Saccadic palsy following cardiac surgery: Possible role of perineuronal nets

Scott Daniel Eggers, Anja K E Horn, Sigrun Roeber, Wolfgang Härtig, Govind Nair, Daniel S. Reich, R. John Leigh

Research output: Contribution to journalArticle

7 Citations (Scopus)

Abstract

Objective: Perineuronal nets (PN) form a specialized extracellular matrix around certain highly active neurons within the central nervous system and may help to stabilize synaptic contacts, promote local ion homeostasis, or play a protective role. Within the ocular motor system, excitatory burst neurons and omnipause neurons are highly active cells that generate rapid eye movements - saccades; both groups of neurons contain the calcium-binding protein parvalbumin and are ensheathed by PN. Experimental lesions of excitatory burst neurons and omnipause neurons cause slowing or complete loss of saccades. Selective palsy of saccades in humans is reported following cardiac surgery, but such cases have shown normal brainstem neuroimaging, with only one clinicopathological study that demonstrated paramedian pontine infarction. Our objective was to test the hypothesis that lesions of PN surrounding these brainstem saccade-related neurons may cause saccadic palsy. Methods: Together with four controls we studied the brain of a patient who had developed a permanent selective saccadic palsy following cardiac surgery and died several years later. Sections of formalin-fixed paraffin-embedded brainstem blocks were applied to double-immunoperoxidase staining of parvalbumin and three different components of PN. Triple immunofluorescence labeling for all PN components served as internal controls. Combined immunostaining of parvalbumin and synaptophysin revealed the presence of synapses. Results: Excitatory burst neurons and omnipause neurons were preserved and still received synaptic input, but their surrounding PN showed severe loss or fragmentation. Interpretation: Our findings support current models and experimental studies of the brainstem saccadegenerating neurons and indicate that damage to PN may permanently impair the function of these neurons that the PN ensheathe. How a postulated hypoxic mechanism could selectively damage the PN remains unclear. We propose that the well-studied saccadic eye movement system provides an accessible model to evaluate the role of PN in health and disease.

Original languageEnglish (US)
Article numbere0132075
JournalPLoS One
Volume10
Issue number7
DOIs
StatePublished - Jul 2 2015

Fingerprint

paralysis
Paralysis
Surgery
Thoracic Surgery
Neurons
surgery
neurons
Eye movements
Saccades
brain stem
Parvalbumins
Brain Stem
eyes
lesions (animal)
Neuroimaging
calcium-binding proteins
Synaptophysin
Calcium-Binding Proteins
infarction
REM Sleep

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Eggers, S. D., Horn, A. K. E., Roeber, S., Härtig, W., Nair, G., Reich, D. S., & Leigh, R. J. (2015). Saccadic palsy following cardiac surgery: Possible role of perineuronal nets. PLoS One, 10(7), [e0132075]. https://doi.org/10.1371/journal.pone.0132075

Saccadic palsy following cardiac surgery : Possible role of perineuronal nets. / Eggers, Scott Daniel; Horn, Anja K E; Roeber, Sigrun; Härtig, Wolfgang; Nair, Govind; Reich, Daniel S.; Leigh, R. John.

In: PLoS One, Vol. 10, No. 7, e0132075, 02.07.2015.

Research output: Contribution to journalArticle

Eggers, SD, Horn, AKE, Roeber, S, Härtig, W, Nair, G, Reich, DS & Leigh, RJ 2015, 'Saccadic palsy following cardiac surgery: Possible role of perineuronal nets', PLoS One, vol. 10, no. 7, e0132075. https://doi.org/10.1371/journal.pone.0132075
Eggers, Scott Daniel ; Horn, Anja K E ; Roeber, Sigrun ; Härtig, Wolfgang ; Nair, Govind ; Reich, Daniel S. ; Leigh, R. John. / Saccadic palsy following cardiac surgery : Possible role of perineuronal nets. In: PLoS One. 2015 ; Vol. 10, No. 7.
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