Skip to main content
Log in

Gaze holding after anterior-inferior temporal lobectomy

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Eye position-sensitive neurons are found in parietooccipital and anterior-inferior temporal cortex. Putative role of these neurons is to facilitate transformation of reference frame from the retina-fixed to world-fixed coordinates and assure precise action. We assessed the nature of ocular motor disorder in a subject who had selective resection of the right anterior-inferior temporal cortex for the treatment of intractable epilepsy from cortical dysplasia. The gaze was stable when the subject was viewing straight-ahead, but centrally directed drifts in the eye position were seen during eccentric horizontal gaze holding. Eye-in-orbit position determined drift velocity and its direction. Conjugate and sinusoidal vertical oscillations were also present. Horizontal drifts and vertical oscillations became prominent and disconjugate in the absence of visual cue. The gaze-holding deficit was consistent with impairment in neural integration, but in the absence of cerebellar and visual deficits. We speculate that brainstem neural integrator might receive cortical feedback regarding world-fixed coordinates. Visual system might calibrate this process. Hence the lesion of the anterior-inferior temporal lobe leads to impairment in the function of neural integrator. Vision might be used to calibrate such feedback, hence the lack of visual cue further impairs the function of the neural integrator leading to worsening of gaze-holding deficits.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908

    CAS  PubMed  Google Scholar 

  2. Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L (1990) Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque. J Neurosci 10:1176–1196

    CAS  PubMed  Google Scholar 

  3. Galletti C, Battaglini PP, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501

    Article  CAS  PubMed  Google Scholar 

  4. Bremmer F, Distler C, Hoffmann KP (1997) Eye position effects in monkey cortex. II. Pursuit- and fixation-related activity in posterior parietal areas LIP and 7A. J Neurophysiol 77:962–977

    CAS  PubMed  Google Scholar 

  5. Bremmer F, Graf W, Ben Hamed S, Duhamel JR (1999) Eye position encoding in the macaque ventral intraparietal area (VIP). NeuroReport 10:873–878

    Article  CAS  PubMed  Google Scholar 

  6. Williams AL, Smith AT (2010) Representation of eye position in the human parietal cortex. J Neurophysiol 104:2169–2177

    Article  PubMed  Google Scholar 

  7. Cogan DG (1965) Ophthalmic manifestations of bilateral non-occipital cerebral lesions. Br J Ophthalmol 49:281–297

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  8. Hecaen H, de Ajuriaguerra J (1954) Balint’s syndrome (psychic paralysis of visual fixation) and its minor forms. Brain 77:373–400

    Article  CAS  PubMed  Google Scholar 

  9. Lehky SR, Tanaka K (2007) Enhancement of object representations in primate perirhinal cortex during a visual working-memory task. J Neurophysiol 97:1298–1310

    Article  PubMed  Google Scholar 

  10. Tanaka K (1996) Inferotemporal cortex and object vision. Annu Rev Neurosci 19:109–139

    Article  CAS  PubMed  Google Scholar 

  11. Desimone R, Albright TD, Gross CG, Bruce C (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4:2051–2062

    CAS  PubMed  Google Scholar 

  12. Ringo JL, Sobotka S, Diltz MD, Bunce CM (1994) Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. J Neurophysiol 71:1285–1288

    CAS  PubMed  Google Scholar 

  13. Sobotka S, Ringo JL (1997) Saccadic eye movements, even in darkness, generate event-related potentials recorded in medial sputum and medial temporal cortex. Brain Res 756:168–173

    Article  CAS  PubMed  Google Scholar 

  14. Nowicka A, Ringo JL (2000) Eye position-sensitive units in hippocampal formation and in inferotemporal cortex of the macaque monkey. Eur J Neurosci 12:751–759

    Article  CAS  PubMed  Google Scholar 

  15. Lehky SR, Peng X, McAdams CJ, Sereno AB (2008) Spatial modulation of primate inferotemporal responses by eye position. PLoS One 3:e3492

    Article  PubMed Central  PubMed  Google Scholar 

  16. Engbert R (2006) Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception. Prog Brain Res 154:177–192

    Article  PubMed  Google Scholar 

  17. Engbert R, Mergenthaler K (2006) Microsaccades are triggered by low retinal image slip. Proc Natl Acad Sci USA 103:7192–7197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878–899

    CAS  PubMed  Google Scholar 

  19. Zee DS, Yee RD, Cogan DG, Robinson DA, Engel WK (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234

    Article  CAS  PubMed  Google Scholar 

  20. Chen-Harris H, Joiner WM, Ethier V, Zee DS, Shadmehr R (2008) Adaptive control of saccades via internal feedback. J Neurosci 28:2804–2813

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Ethier V, Zee DS, Shadmehr R (2008) Changes in control of saccades during gain adaptation. J Neurosci 28:13929–13937

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Ethier V, Zee DS, Shadmehr R (2008) Spontaneous recovery of motor memory during saccade adaptation. J Neurophysiol 99:2577–2583

    Article  PubMed Central  PubMed  Google Scholar 

  23. Tian J, Ethier V, Shadmehr R, Fujita M, Zee DS (2009) Some perspectives on saccade adaptation. Ann NY Acad Sci 1164:166–172

    Article  PubMed  Google Scholar 

  24. Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R (2009) Cerebellar contributions to adaptive control of saccades in humans. J Neurosci 29:12930–12939

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, Thier P (2008) Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur J Neurosci 27:132–144

    Article  PubMed  Google Scholar 

  26. Cannon SC, Robinson DA, Shamma S (1983) A proposed neural network for the integrator of the oculomotor system. Biol Cybern 49:127–136

    Article  CAS  PubMed  Google Scholar 

  27. Robinson DA (1974) The effect of cerebellectomy on the cat’s vestibulo-ocular integrator. Brain Res 71:195–207

    Article  CAS  PubMed  Google Scholar 

  28. Skavenski AA, Robinson DA (1973) Role of abducens neurons in vestibuloocular reflex. J Neurophysiol 36:724–738

    CAS  PubMed  Google Scholar 

  29. Leigh RJ, Zee DS (1980) Eye movements of the blind. Invest Ophthalmol Vis Sci 19:328–331

    CAS  PubMed  Google Scholar 

  30. Balslev D, Himmelbach M, Karnath HO, Borchers S, Odoj B (2012) Eye proprioception used for visual localization only if in conflict with the oculomotor plan. J Neurosci 32:8569–8573

    Article  CAS  PubMed  Google Scholar 

  31. Lewis RF, Zee DS, Hayman MR, Tamargo RJ (2001) Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles. Exp Brain Res 141:349–358

    Article  CAS  PubMed  Google Scholar 

  32. Lambert FM, Combes D, Simmers J, Straka H (2012) Gaze stabilization by efference copy signaling without sensory feedback during vertebrate locomotion. Curr Biol 22:1649–1658

    Article  CAS  PubMed  Google Scholar 

  33. Lambert FM, Malinvaud D, Gratacap M, Straka H, Vidal PP (2013) Restricted neural plasticity in vestibulospinal pathways after unilateral labyrinthectomy as the origin for scoliotic deformations. J Neurosci 33:6845–6856

    Article  CAS  PubMed  Google Scholar 

  34. Horne PD (1973) Long term anticonvulsant therapy and cerebellar atrophy. J Ir Med Assoc 66:147–152

    CAS  PubMed  Google Scholar 

  35. Hagemann G, Lemieux L, Free SL, Krakow K, Everitt AD, Kendall BE et al (2002) Cerebellar volumes in newly diagnosed and chronic epilepsy. J Neurol 249:1651–1658

    Article  CAS  PubMed  Google Scholar 

  36. McLain LW Jr, Martin JT, Allen JH (1980) Cerebellar degeneration due to chronic phenytoin therapy. Ann Neurol 7:18–23

    Article  PubMed  Google Scholar 

  37. Haberland C (1962) Cerebellar degeneration with clinical manifestation in chronic epileptic patients. Psychiatr Neurol (Basel) 143:29–44

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by financial support from Knights Templar Eye Foundation (FG) and Fight-for-sight (FG) research Grants. We are grateful to R. John Leigh, MD for providing technical equipments. Dr. Shaikh was supported by Dystonia Medical Research Foundation grant. Dr. Leigh was supported by NIH Grant EY06717.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aasef G. Shaikh.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shaikh, A.G., Ghasia, F.F. Gaze holding after anterior-inferior temporal lobectomy. Neurol Sci 35, 1749–1756 (2014). https://doi.org/10.1007/s10072-014-1825-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-014-1825-2

Keywords

Navigation