Skip to main content

Advertisement

Log in

Inability to Process Negative Emotions in Cerebellar Damage: a Functional Transcranial Doppler Sonographic Study

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

Recent studies have implicated the cerebellum as part of a circuitry that is necessary to modulate higher order and behaviorally relevant information in emotional domains. However, little is known about the relationship between the cerebellum and emotional processing. This study examined cerebellar function specifically in the processing of negative emotions. Transcranial Doppler ultrasonography was performed to detect selective changes in middle cerebral artery flow velocity during emotional stimulation in patients affected by focal or degenerative cerebellar lesions and in matched healthy subjects. Changes in flow velocity during non-emotional (motor and cognitive tasks) and emotional (relaxing and negative stimuli) conditions were recorded. In the present study, we found that during negative emotional task, the hemodynamic pattern of the cerebellar patients was significantly different to that of controls. Indeed, whereas relaxing stimuli did not elicit an increase in mean flow velocity in any group, negative stimuli increased the mean flow velocity in the right compared with left middle cerebral artery only in the control group. The patterns by which mean flow velocity increased during the motor and cognitive tasks were similar within patients and controls. These findings support that the cerebellum is part of a network that gives meaning to external stimuli, and this particular involvement in processing negative emotional stimuli corroborates earlier phylogenetic hypotheses, for which the cerebellum is part of an older circuit in which negative emotions are crucial for survival and prepare the organism for rapid defense.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Borod JC, Cicero BA, Obler LK, Welkowitz J, Erhan HM, Santschi C, et al. Right hemisphere emotional perception: evidence across multiple channels. Neuropsychology. 1998;12:446–58.

    Article  CAS  PubMed  Google Scholar 

  2. Abbott JD, Cumming G, Fidler F, Lindell AK. The perception of positive and negative facial expressions in unilateral brain-damaged patients: a meta-analysis. Laterality. 2013;18:437–59.

    PubMed  Google Scholar 

  3. Kumar D, Srinivasan N. Emotion perception is mediated by spatial frequency content. Emotion. 2011;11:1144.

    Article  PubMed  Google Scholar 

  4. Önal-Hartmann C, Pauli P, Ocklenburg S, Güntürkün O. The motor side of emotions: investigating the relationship between hemispheres, motor reactions and emotional stimuli. Psychol Res. 2012;76:311–6.

    Article  PubMed  Google Scholar 

  5. Sedda A, Rivolta D, Scarpa P, Burt M, Frigerio E, Zanardi G, et al. Ambiguous emotion recognition in temporal lobe epilepsy: the role of expression intensity. Cogn Affect Behav Neurosci. 2013;13:452–63.

    Article  PubMed  Google Scholar 

  6. Shobe ER. Independent and collaborative contributions of the cerebral hemispheres to emotional processing. Front Hum Neurosci. 2014;22(8):230.

    Google Scholar 

  7. Najt P, Bayer U, Hausmann M. Models of hemispheric specialization in facial emotion perception are evaluation. Emotion. 2013;13:159.

    Article  PubMed  Google Scholar 

  8. Phan KL, Wager T, Taylor SF, Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and FMRI. NeuroImage. 2002;16:331–48.

    Article  PubMed  Google Scholar 

  9. Murphey FC, Nimmo-Smith I, Lawrence AD. Functional neuroanatomy of emotions: a meta-analysis. Cogn Affect Behav Neurosci. 2003;3:207–33.

    Article  Google Scholar 

  10. Park JY, Gu BM, Kang DH, Shin YW, Choi CH, Lee JM, et al. Integration of cross-modal emotional information in the human brain: an fMRI study. Cortex. 2008;46(2):161–9.

    Article  PubMed  Google Scholar 

  11. Schmahmann JD, Pandya DN. The cerebrocerebellar system. Int Rev Neurobiol. 1997;4:31–60.

    Article  Google Scholar 

  12. Schmahmann JD, Sherman J. The cerebellar cognitive affective syndrome. Brain. 1998;121:561–79.

    Article  PubMed  Google Scholar 

  13. Baumann O, Mattingley JB. Functional topography of primary emotion processing in the human cerebellum. Neuroimage. 2012;61:805–11.

    Article  PubMed  Google Scholar 

  14. Schienle A, Scharmüller W. Cerebellar activity and connectivity during the experience of disgust and happiness. Neuroscience. 2013;246:375–81.

    Article  CAS  PubMed  Google Scholar 

  15. Gur RC, Skolnick BE, Gur RE. Effects of emotional discrimination tasks on cerebral blood flow: regional activation and its relation to performance. Brain Cogn. 1994;25:271–86.

    Article  CAS  PubMed  Google Scholar 

  16. Partiot A, Grafman J, Sadato N, Wachs J, Hallett M. Brain activation during the generation of non-emotional and emotional plans. Neuro Rep. 1995;6:1397–400.

    CAS  Google Scholar 

  17. George MS, Ketter TA, Parekh PI, Horwitz B, Herscovitch P, Post RM. Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry. 1995;152:341–51.

    Article  CAS  PubMed  Google Scholar 

  18. Troisi E, Peppe A, Pierantozzi M, Matteis M, Vernieri F, Stanzione P, et al. Emotion processing in Parkinson’s disease. A study using functional transcranial doppler sonography. J Neurol. 2002;249:993–1000.

    Article  CAS  PubMed  Google Scholar 

  19. Aaslid R, Markwalder TH, Nornes H. Noninvasive transcranial doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982;57:769–74.

    Article  CAS  PubMed  Google Scholar 

  20. Bishop CC, Powell S, Rutt D, Browse NL. Transcranial doppler measurement of middle cerebral artery blood flow velocity: a validation study. Stroke. 1986;17:913–5.

    Article  CAS  PubMed  Google Scholar 

  21. Droste DW, Harders AG, Rastogi E. A transcranial Doppler study of blood flow velocity in the middle cerebral arteries performed at rest and during mental activities. Stroke. 1989;20:1005–11.

    Article  CAS  PubMed  Google Scholar 

  22. Klingelhöfer J, Matzander G, Sander D, Schwarze J, Boecker H, Bischoff C. Assessment of functional hemispheric asymmetry by bilateral simultaneous cerebral blood flow velocity monitoring. J Cereb Blood Flow Metab. 1997;17(5):577–85.

    Article  PubMed  Google Scholar 

  23. Silvestrini M, Cupini LM, Matteis M, Troisi E, Caltagirone C. Bilateral simultaneous assessment of cerebral flow velocity during mental activity. J Cereb Blood Flow Metab. 1994;14:643–8.

    Article  CAS  PubMed  Google Scholar 

  24. Troisi E, Silvestrini M, Matteis M, Monaldo BC, Vernieri F, Caltagirone C. Emotion-related cerebral asymmetry: hemodynamics measured by functional ultrasound. J Neurol. 1999;246(12):1172–6.

    Article  CAS  PubMed  Google Scholar 

  25. Appollonio IM, Grafman J, Schwartz V, Massaquoi S, Hallett M. Memory in patients with cerebellar degeneration. Neurology. 1993;43:1536–44.

    Article  CAS  PubMed  Google Scholar 

  26. Caltagirone C, Gainotti G, Carlesimo G, Parnetti L, Fadda L, Gallassi R, et al. The mental deterioration battery: description of an instrument of the neuropsychological diagnosis. Arch Psicol Neurol Psichiatr. 1995;56:461–70.

    Google Scholar 

  27. Wechsler D. Scala di intelligenza Wechsler per adulti rivisitata (WAIS-R). Organizzazioni Speciali: Manuale, Firenze; 1981.

    Google Scholar 

  28. Markus HS, Harrison MJG. Estimation of cerebrovascular reactivity using transcranical Doppler, including the use of breath-holding as vasodilatory stimulus. Stroke. 1992;23:668–73.

    Article  CAS  PubMed  Google Scholar 

  29. Rihs F, Gutbrod K, Gutbrod B, Steiger HJ, Sturzenegger M, Mattle HP. Determination of cognitive hemispheric dominance by “stereo” transcranial Doppler sonography. Stroke. 1995;26(1):70–3.

    Article  CAS  PubMed  Google Scholar 

  30. Rihs F, Sturzenegger M, Gutbrod K, Schroth G, Mattle HP. Determination of language dominance: Wada test confirms functional transcranial Doppler sonography. Neurology. 1999;52(8):1591–6.

    Article  CAS  PubMed  Google Scholar 

  31. Molinari M, Leggio MG, Silveri MC. Verbal fluency and agrammatism. Int Rev Neurobiol. 1997;41:325–39.

    Article  CAS  PubMed  Google Scholar 

  32. Leggio MG, Silveri MC, Petrosini L, Molinari M. Phonological grouping is specifically affected in cerebellar patients: a verbal fluency study. J Neurol Neurosurg Psychiatry. 2000;69(1):102–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Turner BM, Paradiso S, Marvel CL, Pierson R, Boles Ponto LL, Hichwa RD, et al. The cerebellum and emotional experience. Neuropsychologia. 2007;45(6):1331–41.

    Article  PubMed Central  PubMed  Google Scholar 

  34. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.

    Article  PubMed  Google Scholar 

  35. Schmahmann JD, Dojon J, Toga AW, Petrides M, Evans CA. MRI atlas of the human cerebellum. San Diego: Academic Press; 2000.

    Google Scholar 

  36. Dimitrova A, Weber J, Redies C, Kindsvater K, Maschke M, Kolb FP, et al. MRI atlas of the human cerebellar nuclei. Neuroimage. 2002;17:240–55.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

This work was supported by the Italian Ministry of Health (RC08G).

Conflict of interest

The authors have no conflict of interest to declare.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Leggio.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lupo, M., Troisi, E., Chiricozzi, F.R. et al. Inability to Process Negative Emotions in Cerebellar Damage: a Functional Transcranial Doppler Sonographic Study. Cerebellum 14, 663–669 (2015). https://doi.org/10.1007/s12311-015-0662-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-015-0662-z

Keywords

Navigation