Hostname: page-component-8448b6f56d-jr42d Total loading time: 0 Render date: 2024-04-24T22:50:50.146Z Has data issue: false hasContentIssue false

Disconnections in Infantile-Onset Saccade Initiation Delay: A Hypothesis

Published online by Cambridge University Press:  23 September 2016

Michael S. Salman*
Affiliation:
Section of Pediatric Neurology, Children's Hospital, University of Manitoba, Winnipeg, Manitoba
Kristin M. Ikeda
Affiliation:
Faculty of Health Sciences, Michael G. DeGroote School of Medicine, McMaster University, Hamilton, Ontario, Canada
*
Section of Pediatric Neurology, Children's Hospital, AE 308, 820 Sherbrook Street, Winnipeg, Manitoba, R3A 1R9, Canada
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Infantile-onset saccade initiation delay (ISID), commonly known as congenital ocular motor apraxia, is characterized by difficulty in triggering horizontal volitional saccades. It typically presents with head thrusts in infancy and is often associated with developmental delay. Patients with ISID are reported to have abnormalities in various brain regions including the corpus callosum, brainstem, and cerebellum. We propose that ISID is caused by the disruption or disconnection of axons linking analogous brain regions involved in processing saccades across the two sides of the brain or bilateral damage to these regions.

Résumé

Résumé

Le délai dans le déclenchement des saccades qui commence dans l'enfance (DDSE), connu sous le nom d'apraxie oculomotrice congénitale, est caractérisé par une difficulté à déclencher des saccades volontaires horizontales. On l'observe de façon typique lors de mouvements brusques de la tête chez les nourrissons et il est souvent associé à un retard de développement. Des anomalies dans différentes régions du cerveau ont été rapportées chez les patients qui présentent un DDSE, dont le corps calleux, le tronc cérébral et le cervelet. Nous émettons l'hypothèse que le DDSE est dû à une perturbation ou à une déconnexion des axones qui relient des régions analogues du cerveau qui sont impliquées dans le traitement des saccades entre les deux hémisphères ou à un dommage bilatéral dans ces régions.

Type
Medical Hypothesis
Copyright
Copyright © The Canadian Journal of Neurological 2010

References

1. Harris, CM, Shawkat, F, Russell-Eggitt, I, Wilson, J, Taylor, D. Intermittent horizontal saccade failure (‘ocular motor apraxia’) in children. Br J Ophthalmol. 1996;80:151–8.10.1136/bjo.80.2.1518814747Google Scholar
2. Kondo, A, Saito, Y, Floricel, F, Maegaki, Y, Ohno, K. Congenital ocular motor apraxia: clinical and neuroradiological findings, and long-term intellectual prognosis. Brain Dev. 2007;29:431–8.10.1016/j.braindev.2007.01.00217336010Google Scholar
3. Shawkat, FS, Kingsley, D, Kendall, B, Russell-Eggitt, I, Taylor, DSI, Harris, CM. Neuroradiological and eye movement correlates in children with intermittent saccade failure: “ocular motor apraxia”. Neuropediatrics. 1995;26:298305.10.1055/s-2007-9797788719744Google Scholar
4. Zee, DS, Yee, RD, Singer, HS. Congenital ocular motor apraxia. Brain. 1977;100:581–99.10.1093/brain/100.3.581589433Google Scholar
5. Rambold, H, Moser, A, Zurowski, B, Gbadamosi, J, Kómpf, D, Sprenger, A, et al. Saccade initiation in ocular motor apraxia. J Neurol. 2006;253:950–2.10.1007/s00415-006-0123-116619125Google Scholar
6. Jan, JE, Kearney, S, Groenveld, M, Sargent, MA, Poskitt, KJ. Speech, cognition and imaging studies in congenital ocular motor apraxia. Dev Med Child Neurol. 1998;40:95–9.9489497Google Scholar
7. Harris, CM, Hodgkins, PR, Kriss, A, Chong, WK, Thompson, DA, Mezey, LE, et al. Familial congenital saccade initiation failure and isolated cerebellar vermis hypoplasia. Dev Med Child Neurol. 1998;40:775–9.9881808Google Scholar
8. Sharpe, JA, Johnston, JL. Ocular motor paresis versus apraxia. Ann Neurol.1989;25(2):209–10.2919873Google Scholar
9. Fielder, AR, Gresty, MA, Dodd, KL, Mellor, DH, Levene, MI. Congenital ocular motor apraxia. Trans Ophthalmol Soc UK. 1986;105:589–98.2432703Google Scholar
10. Kim, JS, Park, SH, Lee, KW. Spasmus nutans and congenital ocular motor apraxia with cerebellar vermian hypoplasia. Arch Neurol. 2003;60:1621–4.10.1001/archneur.60.11.162114623737Google Scholar
11. Orrison, WW, Robertson, WC. Congenital ocular motor apraxia: a possible disconnection syndrome. Arch Neurol. 1979;36:2931.10.1001/archneur.1979.00500370059013420600Google Scholar
12. Pierrot-Deseilligny, C, Gautier, JC, Loron, P. Acquired ocular motor apraxia due to bilateral frontoparietal infarcts. Ann Neurol. 1988; 23:199202.10.1002/ana.4102302163270327Google Scholar
13. Bodis-Wollner, I, Bucher, SF, Seelos, KC. Cortical activation patterns during voluntary blinks and voluntary saccades. Neurology. 1999;53(8):1800–5.10.1212/WNL.53.8.180010563631Google Scholar
14. Hayakawa, Y, Nakajima, T, Takagi, M, Fukuhara, N, Abe, H. Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study. Ophthalmologica. 2002;216:399405.10.1159/00006755112566881Google Scholar
15. Ritter, P, Villringer, A. Inhibition and functional magnetic resonance imaging. Int Congr Ser. 2002;1235:213–22.10.1016/S0531-5131(02)00189-9Google Scholar
16. Berman, RA, Heiser, LM, Saunders, RC, Colby, CL. Dynamic circuitry for updating spatial representations. I. Behavioral evidence for interhemispheric transfer in the split-brain Macaque. J Neurophysiol. 2005;94:3228–48.10.1152/jn.00028.200515888534Google Scholar
17. Heiser, LM, Berman, RA, Saunders, RC, Colby, CL. Dynamic circuitry for updating spatial representations. II. Physiological evidence for interhemispheric transfer in area LIP of the split-brain macaque. J Neurophysiol. 2005;94(5):3249–58.10.1152/jn.00029.200515888533Google Scholar
18. Paul, LK, Brown, WS, Adolphs, R, Tyszka, JM, Richards, LJ, Mukheree, P, et al. Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nature Rev. 2007;8:287–99.10.1038/nrn2107Google Scholar
19. Orssaud, C, Ingster-Moati, I, Roche, O, Quoc, EB, Dufier, JL. Familial congenital oculomotor apraxia: clinical and electro-oculographic features. Eur J Paediatr Neurol. 2009;13:370–2.10.1016/j.ejpn.2008.06.00618703363Google Scholar
20. Park, HJ, Kim, JJ, Seok, JH, Chun, J, Kim, DI, Lee, JD. Corpus callosal connection mapping using cortical gray matter parcellation and DT-MRI. Hum Brain Mapp. 2008;29:503–16.10.1002/hbm.2031417133394Google Scholar
21. Holtzman, JD. Interactions between cortical and subcortical visual areas: evidence from human commissurotomy patients. Vision Res. 1984;24(8):801–13.10.1016/0042-6989(84)90151-26474837Google Scholar
22. Hughes, HC, Reuter-Lorenz, PA, Fendrich, R, Gazzaniga, MS. Bidirectional control of saccadic eye movements by the disconnected cerebral hemispheres. Exp Brain Res. 1992;91(2):335–9.1459235Google Scholar
23. Colby, CL, Berman, RA, Heiser, LM, Saunders, RC. Corollary discharge and spatial updating: when the brain is split, is space still unified? Prog Brain Res. 2005;149:187205.16226585Google Scholar
24. Lynch, JC. Saccade initiation and latency deficits after combined lesions of the frontal and posterior eye fields in monkeys. J Neurophysiol. 1992;68(5):1913–6.1479455Google Scholar
25. Schiller, PH, True, SD, Conway, JL. Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol. 1980;44(6):1175–89.6778974Google Scholar
26. Sharpe, JA, Lo, AW, Rabinovitch, HE. Control of the saccadic and smooth pursuit systems after cerebral hemidecortication. Brain. 1979;102(2):387403.10.1093/brain/102.2.387455046Google Scholar
27. Schlag, J, Dassonville, P, Schlag-Rey, M. Interaction of the two frontal eye fields before saccade onset. J Neurophysiol. 1998;79(1):6472.9425177Google Scholar
28. Maria, BL, Hoang, KBN, Tusa, RJ, Mancuso, AA, Hamed, LM, Quisling, RG, et al. “Joubert syndrome” revisited: key ocular motor signs with magnetic resonance imaging correlation. J Child Neurol. 1997;12:423–30.10.1177/0883073897012007039373798Google Scholar
29. Spampinato, MV, Kraas, J, Maria, BL, Walton, ZJ, Rumboldt, Z. Absence of decussation of the superior cerebellar peduncles in patients with Joubert syndrome. Am J Med Gen Part A. 2008;146A:1389–94.Google Scholar
30. Yachnis, AT, Rorke, LB. Neuropathology of Joubert syndrome. J Child Neurol. 1999;14:655–9.10.1177/08830738990140100610511338Google Scholar
31. Sztriha, L, Al-Gazali, LI, Aithala, GR, Nork, M. Joubert’s syndrome: new cases and review of clinicopathologic correlation. Pediatr Neurol. 1999;20:274–81.10.1016/S0887-8994(98)00154-410328276Google Scholar
32. Furland, RJ, Eyaid, W, Collura, RV, Tully, LD, Hill, RS, Al-Nouri, D, et al. Abnormal cerebellar development and axonal decussation due to mutations in AHI1 in Joubert syndrome. Nat Genet. 2004; 36(9):1008–13.10.1038/ng141915322546Google Scholar
33. Selhorst, JB, Stark, L, Ochs, AL, Hoyt, WF. Disorders in cerebellar ocular motor control. I. Saccadic overshoot dysmetria. An oculographic, control system and clinico-anatomical analysis. Brain. 1976;99(3):497508.10.1093/brain/99.3.4971000283Google Scholar
34. Keating, EG, Gooley, SG. Saccadic disorders caused by cooling the superior colliculus or the frontal eye field, or from combined lesions of both structures. Brain Res. 1988;438(1–2):247–55.10.1016/0006-8993(88)91343-13345431Google Scholar
35. Krebs, RM, Woldorff, MG, Tempelmann, C, Bodammer, N, Noesselt, T, Boehler, CN, et al. High-field FMRI reveals brain activation patterns underlying saccade execution in the human superior colliculus. PLoS One. 2010 Jan 13;5(1):e8691.AMBIGUOUS (6752 citations)Google Scholar
36. Takahashi, M, Sugiuchi, Y, Shinoda, Y. Commissural mirror symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements. J Neurophysiol 2007;98:2664–82.10.1152/jn.00696.200717728384Google Scholar
37. Brown, H, Willshaw, HE. A case of disturbed vertical gaze. Eur J Paediatr Neurol. 2003;7:173–5.10.1016/S1090-3798(03)00055-212865057Google Scholar
38. Salman, MS, Sharpe, JA, Eizenman, M, Lillakas, L, Westall, C, To, T, et al. Saccades in children. Vision Res. 2006;46(8–9):1432–9.10.1016/j.visres.2005.06.01116051306Google Scholar
39. Le Ber, I, Moreira, M, Rivaud-Péchoux, S, Chamayou, C, Ochsner, F, Kuntzer, T, et al. Cerebellar ataxia with oculomotor apraxia type 1: clinical and genetic studies. Brain. 2003;126:2761–72.10.1093/brain/awg28314506070Google Scholar
40. Le Ber, I, Bouslam, N, Rivaud-Péchoux, S, Guimarâes, J, Benomar, A, Chamayou, C, et al. Frequency and phenotypic spectrum of ataxia with oculomotor apraxia 2: a clinical and genetic study in 18 patients. Brain. 2004;127:759–67.10.1093/brain/awh08014736755Google Scholar