Skip to main content
Log in

Unilateral ablation of the frontal eye field of the rat affects the beating field of ocular nystagmus

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Spontaneous saccadic orientation and compensatory eye movements in response to optokinetic and vestibular velocity steps were studied in head-restrained, pigmented rats before and 1–2 weeks after unilateral ablation of the frontal eye field (FEF). One group of rats (n=5) received a deep lesion and another group of rats (n=4) received a superficial lesion of the left FEF. Postoperative response parameters such as the duration of slow buildup of eye velocity, the steady state velocity gain, the duration of optokinetic afternystagmus and of per- and postrotatory vestibular nystagmus were similar in the two groups of rats and did not differ from preoperative values measured in the same individuals. Superimposed upon these velocity components of nystagmus was a transient orienting response that expressed itself by a shift of the beating field of nystagmus in quick phase direction (gaze shift). The amplitudes of this gaze shift in quick phase direction were asymmetric in rats with a deep FEF lesion. Gaze shift amplitudes toward the side of the lesion were significantly enhanced and gaze shift amplitudes toward the intact side were significantly reduced. Similar asymmetries were observed in the distribution of spontaneous orienting movements of these rats in the light. Spontaneous saccadic eye movements of the same animals in darkness, however, were symmetric in amplitude to either side. These deficits suggest a partial sensory hemineglect after a deep unilateral lesion of the FEF and an involvement of this structure in the selective attention for targets in visual space. Thus the FEF orients the gaze at rest by means of saccades toward points of interest and during simulated circular locomotion by means of a shift of the beating field of nystagmus toward the visual sector that will be approached next.

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.

Similar content being viewed by others

References

  • Bruce CJ, Goldberg ME (1985) Primate frontal eye fields. I. Single neurons discharging before saccades. J Neurophysiol 53:603–635

    Google Scholar 

  • Chelazzi L, Rossi F, Tempia F, Ghirardi M, Strata P (1989) Saccadic eye movements and gaze holding in the head-restrained pigmented rat. Eur J Neurosci 1:639–646

    Google Scholar 

  • Chun K-S, Robinson DA (1978) A model of quick phase generation in the vestibuloocular reflex. Biol Cybern 28:209–221

    CAS  PubMed  Google Scholar 

  • Collewijn H (1989) The vestibulo-ocular reflex: an outdated concept? Prog Brain Res 80:197–209

    Google Scholar 

  • Corwin JV, Kanter S, Watson RT, Heilman KM, Valenstein E, Hashimoto A (1986) Apomorphine has a therapeutic effect on neglect produced by unilateral dorsomedial prefrontal cortex lesions in rats. Exp Neurol 94:683–698

    Google Scholar 

  • Cowey A, Bozek T (1974) Contralateral “neglect” after unilateral dorsomedial prefrontal lesions in rats. Brain Res 72:53–63

    Google Scholar 

  • Crowne DP (1983) The frontal eye field and attention. Psychol Bull 93:232–260

    Google Scholar 

  • Crowne DP, Pathria MN (1982) Some attentional effects of unilateral frontal lesions in the rat. Behav Brain Res 6:25–39

    Google Scholar 

  • Dean P, Redgrave P, Westby GWM (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137–147

    Google Scholar 

  • Donoghue JP, Parham C (1983) Afferent connections of the lateral agranular field of the rat motor cortex. J Comp Neurol 217:390–404

    Google Scholar 

  • Goldberg ME, Segraves MA (1989) The visual and frontal cortices. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. (Reviews of oculomotor research, vol 3) Elsevier, Amsterdam, pp 283–313

    Google Scholar 

  • Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66:23–38

    Google Scholar 

  • Jung R, Mittermaier R (1939) Zur objektiven Registrierung und Analyse verschiedener Nystagmusformen: Vestibulärer, optokinetischer und spontaner Nystagmus in ihren Wechselbeziehungen. Arch Ohren-Nasen-Kehlkopf-Heilkunde 146:410–439

    Google Scholar 

  • Kasper HJ, Hess BJM, Dieringer N (1987) Precise and inexpensive magnetic field search coil system for measuring eye and head movements in small laboratory animals. J Neurosci Methods 19:115–124

    Google Scholar 

  • Keating EG (1991) Frontal eye field lesions impair predictive and visually guided pursuit eye movements. Exp Brain Res 86:311–323

    Google Scholar 

  • Keay K, Westby GWM, Frankland P, Dean P, Redgrave P (1990) Organization of the crossed tecto-reticulo-spinal projection in rat. II. Electrophysiological evidence for separate output channels to the periabducens area and caudal medulla. Neuroscience 37:585–601

    Google Scholar 

  • Latto R, Cowey A (1971) Fixation changes after frontal eye-field lesions in monkeys. Brain Res 30:25–36

    Google Scholar 

  • Leichnetz GR, Goldberg ME (1988) Higher centers concerned with eye movement and visual attention: cerebral cortex and thalamus. In: Büttner-Ennever JA (ed) Neuroanatomy of the oculomotor system. (Reviews of oculomotor research, vol 2) Elsevier, Amsterdam, pp 365–429

    Google Scholar 

  • Leonard CM (1969) The prefrontal cortex of the rat. I. Cortical projections of the mediodorsal nucleus. II. Efferent connections. Brain Res 12:321–343

    Google Scholar 

  • Leonard CM (1972) The connections of the dorsomedial nuclei. Brain Behav Evol 6:524–541

    Google Scholar 

  • Lynch JC (1987) Frontal eye field lesions in monkeys disrupt visual pursuit. Exp Brain Res 68:437–441

    Google Scholar 

  • Meier RK, Dieringer N (1993) The role of compensatory eye and head movements in the rat for image stabilization and gaze orientation. Exp Brain Res 96:54–64

    Google Scholar 

  • Melvill-Jones G (1964) Predominance of anti-compensatory oculomotor response during rapid head rotation. Aerospace Med 35:965–968

    Google Scholar 

  • O-Uchi T, Igarashi M, Kubo T (1981) Effect of frontal-eye-field lesion on eye-head coordination in squirrel monkeys. Ann NY Acad Sci 374:656–673

    Google Scholar 

  • Redgrave P, Dean P, Westby GWM (1990) Organization of the crossed tecto-reticulo-spinal projection in rat. I. Anatomical evidence for separate output channels to the periabducens area and caudal medulla. Neuroscience 37:571–584

    Google Scholar 

  • Reep RL, Corwin JV, Hashimoto A, Watson RT (1984) Afferent connections of medial precentral cortex in the rat. Neurosci Lett 44:247–252

    Google Scholar 

  • Robinson DA, Fuchs AF (1968) Eye movements evoked by stimulation of frontal eye fields. J Neurophysiol 32:637–648

    Google Scholar 

  • Schiller PH, True SD, Conway JL (1980) Deficits in eye movements following frontal eye-field and superior colliculus ablations. J Neurophysiol 44:1175–1189

    CAS  PubMed  Google Scholar 

  • Ungerstedt U, Arbuthnott GW (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24:485–493

    Article  CAS  PubMed  Google Scholar 

  • Van der Steen J, Russell IS, James GO (1986) Effects of unilateral frontal eye-field lesions on eye-head coordination in monkey. J Neurophysiol 55:696–714

    Google Scholar 

  • Vidai PP, Roucoux A, Berthoz A (1982) Horizontal eye position related activity in neck muscles of alert cat. Exp Brain Res 46:448–453

    Google Scholar 

  • Welch K, Stuteville P (1958) Experimental production of unilateral neglect in monkeys. Brain 81:341–347

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bähring, R., Meier, R.K. & Dieringer, N. Unilateral ablation of the frontal eye field of the rat affects the beating field of ocular nystagmus. Exp Brain Res 98, 391–400 (1994). https://doi.org/10.1007/BF00233977

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00233977

Key words

Navigation