Abstract
It has been well demonstrated that the cerebellum is associated with cognitive and affective processing as well as the traditionally conceptualized motor function. In the present chapter, we explore the behavioral and neurobiological implications of a common congenital cerebellar condition, Chiari malformation Type I, on cognitive and affective processing. We also emphasize the associations between Chiari-related chronic pain, cognitive dysfunction, and emotion dysregulation. Based on our review of the literature, we argue that chronic pain can account for a substantial amount of the cognitive dysfunction and emotion dysregulation in Chiari malformation Type I. Yet, there also exists aspects of Chiari-related cognitive dysfunction and emotion dysregulation that appear to be at least partially independent of chronic pain and more directly associated with abnormalities in cerebrospinal fluid flow dynamics and cerebro-cerebellar communication pathways.
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Notes
- 1.
Effect sizes estimated using mean difference and standard deviation data provided in the article.
- 2.
- 3.
The authors speculated that this was because neuropathic pain networks underlying the central sensitization of pain are not directly targeted by decompression surgery.
References
Allen PA, Houston JR, Pollock JW et al (2014) Task-specific and general cognitive effects in Chiari malformation type I. PLoS One 9(4):e94844. https://doi.org/10.1371/journal.pone.0094844
Allen P, Delahanty D, Kaut K et al (2018) Chiari 1000 registry project: assessment of surgical outcome on self-focused attention, pain, and delayed recall. Psychol Med 48(10):1634–1643. https://doi.org/10.1017/S0033291717003117
Alperin N, Loftus J, Oliu C et al (2015) Imaging-based features of headaches in Chiari malformation type I. Neurosurgery 77(1):96–103. https://doi.org/10.1227/NEU.0000000000000740
Barbato M, Liu L, Cadenhead KS et al (2015) Theory of mind, emotion recognition and social perception in individuals at clinical high risk for psychosis: findings from the NAPLS-2 cohort. Schizophrenia Res Cognition 2(3):133–139. https://doi.org/10.1016/j.scog.2015.04.004
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system – a technical review. NMR Biomed 15(7–8):435–455. https://doi.org/10.1002/nbm.782
Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50(1–3):7–15
Benton AL, Sivan AB, Hamsher KS, Varney NR, Spreen O (1994) Contributions to neuropsychological assessment. Oxford University Press, Oxford
Bihan D, Mangin J, Poupon C et al (2001) Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 13(4):534–546. https://doi.org/10.1002/jmri.1076
Biswas D, Eppelheimer MS, Houston JR et al (2019) Quantification of cerebellar crowding in type I Chiari malformation. Ann Biomed Eng 47(3):731–743. https://doi.org/10.1007/s10439-018-02175-z
Bushnell CM, Čeko M, Low LA (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 14(7):502–511. https://doi.org/10.1038/nrn3516
Clausi S, Olivito G, Lupo M, Siciliano L, Bozzali M, Leggio M (2019) The cerebellar predictions for social interactions: theory of mind abilities in patients with degenerative cerebellar atrophy. Front Cell Neurosci 12:510. https://doi.org/10.3389/fncel.2018.00510
Coricelli G (2005) Two-levels of mental states attribution: from automaticity to voluntariness. Neuropsychologia 43(2):294–300. https://doi.org/10.1016/j.neuropsychologia.2004.11.015
Dehaene S, Changeux J-P (2011) Experimental and theoretical approaches to conscious processing. Neuron 70(2):200–227. https://doi.org/10.1016/j.neuron.2011.03.018
Drozdick LW, Raiford SE, Wahlstrom D, Weiss LG (2018) The Wechsler adult intelligence scale—fourth edition and the Wechsler memory scale—fourth edition. In: Flanagan D, McDonough E (eds) Contemporary intellectual assessment: theories, tests, and issues, 4th edn. The Guilford Press, New York, pp 486–511
Duenas M, Ojeda B, Salazar A, Mico JA, Failde I (2016) A review of chronic pain impact on patients, their social environment and the health care system. J Pain Res 9:457–467. https://doi.org/10.2147/jpr.s105892
Dworkin RH, Turk DC, Revicki DA et al (2009) Development and initial validation of an expanded and revised version of the short-form McGill pain questionnaire (SF-MPQ-2). Pain 144(1–2):35–42. https://doi.org/10.1016/j.pain.2009.02.007
Eason R, Harter R, White C (1969) Effects of attention and arousal on visually evoked cortical potentials and reaction time in man. Physiol Behav 4:283–289. https://doi.org/10.1016/0031-9384(69)90176-0
Eppelheimer MS, Houston JR, Bapuraj JR et al (2018) A retrospective 2D morphometric analysis of adult female Chiari type I patients with commonly reported and related conditions. Front Neuroanat 12:2. https://doi.org/10.3389/fnana.2018.00002
Eppelheimer MS, Biswas D, Braun AM et al (2019) Quantification of changes in brain morphology following posterior fossa decompression surgery in women treated for Chiari malformation type 1. Neuroradiology 61(9):1011–1022. https://doi.org/10.1007/s00234-019-02206-z
Fairbank J, Couper J, Davies J, O’Brien J (1980) The Oswestry low back pain disability questionnaire. Physiotherapy 66(8):271–273
Fitzpatrick P, Frazier JA, Cochran D, Mitchell T, Coleman C, Schmidt RC (2018) Relationship between theory of mind, emotion recognition, and social synchrony in adolescents with and without autism. Front Psychol 9:1337. https://doi.org/10.3389/fpsyg.2018.01337
Fontaine D, Almairac F, Santucci S et al (2018) Dural and pial pain-sensitive structures in humans: new inputs from awake craniotomies. Brain 141(4):1040–1048. https://doi.org/10.1093/brain/awy005
Furuya K, Sano K, Segawa H, Ide K, Yoneyama H (1998) Symptomatic tonsillar ectopia. J Neurol Neurosurg Psychiatry 64:221–226
García M, Amayra I, Lázaro E et al (2018a) Comparison between decompressed and non-decompressed Chiari malformation type I patients: a neuropsychological study. Neuropsychologia 121:135–143. https://doi.org/10.1016/j.neuropsychologia.2018.11.002
García M, Lázaro E, López-Paz JF et al (2018b) Cognitive functioning in Chiari malformation type I without posterior fossa surgery. Cerebellum 17(5):564–574. https://doi.org/10.1007/s12311-018-0940-7
Garcia MA, Allen PA, Li X et al (2019) An examination of pain, disability, and the psychological correlates of Chiari malformation pre- and post-surgical correction. Disabil Health J 12(4):649–656. https://doi.org/10.1016/j.dhjo.2019.05.004
García M, Lázaro E, Amayra I et al (2020a) Analysis of visuospatial abilities in Chiari malformation type I. Cerebellum 19(1):6–15. https://doi.org/10.1007/s12311-019-01056-y
García M, Amayra I, López-Paz JF et al (2020b) Social cognition in Chiari malformation type I: a preliminary characterization. Cerebellum 19(3):392–400. https://doi.org/10.1007/s12311-020-01117-7
García M, Eppelheimer MS, Houston JR, et al. Adult age differences in self-reported pain and anterior CSF space in Chiari malformation. Cerebellum Published online 2021. https://doi.org/10.1007/s12311-021-01289-w
González JLB, Campa-Santamarina JMT (2018) Anomalies in the cognitive-executive functions in patients with Chiari malformation type I. Psicothema 30(3):316–321. https://doi.org/10.7334/psicothema2017.401
Haefeli M, Elfering A (2006) Pain assessment. Eur Spine J 15(Suppl 1):S17–S24. https://doi.org/10.1007/s00586-005-1044-x
Happé FGE (1994) An advanced test of theory of mind: understanding of story characters’ thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. J Autism Dev Disord 24(2):129–154. https://doi.org/10.1007/bf02172093
Harrington R, Loffredo DA (2010) Insight, rumination, and self-reflection as predictors of Well-being. J Psychology 145(1):39–57. https://doi.org/10.1080/00223980.2010.528072
Heiss J, Suffredini G, Bakhtian K, Sarntinoranont M, Oldfield E (2012) Normalization of hindbrain morphology after decompression of Chiari malformation type I. J Neurosurg 117(5):942–946. https://doi.org/10.3171/2012.8.JNS111476
Henry J, Crawford J (2005) The short-form version of the depression anxiety stress scales (DASS-21): construct validity and normative data in a large non-clinical sample. Br J Clin Psychol 44(2):227–239. https://doi.org/10.1348/014466505X29657
Hoche F, Guell X, Sherman JC, Vangel MG, Schmahmann JD (2016) Cerebellar contribution to social cognition. Cerebellum 15(6):732–743. https://doi.org/10.1007/s12311-015-0746-9
Hoche F, Guell X, Vangel M, Sherman J, Schmahmann J (2018) The cerebellar cognitive affective/Schmahmann syndrome scale. Brain 141(1):248–270. https://doi.org/10.1093/brain/awx317
Holmes SC, Gonzalez A, Allen PA, Johnson DM (2019) Utilizing group acceptance and commitment therapy (ACT) to address chronic pain, coping, and functioning for patients with Chiari malformation: a case example. Prof Psychology Res Pract 50(5):296–306. https://doi.org/10.1037/pro0000247
Houston J, Eppelheimer M, Pahlavian S et al (2018a) A morphometric assessment of type I Chiari malformation above the McRae line: a retrospective case-control study in 302 adult female subjects. J Neuroradiol 45(1):23–31. https://doi.org/10.1016/j.neurad.2017.06.006
Houston JR, Hughes ML, Lien M-C et al (2018b) An electrophysiological study of cognitive and emotion processing in type I Chiari malformation. Cerebellum 45(1):23–31. https://doi.org/10.1007/s12311-018-0923-8
Houston JR, Pollock JW, Lien M-C, Allen PA (2018c) Emotional arousal deficit or emotional regulation bias? An electrophysiological study of age-related differences in emotion perception. Exp Aging Res 44(3):187–205. https://doi.org/10.1080/0361073X.2018.1449585
Houston JR, Allen PA, Rogers JM et al (2019a) Type I Chiari malformation, RBANS performance, and brain morphology: connecting the dots on cognition and macrolevel brain structure. Neuropsychology 33(5):725–738. https://doi.org/10.1037/neu0000547
Houston JR, Allen NJ, Eppelheimer MS et al (2019b) Evidence for sex differences in morphological abnormalities in type I Chiari malformation. Neuroradiol J 32(6):458–466. https://doi.org/10.1177/1971400919857212
Houston JR, Hughes ML, Bennett IJ et al (2020) Evidence of neural microstructure abnormalities in type I Chiari malformation: associations among fiber tract integrity, pain, and cognitive dysfunction. Pain Med 21(10):2323–2335. https://doi.org/10.1093/pm/pnaa094
Houston ML, Houston JR, Sakaie K et al (2021) Functional connectivity abnormalities in type I Chiari: associations with cognition and pain. Brain Commun 3(3):fcab137. https://doi.org/10.1093/braincomms/fcab137
Ibrahimy A, Huang C-WC-W, Bezuidenhout AF, Allen PA, Bhadelia RA, Loth F (2021) Association between resistance to cerebrospinal fluid flow near the foramen magnum and cough-associated headache in adult Chiari malformation type I. J Biomech Eng 143(5):051003. https://doi.org/10.1115/1.4049788
Inglese M, Bester M (2010) Diffusion imaging in multiple sclerosis: research and clinical implications. NMR Biomed 23(7):865–872. https://doi.org/10.1002/nbm.1515
Karagöz F, Isgi N, Sencer SK (2002) Morphometric measurements of the cranium in patients with Chiari type I malformation and comparison with the Normal population. Acta Neurochir 144:165–171
Kessler H, Bayerl P, Deighton RM, Traue HC (2002) Facially expressed emotion labeling (FEEL): PC-Gestützter test zur Emotionserkennung. [facially expressed emotion labeling (FEEL): a computer-based test for emotion recognition.]. Verhaltenstherapie Verhaltensmedizin 23(3):297–306
Khalsa S, Geh N, Martin B et al (2018) Morphometric and volumetric comparison of 102 children with symptomatic and asymptomatic Chiari malformation type I. J Neurosurg Pediatr 21(1):65–71. https://doi.org/10.3171/2017.8.PEDS17345
Klein R, Hopewell CA, Oien M (2014) Chiari malformation type I: a neuropsychological case study. Mil Med 179(6):e712–e718. https://doi.org/10.7205/MILMED-D-13-00227
Krishna V, Sammartino F, Yee P et al (2016) Diffusion tensor imaging assessment of microstructural brainstem integrity in Chiari malformation type I. J Neurosurg 125(5):1112–1119. https://doi.org/10.3171/2015.9.JNS151196
Krolak-Salmon P, Fischer C, Vighetto A, Mauguiere F (2001) Processing of facial emotional expression: Spatio-temporal data as assessed by scalp event-related potentials. Eur J Neurosci 13(5):987–994. https://doi.org/10.1046/j.0953-816x.2001.01454.x/full
Kumar M, Rathore R, Srivastava A, Yadav S, Behari S, Gupta R (2011) Correlation of diffusion tensor imaging metrics with neurocognitive function in Chiari I malformation. World Neurosurg 76(1–2):189–194. https://doi.org/10.1016/j.wneu.2011.02.022
Kurtcan S, Alkan A, Yetis H et al (2018) Diffusion tensor imaging findings of the brainstem in subjects with tonsillar ectopia. Acta Neurol Belg 118(1):39–45. https://doi.org/10.1007/s13760-017-0792-9
Lázaro E, García M, Ibarrola A et al (2018) Chiari type I malformation associated with verbal fluency impairment. J Speech Lang Hear Res 61(10):2458–2466. https://doi.org/10.1044/2018_JSLHR-S-17-0465
Manto M, Mariën P (2015) Schmahmann’s syndrome - identification of the third cornerstone of clinical ataxiology. Cerebellum Ataxias 2:2. https://doi.org/10.1186/s40673-015-0023-1
Melzack R (1987) The short-form McGill pain questionnaire. Pain 30(2):191–197
Milhorat TH, Chou MW, Trinidad EM et al (1999) Chiari I malformation redefined: clinical and radiographic findings for 364 symptomatic patients. Neurosurgery 44(5):1005–1017. https://doi.org/10.1097/00006123-199905000-00042
Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51(5):527–539. https://doi.org/10.1016/j.neuron.2006.08.012
Moulton EA, Schmahmann JD, Becerra L, Borsook D (2010) The cerebellum and pain: passive integrator or active participator? Brain Res Rev 65(1):14–27. https://doi.org/10.1016/j.brainresrev.2010.05.005
Mueller DM, Oro’ JJ (2004) Prospective analysis of presenting symptoms among 265 patients with radiographic evidence of Chiari malformation type I with or without Syringomyelia. J Am Acad Nurse Prac 16(3):134–138. https://doi.org/10.1111/j.1745-7599.2004.tb00384.x
Mueller DM, Oro’ JJ (2013) The Chiari symptom profile: development and validation of a Chiari-/Syringomyelia-Specific Questionnaire. J Neurosci Nurs 45(4):205–210. https://doi.org/10.1097/JNN.0b013e3182986573
Noseda R, Melo-Carrillo A, Nir R-R, Strassman AM, Burstein R (2019) Non-trigeminal nociceptive innervation of the posterior dura: implications to occipital headache. J Neurosci 39(10):1867–1880. https://doi.org/10.1523/jneurosci.2153-18.2018
Novegno F, Caldarelli M, Massa A et al (2008) The natural history of the Chiari type I anomaly. J Neurosurg Pediatr 2(3):179–187. https://doi.org/10.3171/PED/2008/2/9/179
Oakley BFM, Brewer R, Bird G, Catmur C (2016) Theory of mind is not theory of emotion: a cautionary note on the Reading the mind in the eyes test. J Abnorm Psychol 125(6):818–823. https://doi.org/10.1037/abn0000182
Ossipov MH, Dussor GO, Porreca F (2010) Central modulation of pain. J Clin Invest 120(11):3779–3787. https://doi.org/10.1172/jci43766
Overwalle FV, Baetens K, Mariën P, Vandekerckhove M (2014) Social cognition and the cerebellum: a meta-analysis of over 350 fMRI studies. NeuroImage 86:554–572. https://doi.org/10.1016/j.neuroimage.2013.09.033
Pashler H (1984) Processing stages in overlapping tasks: evidence for a central bottleneck. J Exp Psychol 10(3):358–377
Pashler H (1994) Dual-task interference in simple tasks: data and theory. Psychol Bull 116(2):220–244
Pearce M, Oda N, Mansour A, Bhalerao S (2006) Cognitive disorder NOS with Arnold-Chiari I malformation. Psychosomatics 47(1):88–89. https://doi.org/10.1176/appi.psy.47.1.88
Perner J, Wimmer H (1985) “John thinks that Mary thinks that…” attribution of second-order beliefs by 5- to 10-year-old children. J Exp Child Psychol 39(3):437–471. https://doi.org/10.1016/0022-0965(85)90051-7
Peters A (2002) The effects of normal aging on myelin and nerve fibers: a review. J Neurocytol 31(8–9):581–593
Pollock JW, Khoja N, Kaut KP, Lien M-C, Allen PA (2012) Electrophysiological evidence for adult age-related sparing and decrements in emotion perception and attention. Front Integr Neurosci 6:60. https://doi.org/10.3389/fnint.2012.00060
Randolph C. RBANS UPDATE: repeatable battery for the assessment of neuropsychological status: manual. NCS Pearson, Inc. Published online 2012
Rellecke J, Palazova M, Sommer W, Schacht A (2011) On the automaticity of emotion processing in words and faces: event-related brain potentials evidence from a superficial task. Brain Cogn 77(1):23–32. https://doi.org/10.1016/J.BANDC.2011.07.001
Rellecke J, Sommer W, Schacht A (2012) Does processing of emotional facial expressions depend on intention? Time-resolved evidence from event-related brain potential. Biol Psychol 90(1):23–32. https://doi.org/10.1016/J.BIOPSYCHO.2012.02.002
Rey A (1941) L’examen psychologique dans les cas d’encéphalopathie traumatique. (Les problems.). [The psychological examination in cases of traumatic encepholopathy. Problems.]. Arch Psychol 28:215–285
Riva D, Usilla A, Saletti V, Esposito S, Bulgheroni S (2011) Can Chiari malformation negatively affect higher mental functioning in developmental age? Neurol Sci 32(S3):307–309. https://doi.org/10.1007/s10072-011-0779-x
Rogers JM, Savage G, Stoodley MA (2018) A systematic review of cognition in Chiari I malformation. Neuropsychol Rev 28(2):176–187. https://doi.org/10.1007/s11065-018-9368-6
Ruff RM, Light RH, Parker SB, Levin HS (1996) Benton controlled Oral word association test: reliability and updated norms. Arch Clin Neuropsychol 11(4):329–338
Ruscheweyh R, Kühnel M, Filippopulos F, Blum B, Eggert T, Straube A (2014) Altered experimental pain perception after cerebellar infarction. Pain 155(7):1303–1312. https://doi.org/10.1016/j.pain.2014.04.006
Sahuquillo J, Rubio E, Poca M-A, Rovira A, Rodriquez-Baeza A, Cervera C (1994) Posterior fossa reconstruction: a surgical technique for the treatment of Chiari I malformation and Chiari I/Syringomyelia complex - preliminary results and magnetic resonance imaging quantitative assessment of hindbrain migration. Neurosurgery 35(5):874–884
Schmahmann JD, Sherman JC (1998) The cerebellar cognitive affective syndrome. Brain 121(4):561–579. https://doi.org/10.1093/brain/121.4.561
Schmidt M. Rey auditory verbal learning test: RAVLT: a handbook. Western Psychological Services. Published online 2009
Shaffer N, Martin B, Rocque B et al (2014) Cerebrospinal fluid flow impedance is elevated in type I Chiari malformation. J Biomech Eng 136(2):021012. https://doi.org/10.1115/1.4026316
Smith B, Strahle J, Bapuraj J, Muraszko K, Garton H, Maher C (2013) Distribution of cerebellar tonsil position: implications for understanding Chiari malformation. J Neurosurg 119(3):812–819. https://doi.org/10.3171/2013.5.JNS121825
Song S-K, Yoshino J, Le TQ et al (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. NeuroImage 26(1):132–140. https://doi.org/10.1016/j.neuroimage.2005.01.028
Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cognitive Neurosci 10(5):640–656. https://doi.org/10.1162/089892998562942
Tottenham N, Tanaka JW, Leon AC et al (2009) The NimStim set of facial expressions: judgments from untrained research participants. Psychiatry Res 168(3):242–249. https://doi.org/10.1016/j.psychres.2008.05.006
Tubbs RS, Oakes WJ (2013a) Introduction and classification of the Chiari malformations. In: Tubbs RS, Oakes WJ (eds) The Chiari malformations. Springer, New York. https://doi.org/10.1007/978-1-4614-6369-6_1
Tubbs SR, Oakes WJ (2013b) The Chiari malformations: a historical context. In: Tubbs SR, Oakes WJ (eds) The Chiari malformations. Springer, New York. https://doi.org/10.1007/978-1-4614-6369-6_2
Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiat Scand 67(6):361–370. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x
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Houston, J.R., Maleki, J., Loth, F., Klinge, P.M., Allen, P.A. (2022). Influence of Pain on Cognitive Dysfunction and Emotion Dysregulation in Chiari Malformation Type I. In: Adamaszek, M., Manto, M., Schutter, D.J.L.G. (eds) The Emotional Cerebellum . Advances in Experimental Medicine and Biology, vol 1378. Springer, Cham. https://doi.org/10.1007/978-3-030-99550-8_11
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