Skip to main content

Advertisement

Log in

Subarachnoid hemorrhage and visuospatial and visuoperceptive impairment: disruption of the mirror neuron system

  • Brief Communication
  • Published:
Brain Imaging and Behavior Aims and scope Submit manuscript

Abstract

Nearly 20 % of patients who suffer a subarachnoid hemorrhage (SAH) still display cognitive impairment even a year after follow-up. Visuospatial and visuoperceptive domains may be impaired in this cognitive impairment and may not have been fully studied in these patients. Furthermore, these cognitively impaired domains have been associated with activity in the so-called mirror neuron system (MNS). The aim of the study is to analyze the pattern of brain activity with an MNS task-based functional magnetic resonance imaging (fMRI) study in SAH patients. A complete neuropsychological assessment and fMRI study (with observation and execution conditions) were performed in patients with a history of SAH registered in the database of the Hospital Universitario de Canarias and a healthy control group. The patients had to meet all the following inclusion criteria for the study (less than 50 years old; SAH with a Fisher score 1–3; no vasospasm or ischemia; minimum follow-up of one year). Twelve SAH patients were studied. Three of which displayed visuospatial/visuoperceptive impairment. fMRI study showed the presence of higher activity in MNS regions in these patients than in patients with normal visuospatial/visuoperceptive functions. Furthermore, there was a negative correlation between the test scores and brain activity in premotor regions of the studied patients. SAH patients with visuospatial/visuoperceptive impairment have greater activity in the MNS regions. This finding may be associated with a subcortical dysfunction, leading to a disruption of neural activity and less efficient behavior of this brain network.

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
Fig. 3

References

  • Albert, M. L. (1973). A simple test of visual neglect. Neurology, 23(6), 658–664.

    Article  CAS  PubMed  Google Scholar 

  • Bakker, A., Krauss, G. L., Albert, M. S., Speck, C. L., Jones, L. R., Stark, C. E., et al. (2012). Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron, 74(3), 467–474. doi:10.1016/j.neuron.2012.03.023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benton, A. L., Hamsher KdeS, V. N., & O, S. (1983). Contributions to neuropsychological assessment: a clinical manual. Nueva York: Oxford University Press.

    Google Scholar 

  • Boerboom, W., Heijenbrok-Kal, M. H., Khajeh, L., van Kooten, F., & Ribbers, G. M. (2014). Differences in cognitive and emotional outcomes between patients with perimesencephalic and aneurysmal subarachnoid haemorrhage. Journal of Rehabilitation Medicine, 46(1), 28–32. doi:10.2340/16501977–1236.

    Article  PubMed  Google Scholar 

  • Brunet-Gouet, E., & Decety, J. (2006). Social brain dysfunctions in schizophrenia: a review of neuroimaging studies. Psychiatry Research, 148(2–3), 75–92. doi:10.1016/j.pscychresns.2006.05.001.

    Article  PubMed  Google Scholar 

  • Buxbaum, L. J., Kyle, K. M., & Menon, R. (2005). On beyond mirror neurons: internal representations subserving imitation and recognition of skilled object-related actions in humans. Brain research. Cognitive Brain Research, 25(1), 226–239. doi:10.1016/j.cogbrainres.2005.05.014.

    Article  PubMed  Google Scholar 

  • Calautti, C., & Baron, J.-C. (2003). Functional neuroimaging studies of motor recovery after stroke in adults: a review. Stroke; A Journal of Cerebral Circulation, 34(6), 1553–1566.

    Article  Google Scholar 

  • Cattaneo, L., & Rizzolatti, G. (2009). The mirror neuron system. Archives of Neurology, 66(5), 557–560.

    Article  PubMed  Google Scholar 

  • Thiebaut de Schotten, M., Urbanski, M., Duffau, H., Volle, E., Lévy, R., Dubois, B., & Bartolomeo, P. (2005). Direct evidence for a parietal-frontal pathway subserving spatial awareness in humans. Science (New York, N.Y.), 309(5744), 2226–2228. doi:10.1126/science.1116251.

  • De Vivo, P., Ciritella, P., & Del Gaudio, A. (1998). Appropriate arterial pressure management for subarachnoid hemorrhage. Minerva Anestesiologica, 64(5), 211–213.

    CAS  PubMed  Google Scholar 

  • Dricker, J., Butters, N., Berman, G., Samuels, I., & Carey, S. (1978). The recognition and encoding of faces by alcoholic Korsakoff and right hemisphere patients. Neuropsychologia, 16(6), 683–695.

    Article  CAS  PubMed  Google Scholar 

  • Ellmore, T. M., Rohlffs, F., & Khursheed, F. (2013). FMRI of working memory impairment after recovery from subarachnoid hemorrhage. Frontiers in Neurology, 4, 179. doi:10.3389/fneur.2013.00179.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fisher, C. M., Roberson, G. H., & Ojemann, R. G. (1977). Cerebral vasospasm with ruptured saccular aneurysm--the clinical manifestations. Neurosurgery, 1(3), 245–248.

    Article  CAS  PubMed  Google Scholar 

  • Fisher, C. M., Kistler, J. P., & Davis, J. M. (1980). Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery, 6(1), 1–9.

    Article  CAS  PubMed  Google Scholar 

  • Friston, K. J., Holmes, A. P., Price, C. J., Büchel, C., & Worsley, K. J. (1999). Multisubject fMRI studies and conjunction analyses. NeuroImage, 10(4), 385–396. doi:10.1006/nimg.1999.0484.

    Article  CAS  PubMed  Google Scholar 

  • Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain: A Journal of Neurology, 119(Pt 2), 593–609.

    Article  Google Scholar 

  • Gallese, V., Fogassi, L., Fadiga, L., & Rizzolatti, G. (2002). Action representation and the inferior parietal lobule. In W. B. H. Prinz (Ed.), Attention & Performance XIX Common Mechanisms in Perception and Action (pp. 247–266). Oxford: Oxford Univ.

    Google Scholar 

  • Heilman, K. M., Rothi, L. J., & Valenstein, E. (1982). Two forms of ideomotor apraxia. Neurology, 32(4), 342–346.

    Article  CAS  PubMed  Google Scholar 

  • Hooper, H. (1983). Hooper Visual Organization Test (VOT). Los Angeles: Western Psychological Services.

    Google Scholar 

  • Iacoboni, M., & Mazziotta, J. C. (2007). Mirror neuron system: basic findings and clinical applications. Annals of Neurology, 62(3), 213–218. doi:10.1002/ana.21198.

    Article  PubMed  Google Scholar 

  • Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J. C., & Rizzolatti, G. (2005). Grasping the intentions of others with one’s own mirror neuron system. PLoS Biology, 3(3), e79. doi:10.1371/journal.pbio.0030079.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jabbarli, R., Reinhard, M., Niesen, W.-D., Roelz, R., Shah, M., Kaier, K., et al. (2015). Predictors and impact of early cerebral infarction after aneurysmal subarachnoid hemorrhage. European Journal of Neurology, 22(6), 941–947. doi:10.1111/ene.12686.

    Article  CAS  PubMed  Google Scholar 

  • Junqué, C., & Barroso, J. (2009). Manual de neuropsicología. Madrid: Editorial Síntesis.

    Google Scholar 

  • Kistler, J. P., Crowell, R. M., Davis, K. R., Heros, R., Ojemann, R. G., Zervas, T., & Fisher, C. M. (1983). The relation of cerebral vasospasm to the extent and location of subarachnoid blood visualized by CT scan: a prospective study. Neurology, 33(4), 424–436.

    Article  CAS  PubMed  Google Scholar 

  • Mort, D. J., Malhotra, P., Mannan, S. K., Rorden, C., Pambakian, A., Kennard, C., & Husain, M. (2003). The anatomy of visual neglect. Brain: A Journal of Neurology, 126(Pt 9), 1986–1997. doi:10.1093/brain/awg200.

    Article  Google Scholar 

  • Nichols, T., Brett, M., Andersson, J., Wager, T., & Poline, J.-B. (2005). Valid conjunction inference with the minimum statistic. NeuroImage, 25(3), 653–660.

    Article  PubMed  Google Scholar 

  • Nieuwkamp, D. J., Setz, L. E., Algra, A., Linn, F. H. H., de Rooij, N. K., & Rinkel, G. J. E. (2009). Changes in case fatality of aneurysmal subarachnoid haemorrhage over time, according to age, sex, and region: a meta-analysis. The Lancet. Neurology, 8(7), 635–642. doi:10.1016/S1474–4422(09)70126–7.

    Article  PubMed  Google Scholar 

  • Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.

    Article  CAS  PubMed  Google Scholar 

  • Plata Bello, J., Modroño, C., Marcano, F., & González-Mora, J. L. (2014a). The mirror neuron system and motor dexterity: What happens? Neuroscience, 275, 285–295.

    Article  CAS  PubMed  Google Scholar 

  • Plata Bello, J., Modroño, C., Marcano, F., & González-Mora, J. L. (2014b). The effect of motor familiarity during simple finger opposition tasks. Brain Imaging and Behavior. doi:10.1007/s11682–014-9340-x.

    Google Scholar 

  • Press, C., Bird, G., Walsh, E., & Heyes, C. (2008). Automatic imitation of intransitive actions. Brain and Cognition, 67(1), 44–50. doi:10.1016/j.bandc.2007.11.001.

    Article  PubMed  Google Scholar 

  • Rizzolatti, G. (2005). The mirror neuron system and its function in humans. Anatomy and Embryology, 210(5–6), 419–421. doi:10.1007/s00429–005-0039-z.

    Article  PubMed  Google Scholar 

  • Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169–192. doi:10.1146/annurev.neuro.27.070203.144230.

    Article  CAS  PubMed  Google Scholar 

  • Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., & Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Experimental brain research. Experimentelle Hirnforschung. Expérimentation Cérébrale, 71(3), 491–507.

    Article  CAS  PubMed  Google Scholar 

  • Rypma, B., Berger, J. S., Prabhakaran, V., Bly, B. M., Kimberg, D. Y., Biswal, B. B., & D’Esposito, M. (2006). Neural correlates of cognitive efficiency. NeuroImage, 33(3), 969–979. doi:10.1016/j.neuroimage.2006.05.065.

    Article  PubMed  Google Scholar 

  • Sheldon, S., Macdonald, R. L., Cusimano, M., Spears, J., & Schweizer, T. A. (2013). Long-term consequences of subarachnoid hemorrhage: examining working memory. Journal of the Neurological Sciences, 332(1–2), 145–147. doi:10.1016/j.jns.2013.06.021.

    Article  PubMed  Google Scholar 

  • Springer, M. V., Schmidt, J. M., Wartenberg, K. E., Frontera, J. A., Badjatia, N., & Mayer, S. A. (2009). Predictors of global cognitive impairment 1 year after subarachnoid hemorrhage. Neurosurgery, 65(6), 1043–1050 discussion 1050–1. doi:10.1227/01.NEU.0000359317.15269.20.

    Article  PubMed  Google Scholar 

  • Stienen, M. N., Smoll, N. R., Weisshaupt, R., Fandino, J., Hildebrandt, G., Studerus-Germann, A., & Schatlo, B. (2014). Delayed cerebral ischemia predicts neurocognitive impairment following aneurysmal subarachnoid hemorrhage. World Neurosurgery, 82(5), e599–e605. doi:10.1016/j.wneu.2014.05.011.

    Article  PubMed  Google Scholar 

  • Teunissen, L. L., Rinkel, G. J., Algra, A., & van Gijn, J. (1996). Risk factors for subarachnoid hemorrhage: a systematic review. Stroke; A Journal of Cerebral Circulation, 27(3), 544–549.

    Article  CAS  Google Scholar 

  • Vallar, G. (2001). Extrapersonal visual unilateral spatial neglect and its neuroanatomy. NeuroImage, 14(1 Pt 2), S52–S58. doi:10.1006/nimg.2001.0822.

    Article  CAS  PubMed  Google Scholar 

  • Wong, G. K. C., Lam, S. W., Ngai, K., Wong, A., Siu, D., Poon, W. S., & Mok, V. (2013). Cognitive domain deficits in patients with aneurysmal subarachnoid haemorrhage at 1 year. Journal of Neurology, Neurosurgery, and Psychiatry, 84(9), 1054–1058. doi:10.1136/jnnp-2012-304517.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julio Plata-Bello.

Ethics declarations

Disclosure

All authors declare no conflict of interest.

Ethical approval

The study was approved by the University of La Laguna Ethics Committee, according to the Declaration of Helsinki.

Informed consent

Written informed consent was explained and signed by the patients and the control subjects.

Electronic supplementary material

ESM 1

(DOC 885 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Plata-Bello, J., Modroño, C., Acosta-López, S. et al. Subarachnoid hemorrhage and visuospatial and visuoperceptive impairment: disruption of the mirror neuron system. Brain Imaging and Behavior 11, 1538–1547 (2017). https://doi.org/10.1007/s11682-016-9609-3

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11682-016-9609-3

Keywords

Navigation