst J, Twennaar MK et al (2016) The cognitive profile of ALS: a systematic review and meta-analysis update. J Neurol Neurosurg Psychiatry 87:611–619. https://doi.org/10.1136/jnnp-2015-310734
doi: 10.1136/jnnp-2015-310734
pubmed: 26283685
De Lucia N, Ausiello FP, Spisto M et al (2020) The emotional impact of COVID-19 outbreak in amyotrophic lateral sclerosis patients: evaluation of depression, anxiety and interoceptive awareness. Neurol Sci 41:2339–2341. https://doi.org/10.1007/s10072-020-04592-2
doi: 10.1007/s10072-020-04592-2
pubmed: 32666406
pmcid: 7359442
Girardi A, MacPherson SE, Abrahams S (2011) Deficits in emotional and social cognition in amyotrophic lateral sclerosis. Neuropsychology 25:53–65. https://doi.org/10.1037/a0020357
doi: 10.1037/a0020357
pubmed: 20919762
van Es MA, Hardiman O, Chio A et al (2017) Amyotrophic lateral sclerosis. Lancet 390:2084–2098
doi: 10.1016/S0140-6736(17)31287-4
Montuschi A, Iazzolino B, Calvo A et al (2015) Cognitive correlates in amyotrophic lateral sclerosis: a population-based study in Italy. J Neurol Neurosurg Psychiatry 86:168–173. https://doi.org/10.1136/jnnp-2013-307223
doi: 10.1136/jnnp-2013-307223
pubmed: 24769471
Chiò A, Moglia C, Canosa A et al (2019) Cognitive impairment across ALS clinical stages in a population-based cohort. Neurology 93:E984–E994. https://doi.org/10.1212/WNL.0000000000008063
doi: 10.1212/WNL.0000000000008063
pubmed: 31409738
pmcid: 6745732
Chiò A, Vignola A, Mastro E et al (2010) Neurobehavioral symptoms in ALS are negatively related to caregivers’ burden and quality of life. Eur J Neurol 17:1298–1303. https://doi.org/10.1111/j.1468-1331.2010.03016.x
doi: 10.1111/j.1468-1331.2010.03016.x
pubmed: 20402747
Bora E (2017) Meta-analysis of social cognition in amyotrophic lateral sclerosis. Cortex 88:1–7. https://doi.org/10.1016/j.cortex.2016.11.012
doi: 10.1016/j.cortex.2016.11.012
pubmed: 28002755
Lulé DE, Aho-Özhan HEA, Vázquez C et al (2019) Story of the ALS-FTD continuum retold: Rather two distinct entities. J Neurol Neurosurg Psychiatry 90:586–589. https://doi.org/10.1136/jnnp-2018-318800
doi: 10.1136/jnnp-2018-318800
pubmed: 30257969
Zucchi E, Ticozzi N, Mandrioli J (2019) Psychiatric symptoms in amyotrophic lateral sclerosis: beyond a motor neuron disorder. Front Neurosci 13:1–11. https://doi.org/10.3389/fnins.2019.00175
doi: 10.3389/fnins.2019.00175
Kawada T, Thakore NJ, Pioro EP (2016) Depression in ALS in a large self-reporting cohort. Neurology 87:1631–1632. https://doi.org/10.1212/01.wnl.0000503501.75283.f1
doi: 10.1212/01.wnl.0000503501.75283.f1
pubmed: 27765825
Mezzapesa DM, D’Errico E, Tortelli R et al (2013) Cortical thinning and clinical heterogeneity in amyotrophic lateral sclerosis. PLoS ONE 8:1–8. https://doi.org/10.1371/journal.pone.0080748
doi: 10.1371/journal.pone.0080748
Zhang J, Yin X, Zhao L et al (2014) Regional alterations in cortical thickness and white matter integrity in amyotrophic lateral sclerosis. J Neurol 261:412–421. https://doi.org/10.1007/s00415-013-7215-5
doi: 10.1007/s00415-013-7215-5
pubmed: 24452838
Proudfoot M, Bede P, Turner MR (2019) Imaging cerebral activity in amyotrophic lateral sclerosis. Front Neurol 9:1148. https://doi.org/10.3389/fneur.2018.01148
D’Ambrosio A, Gallo A, Trojsi F et al (2014) Frontotemporal cortical thinning in amyotrophic lateral sclerosis. Am J Neuroradiol 35:304–310. https://doi.org/10.3174/ajnr.A3753
doi: 10.3174/ajnr.A3753
pubmed: 24113470
pmcid: 7965753
Benbrika S, Doidy F, Carluer L et al (2021) Longitudinal study of cognitive and emotional alterations in amyotrophic lateral sclerosis: clinical and imaging data. Front Neurol 12:1–11. https://doi.org/10.3389/fneur.2021.620198
doi: 10.3389/fneur.2021.620198
Ishaque A, Ta D, Khan M et al (2021) Distinct patterns of progressive gray and white matter degeneration in amyotrophic lateral sclerosis. Human Brain Mapping 43:1519–1534. https://doi.org/10.1002/hbm.25738
Pollatos O, Schandry R, Auer DP, Kaufmann C (2007) Brain structures mediating cardiovascular arousal and interoceptive awareness. Brain Res 1141:178–187. https://doi.org/10.1016/j.brainres.2007.01.026
doi: 10.1016/j.brainres.2007.01.026
pubmed: 17296169
Quadt L, Critchley HD, Garfinkel SN (2018) The neurobiology of interoception in health and disease. Ann N Y Acad Sci 1428:112–128. https://doi.org/10.1111/nyas.13915
doi: 10.1111/nyas.13915
pubmed: 29974959
Wang X, Wu Q, Egan L et al (2019) Anterior insular cortex plays a critical role in interoceptive attention. Elife 15(8):e42265. https://doi.org/10.1101/464867
doi: 10.1101/464867
Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70
doi: 10.1038/nrn2555
Carelli L, Solca F, Tagini S et al (2021) Emotional processing and experience in amyotrophic lateral sclerosis: A systematic and critical review. Brain Sci 11:1–15. https://doi.org/10.3390/brainsci11101356
doi: 10.3390/brainsci11101356
Zhang T, Bai T, Xie W et al (2021) Abnormal connectivity of anterior-insular subdivisions and relationship with somatic symptom in depressive patients. Brain Imaging Behav 15:1760–1768. https://doi.org/10.1007/s11682-020-00371-x
doi: 10.1007/s11682-020-00371-x
pubmed: 32748317
Lischke A, Pahnke R, Mau-Moeller A, Weippert M (2021) Heart rate variability modulates interoceptive accuracy. Front Neurosci 14:612445. https://doi.org/10.3389/fnins.2020.612445
Quadt L, Critchley HD, Garfinkel SN (2018) The neurobiology of interoception in health and disease. Ann N Y Acad Sci 1428:112–28. https://doi.org/10.1111/NYAS.13915
Santangelo G, Vitale C, Baiano C et al (2018) Interoceptive processing deficit: a behavioral marker for subtyping Parkinson’s disease. Parkinsonism Relat Disord 53:64–69. https://doi.org/10.1016/j.parkreldis.2018.05.001
doi: 10.1016/j.parkreldis.2018.05.001
pubmed: 29748110
Raimo S, Boccia M, Di Vita A et al (2020) Interoceptive awareness in focal brain-damaged patients. Neurol Sci 41:1627–1631. https://doi.org/10.1007/s10072-019-04172-z
doi: 10.1007/s10072-019-04172-z
pubmed: 31838632
Gonzalez Campo C, Salamone PC, Rodríguez-Arriagada N et al (2020) Fatigue in multiple sclerosis is associated with multimodal interoceptive abnormalities. Mult Scler J 26:1845–1853. https://doi.org/10.1177/1352458519888881
doi: 10.1177/1352458519888881
Conroy É, Kennedy P, Heverin M et al (2021) Informal caregivers in amyotrophic lateral sclerosis: a multi-centre, exploratory study of burden and difficulties. Brain Sci 11:1–16. https://doi.org/10.3390/brainsci11081094
doi: 10.3390/brainsci11081094
Chiò A, Gauthier A, Calvo A et al (2005) Caregiver burden and patients’ perception of being a burden in ALS. Neurology 64:1780–1782. https://doi.org/10.1212/01.WNL.0000162034.06268.37
doi: 10.1212/01.WNL.0000162034.06268.37
pubmed: 15911811
Vignola A, Guzzo A, Calvo A et al (2008) Anxiety undermines quality of life in ALS patients and caregivers. Eur J Neurol 15:1231–1236. https://doi.org/10.1111/j.1468-1331.2008.02303.x
doi: 10.1111/j.1468-1331.2008.02303.x
pubmed: 18803649
Brooks BR, Miller RG, Swash M, Munsat TL (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler 1:293–299. https://doi.org/10.1080/146608200300079536
doi: 10.1080/146608200300079536
Chiò A, Calvo A, Moglia C et al (2011) Phenotypic heterogeneity of amyotrophic lateral sclerosis: a population based study. J Neurol Neurosurg Psychiatry 82:740–746. https://doi.org/10.1136/jnnp.2010.235952
doi: 10.1136/jnnp.2010.235952
pubmed: 21402743
Czaplinski A, Yen AA, Appel SH (2006) Forced vital capacity (FVC) as an indicator of survival and disease progression in an ALS clinic population. J Neurol Neurosurg Psychiatry 77:390–392. https://doi.org/10.1136/jnnp.2005.072660
doi: 10.1136/jnnp.2005.072660
pubmed: 16484652
pmcid: 2077717
Folstein M, Folstein S, McHugh P (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198. https://doi.org/10.1016/0022-3956(75)90026-6
doi: 10.1016/0022-3956(75)90026-6
pubmed: 1202204
Poletti B, Solca F, Carelli L et al (2016) The validation of the Italian Edinburgh Cognitive and Behavioural ALS Screen (ECAS). Amyotroph Lateral Scler Front Degener 17:489–498. https://doi.org/10.1080/21678421.2016.1183679
doi: 10.1080/21678421.2016.1183679
Laiacona M, Inzaghi MG, De Tanti A, Capitani E (2000) Wisconsin card sorting test: a new global score, with Italian norms, and its relationship with the Weigl sorting test. Neurol Sci 21:279–291. https://doi.org/10.1007/s100720070065
doi: 10.1007/s100720070065
pubmed: 11286040
Barbarotto R, Laiacona M, Frosio R et al (1998) A normative study on visual reaction times and two Stroop colour-word tests. Neurol Sci 19:161–170. https://doi.org/10.1007/bf00831566
doi: 10.1007/bf00831566
Carlesimo C, Caltagirone C, Gainotti G (1996) The Mental Deterioration Battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. Eur Neurol 36:378–384. https://doi.org/10.1159/000117297
doi: 10.1159/000117297
pubmed: 8954307
Orsini A, Grossi D, Capitani E et al (1987) Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Italian J Neurol Sci 8:537–548. https://doi.org/10.1007/BF02333660
doi: 10.1007/BF02333660
Caffarra P, Vezzadini G, Dieci F et al (2002) Rey-Osterrieth complex figure: Normative values in an Italian population sample. Neurol Sci 22:443–447. https://doi.org/10.1007/s100720200003
doi: 10.1007/s100720200003
pubmed: 11976975
Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62. https://doi.org/10.1136/jnnp.23.1.56
doi: 10.1136/jnnp.23.1.56
pubmed: 14399272
pmcid: 495331
Beck AT, Epstein N, Brown G, Steer RA (1988) An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol 56:893–897. https://doi.org/10.1037/0022-006X.56.6.893
doi: 10.1037/0022-006X.56.6.893
pubmed: 3204199
Spinnler H, Tognoni G (1987) Standardizzazione e taratura italiana di test neuropsicologici. Italian J Neurol Sci Suppl 8:1–120
Strong MJ, Abrahams S, Goldstein LH et al (2017) Amyotrophic lateral sclerosis - frontotemporal spectrum disorder (ALS-FTSD): revised diagnostic criteria. Amyotroph Lateral Scler Front Degener 18:153–174. https://doi.org/10.1080/21678421.2016.1267768
doi: 10.1080/21678421.2016.1267768
Dunn BD, Stefanovitch I, Buchan K et al (2009) A reduction in positive self-judgment bias is uniquely related to the anhedonic symptoms of depression. Behav Res Ther 47:374–381. https://doi.org/10.1016/j.brat.2009.01.016
doi: 10.1016/j.brat.2009.01.016
pubmed: 19237152
pmcid: 2679118
Pollatos O, Traut-Mattausch E, Schandry R (2009) Differential effects of anxiety and depression on interoceptive accuracy. Depress Anxiety 26:167–173. https://doi.org/10.1002/da.20504
doi: 10.1002/da.20504
pubmed: 19152366
Shaffer F, Ginsberg JP (2017) An overview of heart rate variability metrics and norms. Front Public Health 5:258. https://doi.org/10.3389/fpubh.2017.00258
doi: 10.3389/fpubh.2017.00258
pubmed: 29034226
pmcid: 5624990
Longarzo M, D’Olimpio F, Chiavazzo A et al (2015) The relationships between interoception and alexithymic trait. The Self-Awareness Questionnaire in healthy subjects. Front Psych 6:1149. https://doi.org/10.3389/fpsyg.2015.01149
Mehling WE, Price C, Daubenmier JJ et al (2012) The Multidimensional Assessment of Interoceptive Awareness (MAIA). PLoS ONE 7:e48230. https://doi.org/10.1371/journal.pone.0048230
Calì G, Ambrosini E, Picconi L et al (2015) Investigating the relationship between interoceptive accuracy, interoceptive awareness, and emotional susceptibility. Front Psychol 6:1–13. https://doi.org/10.3389/fpsyg.2015.01202
doi: 10.3389/fpsyg.2015.01202
Bressi C, Taylor G, Parker J et al (1996) Cross validation of the factor structure of the 20-item Toronto Alexithymia Scale: An Italian multicenter study. J Psychosom Res 41:551–559. https://doi.org/10.1016/S0022-3999(96)00228-0
doi: 10.1016/S0022-3999(96)00228-0
pubmed: 9032718
Raimo S, Trojano L, Spitaleri D et al (2014) Apathy in multiple sclerosis: a validation study of the apathy evaluation scale. J Neurol Sci 347:295–300. https://doi.org/10.1016/j.jns.2014.10.027
doi: 10.1016/j.jns.2014.10.027
pubmed: 25455303
Santangelo G, Barone P, Cuoco S et al (2014) Apathy in untreated, de novo patients with Parkinson’s disease: validation study of Apathy Evaluation Scale. J Neurol 261:2319–2328. https://doi.org/10.1007/s00415-014-7498-1
doi: 10.1007/s00415-014-7498-1
pubmed: 25228003
Kimura F, Fujimura C, Ishida S et al (2006) Progression rate of ALSFRS-R at time of diagnosis predicts survival time in ALS. Neurology 66:265–267. https://doi.org/10.1212/01.wnl.0000194316.91908.8a
doi: 10.1212/01.wnl.0000194316.91908.8a
pubmed: 16434671
Lange CG, James W (1967) The emotions. Hafner
Ricciardi L, Ferrazzano G, Demartini B et al (2016) Know thyself: exploring interoceptive sensitivity in Parkinson’s disease. J Neurol Sci 364:110–115. https://doi.org/10.1016/j.jns.2016.03.019
doi: 10.1016/j.jns.2016.03.019
pubmed: 27084227
Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013) Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cereb Cortex 23:739–749. https://doi.org/10.1093/cercor/bhs065
doi: 10.1093/cercor/bhs065
pubmed: 22437053
Sedda A (2014) Disorders of emotional processing in amyotrophic lateral sclerosis. Curr Opin Neurol 27:659–665
doi: 10.1097/WCO.0000000000000147