Blinks slow memory-guided saccades
Alice S. Powers,1Michele A. Basso,4,5,6,7and Craig Evinger2,3,8
1Department of Psychology, Stony Brook University, Stony Brook, New York;2Department of Neurobiology and Behavior,
Stony Brook University, Stony Brook, New York;3Department of Ophthalmology, Stony Brook University, Stony Brook,
New York;4Department of Neuroscience, University of Wisconsin Madison, Madison, Wisconsin;5Department of
Ophthalmology and Visual Sciences, University of Wisconsin Madison, Madison, Wisconsin;6Department of Psychiatry
and Biobehavioral Sciences, University of California Los Angeles, Los Angeles, California;7Semel Institute for Neuroscience
and Human Behavior, University of California Los Angeles, Los Angeles, California; and8State University of New York Eye
Institute, Syracuse, New York
Submitted 27 August 2012; accepted in final form 12 November 2012
Powers AS, Basso MA, Evinger C. Blinks slow memory-guided
saccades. J Neurophysiol 109: 734–741, 2013. First published No-
vember 14, 2012; doi:10.1152/jn.00746.2012.—Memory-guided sac-
cades are slower than visually guided saccades. The usual explanation
for this slowing is that the absence of a visual drive reduces the
discharge of neurons in the superior colliculus. We tested a related
hypothesis: that the slowing of memory-guided saccades was due also
to the more frequent occurrence of gaze-evoked blinks with memory-
guided saccades compared with visually guided saccades. We re-
corded gaze-evoked blinks in three monkeys while they performed
visually guided and memory-guided saccades and compared the
kinematics of the different saccade types with and without blinks.
Gaze-evoked blinks were more common during memory-guided sac-
cades than during visually guided saccades, and the well-established
relationship between peak and average velocity for saccades was
disrupted by blinking. The occurrence of gaze-evoked blinks was
associated with a greater slowing of memory-guided saccades com-
pared with visually guided saccades. Likewise, when blinks were
absent, the peak velocity of visually guided saccades was only slightly
higher than that of memory-guided saccades. Our results reveal
interactions between circuits generating saccades and blink-evoked
eye movements. The interaction leads to increased curvature of
saccade trajectories and a corresponding decrease in saccade velocity.
Consistent with this interpretation, the amount of saccade curvature
and slowing increased with gaze-evoked blink amplitude. Thus, al-
though the absence of vision decreases the velocity of memory-guided
saccades relative to visually guided saccades somewhat, the cooccur-
rence of gaze-evoked blinks produces the majority of slowing for
main sequence; orbicularis oculi; eye movements; lid movements;
SACCADIC EYE MOVEMENTS ARE rapid movements of the eyes that
reorient the line of sight. They are characterized by their
increase in speed with increasing amplitude (Becker 1989;
Westheimer 1954). The main sequence, the relationship be-
tween saccade amplitude and peak velocity (Bahill et al. 1975),
and the relationship between peak and average saccade veloc-
ity (Becker 1989; Evinger et al. 1981), are powerful measures
that can assess abnormalities in the brain stem circuitry con-
trolling saccade generation (Jürgens et al. 1981; Schmid-Burgk
et al. 1982).
Saccadic eye movements are driven by a variety of cues. In
the laboratory, a common approach is to use visual stimuli
located in the peripheral visual field as targets for saccades,
visually guided saccades. If the target appears in the periphery
only transiently, and the saccade is made at a later time when
the target is no longer visible, then the saccade is referred to as
memory guided (Hikosaka and Wurtz 1983). Visually guided
and memory-guided saccades exhibit different main sequence
functions, in spite of the fact that they share midbrain and brain
stem circuits for their generation (Moschovakis et al. 1996;
Sparks and Mays 1990). In general, saccades guided by mem-
ory are slower than saccades guided by vision (Gnadt and
Andersen 1988; Hikosaka and Wurtz 1983; Smit et al. 1987;
White et al. 1994). One hypothesis for this difference is that the
lack of visual drive to the superior colliculus reduces the
activity of neurons within the superior colliculus, which, in
turn, leads to slower saccadic velocities. Support for this idea
comes from data showing that transient reductions in superior
colliculus activity with either lidocaine or muscimol reduce
saccadic velocity (Basso et al. 2000; Hikosaka and Wurtz
1985; Lee et al. 1988). Similarly, saccades made to locations
without visual stimuli are associated with a reduced discharge
of action potentials from superior colliculus neurons compared
with saccades made to locations with visual stimuli (Edelman
and Goldberg 2001).
Another possible reason for the slowing of memory-guided
saccades is that a blink is more likely to occur with a memory-
than a visually guided saccade. Just as reflex blinks slow
saccadic eye movements by superimposing a “down and in”
movement on the ongoing saccadic eye movement (Goossens
and Van Opstal 2000a; Goossens and Van Opstal 2000b;
Rambold et al. 2004; Rottach et al. 1998), a blink associated
with a saccade, a gaze-evoked blink, may slow the saccadic eye
movement that it accompanies. Consistent with this hypothesis,
gaze-evoked blinks are less likely to occur in the presence of
visual stimuli that are behaviorally significant (Evinger et al.
1994; Williamson et al. 2005). For example, gaze-evoked
blinks rarely occur when monkeys make saccades to visual
targets for a reward, but frequently occur during unrewarded
saccades after the trial (Powers et al. 2006). Here, we test the
hypothesis that the occurrence of blinks associated with sac-
cades is the dominant reason for the slowing of memory-
guided saccades. We measured saccades guided by vision and
guided by memory in three monkeys and compared the main
sequence and curvature of saccades with and without blinks.
Address for reprint requests and other correspondence: A. Powers, Dept. of
Psychology, Stony Brook Univ., Stony Brook, NY 11794-2500 (e-mail:
J Neurophysiol 109: 734–741, 2013.
First published November 14, 2012; doi:10.1152/jn.00746.2012.
7340022-3077/13 Copyright © 2013 the American Physiological Society www.jn.org
Author contributions: A.S.P., M.A.B., and C.E. conception and design of
research; A.S.P. and M.A.B. performed experiments; A.S.P., M.A.B., and C.E.
analyzed data; A.S.P., M.A.B., and C.E. interpreted results of experiments;
A.S.P., M.A.B., and C.E. drafted manuscript; A.S.P., M.A.B., and C.E. edited
and revised manuscript; A.S.P., M.A.B., and C.E. approved final version of
manuscript; C.E. prepared figures.
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741BLINKS AND SACCADES
J Neurophysiol • doi:10.1152/jn.00746.2012 • www.jn.org