1Regional Primate Research Center, 2Department of Physiology and Biophysics, and 3Department of Otolaryngology HNS, University of Washington, Seattle, Washington 98195
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ABSTRACT |
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Ling, Leo, Albert F. Fuchs, James O. Phillips, and Edward G. Freedman. Apparent Dissociation Between Saccadic Eye Movements and the Firing Patterns of Premotor Neurons and Motoneurons. J. Neurophysiol. 82: 2808-2811, 1999. Saccadic eye movements result from high-frequency bursts of activity in ocular motoneurons. This phasic activity originates in premotor burst neurons. When the head is restrained, the number of action potentials in the bursts of burst neurons and motoneurons increases linearly with eye movement amplitude. However, when the head is unrestrained, the number of action potentials now increase as a function of the change in the direction of the line of sight during eye movements of relatively similar amplitudes. These data suggest an apparent uncoupling of premotor neuron and motoneuron activity from the resultant eye movement.
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INTRODUCTION |
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One of the basic tenets of oculomotor research is
that the activity of the motoneurons that innervate the eye muscles
uniquely specifies the movement of the eye in the head under all
circumstances (Robinson 1975). This has been
demonstrated for abducens motoneurons, which drive the lateral rectus
muscle to produce abduction of the eye (Fuchs and Luschei
1970
). Furthermore, the discharge patterns of all
abducens neurons are thought to be qualitatively similar (Keller
and Robinson 1972
); all reflect the passive constraints imposed by the globe and its connective tissue, known collectively as
the oculomotor plant (Robinson 1975
).
Most previous studies of eye-movement-related neurons in the brain
stem were done with the subject's head restrained so that changes in
the direction of the line of sight (gaze amplitude) were accomplished
only with saccadic eye movements. During ipsiversive saccades,
motoneurons exhibit a burst of action potentials, which overcomes the
viscous drag of the oculomotor plant. During the stable fixations that
precede and follow saccades, abducens neurons display a steady firing
rate, which is proportional to the eccentricity of the eye in the orbit
(Fuchs and Luschei 1970; Keller and Robinson 1972
). This steady firing holds the eye in place against the
elastic restoring forces of the plant.
Physiological data from several species indicate that the burst of
motoneurons with ipsiversive saccades and their pause in activity with
contraversive saccades is the result of direct inputs from medium-lead
burst neurons (MLBs), which are part of a neuronal burst generator that
resides in the brain stem reticular formation (Moshovakis et al.
1996). During saccades, MLBs discharge a high-frequency burst,
and saccade amplitude increases linearly with the number of action
potentials. According to the Robinson (1975)
model, MLBs
transmit a saccade velocity command to motoneurons based on the eye
motor error. This command also is integrated, in the mathematical
sense, to provide the eye-position-related steady discharge of ocular
motoneurons. The observed linear increase of saccade amplitude with the
number of action potentials in MLBs is a corollary of this mathematical integration.
When the head is free to turn, gaze shifts can be achieved by a
combination of eye saccades and rapid head movements (Freedman and Sparks 1997; Guitton and Volle 1987
;
Phillips et al. 1995
). MLBs continue to discharge a
vigorous burst for such head-unrestrained gaze shifts, and the number
of action potentials in the burst of many such cells is better
correlated with gaze amplitude than with eye amplitude (Cullen
and Guitton 1997
; Phillips 1993
;
Whittington et al. 1984
). The fact that the number of
action potentials in premotoneuron bursts does not predict the
amplitude of eye movements suggests that premotor activity can be
uncoupled from the resultant eye movement. However, the interpretation
of the behavior of premotor brain stem neurons depends critically on
how these neural signals are processed on the way to the eye muscles.
Therefore it is important to know how ocular motoneurons behave when
the head is unrestrained.
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METHODS |
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Extracellular action potentials were recorded from the brain
stem of four monkeys trained to follow a small jumping light spot for
an applesauce reward. Detailed descriptions of our target presentation
and unit recording conditions have been published elsewhere
(Phillips et al. 1999). Tracking of the jumping target was achieved either with the head unrestrained or held. Gaze shifts with the head unrestrained were collected before those with the head
fixed; ~50% of the neurons were lost when the head was fixed. Activity was recorded from abducens neurons and MLBs. Although our
abducens neurons were not identified by their projections, their
discharge characteristics (thresholds and slopes of firing rate vs. eye
position relations) were typical of the lateral rectus motoneurons or
internuclear neurons, which project directly to medial rectus
motoneurons, that we described previously (Fuchs et al.
1988
). In contrast to burst-tonic neurons in the nearby nucleus
prepositus hypoglossi, ours all paused for contraversive saccades. The
MLBs considered here lay rostral to the ipsilateral abducens nucleus,
i.e., were excitatory, and had latencies <10 ms; we will refer to them
as excitatory burst neurons (EBNs). Each gaze shift and its
associated instantaneous firing rate were displayed on a computer
monitor, and locally developed programs identified the onset and end of
the gaze shift and its eye- and head-movement components and counted
the associated action potentials.
All the surgeries, training procedures, and recording conditions in this study were approved by the Animal Care and Use Committee at the University of Washington.
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RESULTS |
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Figure 1 compares the behavior of an EBN with that of an abducens neuron during head-fixed gaze shifts. As reported elsewhere, saccade amplitude increases linearly with the number of spikes in the burst (Fig. 1B). For the 14 EBNs examined here, the slope was 1.07 ± 0.34°/action potential (mean ± SD; r = 0.94 ± 0.05). As expected from the direct connections of EBNs to motoneurons, saccade amplitude also increases linearly with the number of action potentials in the burst of an abducens neuron (Fig. 1D). For 14 abducens neurons recorded with the head restrained, the slope of the relation was 0.96 ± 0.36°/action potential (r = 0.93 ± 0.04).
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Figure 2 shows the behavior of the EBN in Fig. 1 when the head is free to turn. In Fig. 2A, gaze shifts of different sizes are produced by eye displacements of nearly equal size. Because burst duration is longer for the larger gaze shift but peak firing rates are roughly comparable, the same amplitude eye saccade is associated with different numbers of action potentials. After eye-movement amplitude saturates during the largest gaze shifts, the number of action potentials continues to increase (Fig. 2B). Consequently, the number of spikes shows a linear relation with gaze amplitude but a nonlinear relation with eye amplitude.
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During head-unrestrained gaze shifts, the relation between movement amplitude and the number of action potentials in the burst of abducens neurons resembles that observed in EBNs. For the abducens neuron of Fig. 1, the number of action potentials in the burst again was larger for the larger of the two illustrated gaze shifts, although the amplitudes of the two eye-movement components were roughly equal (Fig. 2C). Indeed, although the number of action potentials ranged from 30 to 60, the amplitude of the saccade changed little. In contrast, gaze amplitude continued to increase with the number of action potentials.
We observed a saturation of the relation between eye amplitude and
number of action potentials in all 30 of our abducens units recorded
with the head unrestrained. To compare data across neurons, we fit the
number of action potentials versus eye- or gaze-amplitude relations
with exponential functions. The relation between either eye or gaze
amplitude and the number of action potentials (N) was
fit with exponentials of the following form:
a1 + a2 * exp(a3 * N).
For the example in Fig. 2D, r2 was 0.95 for
gaze movement and 0.94 for eye movement. As can be seen in Fig.
3, the best fit with eye amplitude always
appears to saturate, whereas that for gaze amplitude usually continues to increase.
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It seems unlikely that the saturation is due to active braking by the antagonist because we saw no evidence of a burst of firing at the end of saccades in the contraversive direction. Also, correcting for the position component of the unit's discharge did not change the fundamental differences between the gaze and eye relations.
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DISCUSSION |
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With the head unrestrained, the number of action potentials in a
motoneuron burst no longer accurately predicts the amplitude of an eye
movement as it did with the head restrained. This is not to imply that
when the head is unrestrained the dynamics of the oculomotor plant are
different. Rather, when the head contributes to gaze shifts, the wide
variety of movement kinematics exposes complexities of the plant that
first-order approximations neglect (Fuchs et al. 1988).
Dissociations between motoneuron discharge and eye movements also
appear during monocular eye movements (Zhou and King
1998
).
Because EBNs and motoneurons show similar relations between the number
of action potentials and either eye- or gaze-movement amplitude, both
must encode the same variable. If this variable were gaze, then we are
left with the illogical conclusion that eye motoneurons encode
eye-position-in-space. This clearly is incorrect because abducens
motoneurons are deeply modulated if an animal stabilizes its gaze in
space during the vestibuloocular reflex (Skavenski and Robinson
1973).
The burst of motoneurons commands an eye saccade and nothing more.
Because premotor elements behave in the same way as motoneurons, their
discharge must be a "smart" eye movement command rather than a
signal that encodes gaze amplitude, as previously suggested (Cullen and Guitton 1997; Pélisson et al.
1988
; Tomlinson 1990
; Whittington et al.
1984
).
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ACKNOWLEDGMENTS |
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We are grateful for the participation of Y. Iwamoto, S. Newlands, and C. Siebold in some phases of these experiments. We appreciate the editorial magic of K. Elias.
This research was supported by National Institutes of Health Grants RR-00166 and EY-00745 and by Training Grant 5T32NS-07395 to E. G. Freedman.
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FOOTNOTES |
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Address for reprint requests: A. F. Fuchs, Regional Primate Research Center, Box 357330, University of Washington, Seattle, WA 98195-7330.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 24 June 1999; accepted in final form 3 August 1999.
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REFERENCES |
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