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The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2612-2632
Copyright ©1999 by the American Physiological Society
Aerospace Medical Research Unit, McGill University, Montreal, Quebec H3G 1Y6, Canada
Sylvestre, Pierre A. and
Kathleen E. Cullen.
Quantitative Analysis of Abducens Neuron Discharge Dynamics
During Saccadic and Slow Eye Movements. J. Neurophysiol. 82: 2612-2632, 1999. The mechanics of the eyeball
and its surrounding tissues, which together form the oculomotor plant,
have been shown to be the same for smooth pursuit and saccadic eye
movements. Hence it was postulated that similar signals would be
carried by motoneurons during slow and rapid eye movements. In the
present study, we directly addressed this proposal by determining which
eye movement-based models best describe the discharge dynamics of
primate abducens neurons during a variety of eye movement behaviors. We
first characterized abducens neuron spike trains, as has been
classically done, during fixation and sinusoidal smooth pursuit. We
then systematically analyzed the discharge dynamics of abducens neurons
during and following saccades, during step-ramp pursuit and during high
velocity slow-phase vestibular nystagmus. We found that the commonly
utilized first-order description of abducens neuron firing rates
(FR = b + kE + r
, where FR is firing rate, E and are eye
position and velocity, respectively, and b,
k, and r are constants) provided an
adequate model of neuronal activity during saccades, smooth pursuit,
and slow phase vestibular nystagmus. However, the use of a second-order
model, which included an exponentially decaying term or "slide"
(FR = b + kE + r + uË 
c
), notably improved our ability to describe
neuronal activity when the eye was moving and also enabled us to model
abducens neuron discharges during the postsaccadic interval. We also
found that, for a given model, a single set of parameters could not be
used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients (r and k in the above models,
respectively) consistently decreased as a function of the mean (and
peak) eye velocity that was generated. In contrast, the bias
(b, firing rate when looking straight ahead) invariably
increased with eye velocity. Although these trends are likely to
reflect, in part, nonlinearities that are intrinsic to the extraocular
muscles, we propose that these results can also be explained by
considering the time-varying resistance to movement that is generated
by the antagonist muscle. We conclude that to create realistic and
meaningful models of the neural control of horizontal eye movements, it
is essential to consider the activation of the antagonist, as well as
agonist motoneuron pools.
This article has been cited by other articles:
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L. Ling, A. Fuchs, C. Siebold, and P. Dean Effects of Initial Eye Position on Saccade-Related Behavior of Abducens Nucleus Neurons in the Primate J Neurophysiol, December 1, 2007; 98(6): 3581 - 3599. [Abstract] [Full Text] [PDF]
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J. R. Economides, D. L. Adams, C. M. Jocson, and J. C. Horton Ocular Motor Behavior in Macaques With Surgical Exotropia J Neurophysiol, December 1, 2007; 98(6): 3411 - 3422. [Abstract] [Full Text] [PDF]
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M. Beraneck and K. E. Cullen Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse J Neurophysiol, September 1, 2007; 98(3): 1549 - 1565. [Abstract] [Full Text] [PDF]
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M. K. McCluskey and K. E. Cullen Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture J Neurophysiol, April 1, 2007; 97(4): 2976 - 2991. [Abstract] [Full Text] [PDF]
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 V. E. Das and M. J. Mustari Correlation of Cross-Axis Eye Movements and Motoneuron Activity in Non-Human Primates with "A" Pattern Strabismus Invest. Ophthalmol. Vis. Sci., February 1, 2007; 48(2): 665 - 674. [Abstract] [Full Text] [PDF]
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S. G. Sadeghi, L. B. Minor, and K. E. Cullen Response of Vestibular-Nerve Afferents to Active and Passive Rotations Under Normal Conditions and After Unilateral Labyrinthectomy J Neurophysiol, February 1, 2007; 97(2): 1503 - 1514. [Abstract] [Full Text] [PDF]
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 S. G. Sadeghi, M. J. Chacron, M. C. Taylor, and K. E. Cullen Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System J. Neurosci., January 24, 2007; 27(4): 771 - 781. [Abstract] [Full Text] [PDF]
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R. Ramachandran and S. G. Lisberger Transformation of Vestibular Signals Into Motor Commands in the Vestibuloocular Reflex Pathways of Monkeys J Neurophysiol, September 1, 2006; 96(3): 1061 - 1074. [Abstract] [Full Text] [PDF]
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P. A. Sylvestre and K. E. Cullen Premotor correlates of integrated feedback control for eye-head gaze shifts. J. Neurosci., May 3, 2006; 26(18): 4922 - 4929. [Abstract] [Full Text] [PDF]
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K. K. Porter, R. R. Metzger, and J. M. Groh Representation of Eye Position in Primate Inferior Colliculus J Neurophysiol, March 1, 2006; 95(3): 1826 - 1842. [Abstract] [Full Text] [PDF]
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S. Sklavos, D. M. Dimitrova, S. J. Goldberg, J. Porrill, and P. Dean Long Time-Constant Behavior of the Oculomotor Plant in Barbiturate-Anesthetized Primate J Neurophysiol, February 1, 2006; 95(2): 774 - 782. [Abstract] [Full Text] [PDF]
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 J. A. Cromer and D. M. Waitzman Neurones associated with saccade metrics in the monkey central mesencephalic reticular formation J. Physiol., February 1, 2006; 570(3): 507 - 523. [Abstract] [Full Text] [PDF]
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W.W.P. Chan and H. L. Galiana Integrator Function in the Oculomotor System Is Dependent on Sensory Context J Neurophysiol, June 1, 2005; 93(6): 3709 - 3717. [Abstract] [Full Text] [PDF]
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J. J. DiCarlo and J. H. R. Maunsell Using Neuronal Latency to Determine Sensory-Motor Processing Pathways in Reaction Time Tasks J Neurophysiol, May 1, 2005; 93(5): 2974 - 2986. [Abstract] [Full Text] [PDF]
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S. Ono, V. E. Das, J. R. Economides, and M. J. Mustari Modeling of Smooth Pursuit-Related Neuronal Responses in the DLPN and NRTP of the Rhesus Macaque J Neurophysiol, January 1, 2005; 93(1): 108 - 116. [Abstract] [Full Text] [PDF]
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P. A. Sylvestre, J. T. L. Choi, and K. E. Cullen Discharge Dynamics of Oculomotor Neural Integrator Neurons During Conjugate and Disjunctive Saccades and Fixation J Neurophysiol, August 1, 2003; 90(2): 739 - 754. [Abstract] [Full Text] [PDF]
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P. A. Sylvestre and K. E. Cullen Dynamics of Abducens Nucleus Neuron Discharges During Disjunctive Saccades J Neurophysiol, December 1, 2002; 88(6): 3452 - 3468. [Abstract] [Full Text] [PDF]
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M. Huterer and K. E. Cullen Vestibuloocular Reflex Dynamics During High-Frequency and High-Acceleration Rotations of the Head on Body in Rhesus Monkey J Neurophysiol, July 1, 2002; 88(1): 13 - 28. [Abstract] [Full Text] [PDF]
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K. E. Cullen and L. B. Minor Semicircular Canal Afferents Similarly Encode Active and Passive Head-On-Body Rotations: Implications for the Role of Vestibular Efference J. Neurosci., May 30, 2002; (2002) 20026418. [Abstract] [Full Text] [PDF]
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 D. M. WAITZMAN, J. PATHMANATHAN, R. PRESNELL, A. AYERS, and S. DePALMA Contribution of the Superior Colliculus and the Mesencephalic Reticular Formation to Gaze Control Ann. N.Y. Acad. Sci., April 1, 2002; 956(1): 111 - 129. [Abstract] [Full Text] [PDF]
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A. S. Dubrovsky and K. E. Cullen Gaze-, Eye-, and Head-Movement Dynamics During Closed- and Open-Loop Gaze Pursuit J Neurophysiol, February 1, 2002; 87(2): 859 - 875. [Abstract] [Full Text] [PDF]
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P. A. Sylvestre, H. L. Galiana, and K. E. Cullen Conjugate and Vergence Oscillations During Saccades and Gaze Shifts: Implications for Integrated Control of Binocular Movement J Neurophysiol, January 1, 2002; 87(1): 257 - 272. [Abstract] [Full Text] [PDF]
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P. A. SYLVESTRE, J. E. ROY, and K. E. CULLEN Do Extraocular Motoneurons Encode Head Velocity during Head-Restrained versus Head-Unrestrained Saccadic and Smooth Pursuit Movements? Ann. N.Y. Acad. Sci., October 1, 2001; 942(1): 497 - 500. [Full Text] [PDF]
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K. E. Cullen, H. L. Galiana, and P. A. Sylvestre Comparing Extraocular Motoneuron Discharges During Head-Restrained Saccades and Head-Unrestrained Gaze Shifts J Neurophysiol, January 1, 2000; 83(1): 630 - 637. [Abstract] [Full Text] [PDF]
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