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The Journal of Neurophysiology Vol. 84 No. 2 August 2000, pp. 1035-1049
Copyright ©2000 by the American Physiological Society
1Biological Computation Research Department, Bell Laboratories, Lucent Technologies, Murray Hill, New Jersey 07974; 2Department of Physiology and Neuroscience, NYU School of Medicine, New York, New York 10016; and 3Brain and Cognitive Sciences Department, MIT, Cambridge, Massachusetts 02139
Aksay, E.,
R. Baker,
H. S. Seung, and
D. W. Tank.
Anatomy and Discharge Properties of Pre-Motor Neurons in the
Goldfish Medulla That Have Eye-Position Signals During Fixations. J. Neurophysiol. 84: 1035-1049, 2000. Previous work in goldfish has suggested that the oculomotor
velocity-to-position neural integrator for horizontal eye movements may
be confined bilaterally to a distinct group of medullary neurons that
show an eye-position signal. To establish this localization, the
anatomy and discharge properties of these position neurons were
characterized with single-cell Neurobiotin labeling and extracellular recording in awake goldfish while monitoring eye movements with the
scleral search-coil method. All labeled somata (n = 9)
were identified within a region of a medially located column of the inferior reticular formation that was ~350 µm in length, ~250 µm in depth, and ~125 µm in width. The dendrites of position
neurons arborized over a wide extent of the ventral half of the medulla with especially heavy ramification in the initial 500 µm rostral of
cell somata (n = 9). The axons either followed a
well-defined ventral pathway toward the ipsilateral abducens
(n = 4) or crossed the midline (n = 2)
and projected toward the contralateral group of position neurons and
the contralateral abducens. A mapping of the somatic region using
extracellular single unit recording revealed that position neurons
(n > 120) were the dominant eye-movement-related cell
type in this area. Position neurons did not discharge below a threshold
value of horizontal fixation position of the ipsilateral eye. Above
this threshold, firing rates increased linearly with increasing
temporal position [mean position sensitivity = 2.8 (spikes/s)/°,
n = 44]. For a given fixation position, average rates
of firing were higher after a temporal saccade than a nasal one
(n = 19/19); the magnitude of this hysteresis increased
with increasing position sensitivity. Transitions in firing rate
accompanying temporal saccades were overshooting (n = 43/44), beginning, on average, 17.2 ms before saccade onset
(n = 17). Peak firing rate change accompanying temporal
saccades was correlated with eye velocity (n = 36/41).
The anatomical findings demonstrate that goldfish medullary position
neurons have somata that are isolated from other parts of the
oculomotor system, have dendritic fields overlapping with axonal
terminations of neurons with velocity signals, and have axons that are
capable of relaying commands to the abducens. The physiological
findings demonstrate that the signals carried by position neurons could
be used by motoneurons to set the fixation position of the eye. These
results are consistent with a role for position neurons as elements of
the velocity-to-position neural integrator for horizontal eye movements.
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