Skip to main content
Log in

Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The interstitial nucleus of Cajal (iC) is known to be the neural integrator for vertical and torsional eye movements. Burst-tonic neurons are thought to be the neural substrate for this function. Until now, the iC has not been specifically considered to play a part in saccade generation. The aim of this study was to characterize saccade-related burst neurons in the iC during torsional and vertical eye movements. Saccade-related burst neurons were recorded in the iC of macaque monkeys during fast phases of torsional and vertical vestibular nystagmus, spontaneous and visually guided eye movements, and in light and darkness. Burst neurons in the iC (n=85) were found intermingled between burst-tonic and tonic neurons. They were not spontaneously active, showed no eye position sensitivity, and responded during saccades and quick phases of nystagmus with a burst of activity whose duration was closely correlated with saccade amplitude and hence saccade duration (correlation coefficients up to 0.9). Latency in the on-direction was, on average, 10.4 ms (range 5–23 ms); it decreased with different saccade directions and became negative in the off-direction. In a horizontal-vertical coordinate system, on-direction of the majority of neurons was either upward (n=52) or downward (n=33). There was no horizontal on-direction. Burst neurons of different vertical on-directions were found intermingled throughout the iC. In the vertical-torsional plane, on-direction always showed an ipsiversive torsional component, i.e., a clockwise (positive) torsion for neurons in the right iC and a counterclockwise (negative) torsional component when recorded in the left iC. The findings indicate that saccade-related burst neurons in the iC control coordinate axes for vertical and torsional quick eye rotations. As in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), burst neurons in the iC encode vertical saccades with an ipsitorsional direction with similar burst characteristics. It is suggested that iC burst neurons play a part in the local feedback loop of the reciprocal iC-riMLF projections.

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

  • Bartl K, Siebold C, Glasauer S, Helmchen C, Büttner U (1996) A simplified calibration method for 3D eye movement recordings using search coils. Vision Res 36:997–1006

    Google Scholar 

  • Büttner U, Büttner-Ennever JA, Henn V (1977) Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res 130:239–252

    Google Scholar 

  • Büttner-Ennever JA, Büttner U (1978) A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151:31–47

    Google Scholar 

  • Büttner-Ennever JA, Büttner U (1992) Neuroanatomy of the ocular motor pathways. Baillieres Clin Neurol Vol 1/2 263–287

    Google Scholar 

  • Büttner-Ennever JA, Büttner U (1988) The reticular formation. Rev Oculomot Res 2:119–176

    Google Scholar 

  • Crawford JD, Vilis T (1993) Modularity and parallel processing in the oculomotor integrator. Exp Brain Res 96:443–456

    Google Scholar 

  • Crawford JD, Vilis T (1992) Symmetry of oculomotor burst neuron coordinates about Listing's plane. J Neurophysiol 68:432–448

    Google Scholar 

  • Crawford JD, Cadera W, Vilis T (1991) Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal. Science 252:1551–1553

    Google Scholar 

  • Fukushima K, Fukushima J, Harada C, Ohashi T, Kase M (1990a) Neuronal activity related to vertical eye movement in the region of the interstitial nucleus of Cajal in alert cats. Exp Brain Res 79:43–64

    Google Scholar 

  • Fukushima K, Harada C, Fukushima J, Suzuki Y (1990b) Spatial properties of vertical eye movement-related neurons in the region of the interstitial nucleus of Cajal in awake cats. Exp Brain Res 79:25–42

    Google Scholar 

  • Fukushima K, Fukushima J, Ohashi T, Kase M (1991) Possible downward burster-driving neurons related to the anterior semicircular canal in the region of the interstitial nucleus of Cajal in alert cats. Neurosci Res 12:536–544

    Google Scholar 

  • Fukushima K, Kaneko CR, Fuchs AF (1992) The neuronal substrate of integration in the oculomotor system. Prog Neurobiol 39:609–639

    Google Scholar 

  • Fukushima K, Ohashi T, Fukushima J, Kaneko CR (1995) Discharge characteristics of vestibular and saccade neurons in the rostral midbrain of alert cats. J Neurophysiol 73:2129–2143

    Google Scholar 

  • Haustein W (1989) Considerations on Listing's law and the primary position by means of a matrix description of eye position control. Biol Cybern 60:411–420

    Google Scholar 

  • Helmchen C, Straube A, Büttner U (1994) Saccade-related activity in the fastigial oculomotor region of the macaque monkey during spontaneous eye movements in light and darkness. Exp Brain Res 98:474–482

    Google Scholar 

  • Henn V (1992) Pathophysiology of rapid eye movements in the horizontal, vertical and torsional directions. Baillieres Clin Neurol Vol 1–2 373–391

    Google Scholar 

  • Henn V, Cohen B (1976) Coding of information about rapid eye movements in the pontine reticular formation of alert monkeys. Brain Res 108:307–325

    Google Scholar 

  • Hepp K, Henn V, Vilis T, Cohen B (1989) Brainstem regions related to saccade generation. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 105–212

    Google Scholar 

  • Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535–538

    Google Scholar 

  • Kaneko CRS, Evinger C, Fuchs AF (1981) Role of cat pontine burst neurons in generation of saccadic eye movements. J Neurophysiol 46:387–408

    Google Scholar 

  • Kaneko CRS, Fukushima K (1993) Burst driver neurons in the mesencephalon of the trained rhesus monkey. Soc Neurosci Abstr 19:859

    Google Scholar 

  • King WM, Fuchs AF (1979) Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. J Neurophysiol 42:861–876

    Google Scholar 

  • King WM, Fuchs AF, Magnin M (1981) Vertical eye movementrelated responses of neurons in midbrain near interstitial nucleus of Cajal. J Neurophysiol 46:549–562

    Google Scholar 

  • King WM, Leigh RJ (1982) Physiology of vertical gaze. In: Lennerstrand EG, Zee DS, Keller EL (eds) Functional basis of ocular motility disorders. Pergamon, Oxford, pp 267–276

    Google Scholar 

  • Leigh RJ, Seidman SH, Grant MP, Hanna JP (1993) Loss of ipsidirectional quick phases of torsional nystagmus with a unilateral midbrain lesion. J Vestib Res 3:115–121

    Google Scholar 

  • Le Taillanter M (1991a) The interstitial nucleus of Cajal of the cat. I. Neurons activity related to vertical eye movements. Arch Ital Biol 129:73–85

    Google Scholar 

  • Le Taillanter M (1991b) The interstitial nucleus of Cajal of the cat. II. Effects of kainic acid lesions on vertical optokinetic nystamgus and after-nystagmus. Arch Ital Biol 129:87–96

    Google Scholar 

  • Li W-B, Shiraishi Y, Nakao S (1993) Topographical organization of cat mesodiencephalic areas for monosynaptic activation of vertical oculomotoneurons. Exp Brain Res 94:43–52

    Google Scholar 

  • Moschovakis AK, Scudder CA, Highstein SM (1991a) Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on directions. J Neurophysiol 65:203–217

    Google Scholar 

  • Moschovakis AK, Scudder CA, Highstein SM, Warren JD (1991b) Structure of the primate oculomotor burst generator. II. Medium-lead burst neurons with downward on-directions. J Neurophysiol 65:218–229

    Google Scholar 

  • Moschovakis AK (1994) Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. Biol Cybern 70:291–302

    Google Scholar 

  • Moschovakis AK, Highstein SM (1994) The anatomy and physiology of primate neurons that control rapid eye movements. Annu Rev Neurosci 17:465–488

    Google Scholar 

  • Robinson DA, Zee DS (1981) Theoretical considerations of the function and circuitry of various rapid eye movements. Prog Oculomot Res Vol 12 3–9

    Google Scholar 

  • Scudder CA (1988) A new local feedback model of the saccadic burst generator. J Neurophysiol 59:1455–1475

    Google Scholar 

  • Shiraishi Y, Nakao S (1994) Projections of vertical eye movementrelated and head rotation-related neurons in the medial mesodiencephalic junction to pontine reticular formation in cat. Neurosci Lett 171:85–88

    Google Scholar 

  • Shiraishi Y, Nakao S (1995) Differential locations in the midbrain of distinct groups of vertical eye movement-related neurones in cat: their projections and direct connections with oculomotor neurones. Acta Physiol Scand 154:151–163

    Google Scholar 

  • Strassman A, Highstein SM, McCrea RA (1986) Anatomy and Physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J Comp Neurol 249:337–357

    Google Scholar 

  • Suzuki Y, Straumann D, Hepp K, Henn V (1994) Three-dimensional representation of position coding in extra-ocular motoneurons in the rhesus monkey. In: Fuchs AF, Brandt Th, Büttner U, Zee DS (eds) Four decades of seminal vestibulooculomotor research. Thieme, Stuttgart, pp 528–536

    Google Scholar 

  • Suzuki Y, Büttner-Ennever JA, Straumann D, Hepp K, Hess BJM, Henn V (1995) Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uniand bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF). Exp Brain Res 106:215–232

    Google Scholar 

  • Tweed D, Cadera W, Vilis T (1990) Computing three dimensional eye position quaternions and eye velocity from search coil signals. Vison Res 30:97–110

    Google Scholar 

  • Vilis T, Hepp K, Schwarz U, Henn V (1989) On the generation of vertical and torsional rapid eye movements in the monkey. Exp Brain Res 77:1–11

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Helmchen, C., Rambold, H. & Büttner, U. Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey. Exp Brain Res 112, 63–78 (1996). https://doi.org/10.1007/BF00227179

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227179

Key words

Navigation