Advertisement
Review article| Volume 23, SUPPLEMENT 1, S24-S27, December 2001

Download started.

Ok

Facilitation of saccade initiation by brainstem cholinergic system

      Abstract

      It is well known that the intermediate layer (SGI) of the mammalian superior colliculus (SC) receives cholinergic inputs originating from the pedunculopontine tegmental nucleus (PPTN). The action of the cholinergic input on the SGI neurons was investigated using whole-cell patch-clamp recording technique in slice preparations obtained from rats. Application of acetylcholine (ACh) induced fast inward currents mediated by nicotinic ACh receptors in the SGI neurons. Depolarization induced by nicotine enhanced the N-methyl-d-aspartate receptor-mediated excitatory postsynaptic potential component and lowered the threshold of bursting response in the SGI neurons to stimulation of the superficial layer. Thus, the cholinergic input to the SGI facilitates the signal transmission through the direct visuomotor pathway in the SC. The behavioral correlate of this observation was explored by microinjection of nicotine into the SC of awake monkeys during visually guided saccade task; injection of nicotine increased frequency of express saccades, the saccades with extremely short reaction times (<120 ms). Analysis of single unit activity of the PPTN neurons revealed that a population of the PPTN neurons increased firing preceding saccades in a particular direction and also during the GAP period between the offset of fixation point and onset of the saccade target. Thus, PPTN neurons may be involved in execution and preparation of saccades. All these results explain the mechanisms of how the brainstem cholinergic system facilitates initiation of saccades presumably depending on attention or vigilance level of the animal.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Brain and Development
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Garcia-Rill E.
        The pedunculopontine nucleus.
        Prog Neurobiol. 1991; 36: 363-389
        • Steriade M.
        Arousal: revisiting the reticular activating system.
        Science. 1996; 272: 225-226
        • Kobayashi Y.
        • Inoue Y.
        • Yamamoto M.
        • Aizawa H.
        • Isa T.
        Coding of multimodal signals in the pedunculopontine nucleus neurons related to performance of visually guided saccade task.
        Soc Neurosci Abstr. 2000; 26: 363.15
        • Uhlrich D.J.
        • Tamamaki N.
        • Murphy P.C.
        • Sherman S.M.
        Effects of brainstem parabrachial activation on receptive field properties of cells in the cat's lateral geniculate nucleus.
        J. Neurophysiol. 1995; 73: 2428-2447
        • Brown J.
        • Bullock D.
        • Grossberg S.
        How the basal ganglia use parallel excitatory and inhibitory pathways to selectively respond to unexpected rewarding cues.
        J Neurosci. 1999; 19: 10502-10511
        • Matsumura M.
        • Watanabe K.
        • Ohye C.
        Single unit activity in the primate nucleus tegmenti pedunculopontinus related to voluntary arm movement.
        Neurosci Res. 1997; 28: 155-165
        • Beninato M.
        • Spencer R.F.
        A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry.
        J Comp Neurol. 1986; 253: 525-538
        • Graybiel A.M.
        A stereometric pattern of distribution of acetylcholinesterase in the deep layers of the superior colliculus.
        Nature. 1978; 272: 539-541
        • Hall W.C.
        • Fitzpatrick D.
        • Klatt L.L.
        • Raczkowski D.
        Cholinergic innervation of the superior colliculus in the cat.
        J Comp Neurol. 1989; 287: 495-514
        • Henderson Z.
        • Sherriff F.E.
        Distribution of choline acetyltransferase immunoreactive axons and terminals in the rat and ferret brainstem.
        J Comp Neurol. 1991; 314: 147-163
        • Jeon C.J.
        • Spencer R.F.
        • Mize R.R.
        Organization and synaptic connections of cholinergic fibers in the cat superior colliculus.
        J Comp Neurol. 1993; 333: 360-374
        • Ma T.P.
        • Graybiel A.M.
        • Wurtz R.H.
        Location of saccade-related neurons in the macaque superior colliculus.
        Exp Brain Res. 1991; 85: 21-35
        • Schnurr B.
        • Spatz W.B.
        • Illing R.B.
        Similarities and differences between cholinergic systems in the superior colliculus of guinea pig and rat.
        Exp Brain Res. 1992; 90: 291-296
        • Sparks D.L.
        • Hartwich-Young R.
        The deep layers of the superior colliculus.
        Rev Oculomotor Res. 1998; 3: 231-235
        • Kustov A.A.
        • Robinson D.L.
        Shared neural control of attention shifts and eye movements.
        Nature. 1996; 384: 74-77
        • Glimcher P.W.
        • Sparks D.L.
        Movement selection in advance of action in the superior colliculus.
        Nature. 1992; 355: 542-545
        • Dorris M.C.
        • Munoz D.P.
        Saccadic probability influences motor preparation signals and time to saccade initiation.
        J Neurosci. 1998; 18: 7015-7026
        • Isa T.
        • Endo T.
        • Saito Y.
        Nicotinic facilitation of signal transmission in the local circuit of the rat superior colliculus.
        Soc Neurosci Abstr. 1998; 24: 60.13
        • Isa T.
        • Endo T.
        • Saito Y.
        The visuomotor pathway in the local circuit of the rat superior colliculus.
        J Neurosci. 1998; 18: 8496-8504
        • Aizawa H.
        • Kobayashi Y.
        • Yamamoto M.
        • Isa T.
        Injection of nicotine into superior colliculus facilitates occurrence of express saccades in monkeys.
        J Neurophysiol. 1999; 82: 1642-1646
        • Dorris M.C.
        • Munoz D.P.
        A neural correlate for the gap effect on saccadic reaction times in monkey.
        J Neurophysiol. 1995; 73: 2558-2562
        • Kobayashi Y.
        • Aizawa H.
        • Yamamoto M.
        • Isa T.
        Control of saccadic reaction time by pedunculopontine tegmental nucleus neurons in monkeys.
        Soc Neurosci Abstr. 1999; 25: 661.7
        • Billet S.
        • Cant N.B.
        • Hall W.C.
        Cholinergic projections to the visual thalamus and superior colliculus.
        Brain Res. 1999; 847: 121-123
        • Sherman S.M.
        Dual response modes in lateral geniculate neurons: mechanisms and functions.
        Vis Neurosci. 1996; 13: 205-213