Does orbital proprioception contribute to gaze stability during translation?

RESEARCH ARTICLE

Does orbital proprioception contribute to gaze stabilityduring translation?

Min Wei • Nan Lin • Shawn D. Newlands

Received: 3 August 2011 / Accepted: 8 September 2011 / Published online: 27 September 2011

� Springer-Verlag 2011

Abstract Translational motion induces retinal image slip

which varies with object distance. The brain must know

binocular eye position in real time in order to scale eye

movements so as to minimize retinal slip. Two potential

sources of eye position information are orbital propriocep-

tion and an internal representation of eye position derived

from central ocular motor signals. To examine the role of

orbital proprioceptive information, the position of the left

eye was perturbed by microstimulation of the left abducens

nerve during translational motion to the right or left along

the interaural axis in two rhesus macaques. Microstimula-

tion rotated the eye laterally, activating eye muscle pro-

prioceptors, while keeping central motor commands

undisturbed. We found that microstimulation-induced eye

position changes did not affect the translational VOR in the

abductive (lateral rectus) direction, but it did influence the

responses in the adductive (medial rectus) direction. Our

findings demonstrate that proprioceptive inputs appear to be

involved in the TVOR responses at least during ipsilateral

head movements and proprioceptive influences on the

TVOR may involve vergence-related signals to the oculo-

motor nucleus. However, internal representation of eye

position, derived from central ocular motor signals, likely

plays the dominant role in providing eye position infor-

mation for scaling eye movements during translational

motion, particularly in the abducent direction.

Keywords Eye movement � Vestibulo-ocular reflex �Proprioception � Viewing distance � Translational motion

Introduction

As we move through a stationary visual environment, such

as when walking or riding in a car, the speed of images

traveling over the retina varies with object distance. Gen-

erally, it is impossible to stabilize the entire visual world at

any moment during translational movements. Instead, the

translational vestibulo-ocular reflex (TVOR) has evolved to

maintain a target of interest on both foveae simultaneously

(Angelaki 2004; Angelaki and Hess 2001; Miles 1993,

1998; Paige and Tomko 1991a, b). To stabilize the foveal

image during translation, the amplitude of compensatory

eye movements must be scaled precisely depending on

both viewing direction and viewing distance from each eye.

As a result, eye movement responses to translation exhibit

a dependence on eye position relative to the head (Angelaki

and Hess 2001; Wei and Angelaki 2006) and on vergence

angle, a relative position of one eye to the other (Angelaki

2004; Angelaki and Hess 2001; McHenry and Angelaki

2000; Paige 1991; Paige and Tomko 1991b; Schwarz and

Miles 1991; Wei et al. 2003).

Internal representations of eye position derived from

motor command signals (corollary discharge) (Green and

Angelaki 2010; Green et al. 2007) and proprioceptive

M. Wei � N. Lin � S. D. Newlands

Department of Otolaryngology, University of Texas Medical

Branch, Galveston, TX 77555-0521, USA

M. Wei (&) � S. D. Newlands (&)

Department of Otolaryngology, University of Rochester Medical

Center, 601 Elmwood Ave., Box 629, Rochester,

NY 14642, USA

e-mail: [email protected]

S. D. Newlands

e-mail: [email protected]

Present Address:N. Lin

Department of Biomedical Sciences, Mercer University School

of Medicine, 4700 Waters Avenue, Savannah, GA 31404, USA

123

Exp Brain Res (2011) 215:77–87

DOI 10.1007/s00221-011-2873-y

information from palisade endings in extraocular muscles

(Buttner-Ennever and Horn 2002; Eberhorn et al. 2005;

Ruskell 1999) can encode information about instantaneous

eye position. Previous reports have demonstrated that

internal models of eye movement command signals from

different levels in the central nervous system contribute to

VOR scaling. For example, when viewing distance changes

can be anticipated in visual-motor tasks requiring either

target fixation or smooth pursuit, the VOR gain can be

adjusted in advance of the actual eye position change

(Paige 1991; Semrau et al. 2006; Snyder et al. 1992). In

experiments where a subject executes an eye movement

that will change ocular vergence, the gain of the rotational

VOR (RVOR) anticipates the actual vergence change by

50 ms or more (Snyder et al. 1992) and the TVOR antic-

ipates the eye position change by about 169 ms (Semrau

et al. 2006). These data suggest that a motor command-

related signal (efferent copy or corollary discharge) rather

than proprioceptive eye position information is the main

source used to modulate the VOR responses under these

experimental conditions. The eye responds to head move-

ment at a very short latency (6–7 ms for RVOR; Huterer

and Cullen 2002; Minor et al. 1999; and 7–13 ms for

TVOR, Angelaki and McHenry1999; Zhou et al. 2002,

2003), and the effect of viewing distance on the VOR is

seen within 30 ms of the initiation of the head movement

(Snyder and King 1992, 1996). Signals from brainstem

nuclei, such as prepositus hypoglossi and the vestibular

nuclei, or the midbrain are likely involved in VOR gain

modulation during static fixation tasks. The abundance of

neurons that encode eye position in the prepositus hypo-

glossi and vestibular nuclei (Chen-Huang and McCrea

1999; Cullen and McCrea 1993; Fuchs and Kimm 1975;

Keller 1974; King et al. 1976; McFarland and Fuchs 1992;

Meng and Angelaki 2006; Scudder and Fuchs 1992) could

be the substrate for VOR scaling based on internal repre-

sentation of eye position (Green and Angelaki 2010, Green

et al. 2007).

While corollary discharge mechanisms appear to play a

dominant role in eye movement control mechanisms,

experimental data suggest a role for proprioceptive infor-

mation in eye alignment, maintenance of eye fixation, and

perception of a target’s spatial location (Donaldson 2000;

Gauthier et al. 1990; Lewis et al. 1994; Weir et al. 2000).

However, as the TVOR depends on eye position in real

time to maintain gaze stability during translational motion

and considering that the vestibular system and proprio-

ceptive information from the body and neck are highly

convergent (Angelaki et al. 2009; Cullen 2004; Gdowski

and McCrea 2000), one may expect some role for propri-

oception from the eye plant in TVOR modulation.

To examine the relative role of orbital proprioception

compared with corollary discharge in modulating TVOR

responses, we brought one eye away from its original fix-

ation position by microstimulation of the abducens nerve

while TVOR responses were studied during transient

translational motion along the interaural axis. If orbital

proprioception provides enough information for the TVOR

modulation mechanism, one should expect the eye velocity

response to translation to be scaled as a function of the

perturbed (actual) eye position. If the mechanism depends

only on an internal representation of eye position, then

TVOR response amplitudes should be unaffected by the

microstimulation. Our results showed that unilateral pas-

sive abductive eye position displacement caused by abdu-

cens stimulation influenced TVOR responses for the eye

ipsilateral to the head movement (adductive eye move-

ments) but not for the eye contralateral to the direction of

movement (abductive eye movements).

Materials and methods

Subjects and experimental preparation

Two rhesus monkeys (6.3 and 7 kg) were chronically

implanted with a stainless steel sleeve (for connecting a

stainless steel head restraint bar) and a neural recording

chamber, both anchored to dental acrylic applied on

inverted stainless steel T-bolts inserted in narrow slits

drilled into the skull (Newlands et al. 2009). A 3-turn

15.5 mm scleral eye coil was surgically implanted under

the conjunctiva in each eye (Judge et al. 1980). All surgical

procedures and animal handling were in accordance with

institutional (the University of Texas Medical Branch,

Galveston) and National Institutes of Health guidelines.

During experiments, the animal’s head was restrained

and the animal was seated upright in a primate chair

secured on a vestibular turntable system (SHOT Inc.,

Greenville, IN) atop a linear sled. A three-axis linear

accelerometer was mounted on the head restraint structure

at about the same level as the vestibular end organs. Bin-

ocular horizontal and vertical eye movements were mea-

sured by a magnetic coil system (CNC Engineering,

Seattle, WA), and eye movement signals were digitized at

800 Hz with 16-bit resolution and stored for off-line

analysis. A program custom-written in LabVIEW real-time

software (National Instruments, Austin, TX) controlled the

visual stimulus presentation, the microstimulation, the sled

motion profiles, and data acquisition.

The left abducens nucleus was first identified by its

characteristic burst–tonic activity during ipsilateral eye

movements (Fuchs and Luschei 1970). The left abducens

nerve was then identified two millimeters anterior, lateral,

and ventral to the abducens nucleus by its same burst–tonic

activity during ipsilateral eye movements (Klier et al.

78 Exp Brain Res (2011) 215:77–87

123

2006). Only the left abducens nerve was stimulated in these

experiments (Fig. 1). For microstimulation trials, a bipha-

sic stimulation train (pulse duration: 0.2 ms; frequency:

500 Hz) was generated by a biphasic pulse generator (BAK

Electronics, Mount Airy, MD) and passed through a

stimulation isolator (BAK Electronics, Mount Airy, MD).

The stimulation resulted in a step of eye position that

remained until the stimulation was turned off. In the

present experiment, we defined the threshold of abducens

nerve stimulation as the lowest current eliciting an obvious,

reliably detectable eye movement (eye movement velocity

[15�/s and seen in 100% of 10 consecutive stimulation

trials). Three stimulation intensities, 1.5, 2.0, and 2.5 times

the threshold level, were used in the experiment and the

current never exceeded 100 lA.

Animal training and experimental protocol

Both animals had been previously trained on different

saccade and smooth pursuit tasks. Eye movements were

calibrated daily via a task which required the animal to

fixate targets with ±108 and ±208 horizontal and vertical

eccentricities monocularly. Three red light-emitting diodes

(LEDs) were mounted at eye level directly between the two

eyes at distances of 12, 48, and 96 cm from the animal. The

frame on which the targets were displayed was tilted

toward the animal slightly (\2�) to avoid the far targets

being blocked by the near ones. While the animal was

stationary, one of the three targets was turned on in a dimly

lit room. Room lights were on while the monkey fixated

and were extinguished just as the fixation target was turned

off. The animal was required to fixate the illuminated target

for one second prior to turning off the target and room

lights and hold that eye position stable on the remembered

target for at least another 300 ms in complete darkness for

drops of liquid reward (with vergence and version windows

of ±1� and ±1.5�, respectively). After the animal was

familiar with the experimental procedure, leftward and

rightward passive whole-body translational movements

along the interaural axis were added. The motion profile

consisted of a position ramp (±5 cm) with step acceleration

(peak value *196 cm/s2, or 0.2 g) over a short duration

(*350 ms). For each trial in any single block, one of the

three LED targets and one of the three sled states (leftward

motion, stationary or rightward motion) were randomly

chosen and delivered, avoiding predication of target loca-

tion or motion direction. Data were collected after

*1 week when the animals were familiar with the motion

procedures.

In the data collection trials, microstimulation to the left

abducens nerve was delivered for 500 ms, starting imme-

diately after the target and room lights were turned off

(‘‘target-off’’). The motion onset occurred in the dark 70,

120, or 170 ms after target-off. This motion delay relative

to the microstimulation allowed the left eye to reach and

maintain a new, more abducted position and also allowed

adequate time for possible proprioceptive feedback. In the

microstimulation trials, only the near target was used as the

fixation point because as the stimulation abducted the eye

from its original fixation position for the near target, this

movement also set the point of binocular fixation further

from the animal. TVOR magnitude is greater with near

targets and declines sharply with distant targets (smaller

vergence angle), so the effect of changing eye position

could be better seen starting with near target fixation. The

behavioral window was removed during motion and

microstimulation trials to avoid inappropriate punishment,

but was enforced in stationary trials without microstimu-

lation to ensure that animals always tried to maintain

vergence in the dark at least 300 ms to be rewarded. The

general procedures and motion profiles were kept consis-

tent across the experiment. On trials where the monkey

broke target fixation, the trial was aborted, and the data

were discarded. Trials with saccadic movements during

sled motion were also excluded in the current analysis.

Control data were collected using identical procedures and

motion profiles as those used during the microstimulation

trials. The interval between two adjacent trials was *7 s.

Data analysis

Experimental data were analyzed with custom-written

scripts in MatLab (MathWorks, Natick, MA). Eye velocity

was computed by differentiation of eye position using a

polynomial filter (Angelaki 1998; Savitsky and Golay

1964). Leftward eye movements are plotted as positive.

Because the microstimulation of the abducens nerve only

elicited abductive eye movement, and generally vertical

Fig. 1 Schematic diagram of involuntary eye displacement by

stimulating the left abducens nerve during fixation of a near target

Exp Brain Res (2011) 215:77–87 79

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eye excursions were small during lateral motion, so only

horizontal eye movement was analyzed in present experi-

ments. Analysis was done for both the right and left eyes.

The left abducens nerve was subject to continuous stimu-

lation throughout the duration of the trials, relocating the

position of the left eye in the orbit and relative to the right

eye. For the right eye, stimulation of the left abducens does

not change its position, only its relative position to the left

eye. This relationship between the two eyes is described by

the vergence angle (VA, mathematically as the right eye

position - left eye position).

We examined the influence of changing of left eye

position on TVOR by directly comparing eye velocities

after motion onset. In the stimulation trials, because only

left eye was deviated from its original fixation position at

near target and the right eye position was relatively stable

before motion onset, therefore the difference of VA

between the data before target-off and the data before

motion onset actually was nearly the same as the change of

left eye position (CLEP) induced by the stimulation. We

defined this difference of VA as the CLEP relative to the

vergence angle at near target. In detail, the CLEP was

calculated as the difference of VA between the data at

10 ms before target-off (T1 in Fig. 2b) and the data right

before the motion onset (T2 in Fig. 2b) for the near target

(12 cm) in both control and stimulation trials. However,

the mean value of VA (MVA) for the near target trials was

used as a substitute value for T1 in control trials to cal-

culate the CLEP for the far target, i.e., the MVA at 10 ms

before target-off (T1) was first calculated for near target in

control trials. The CLEP for far target was computed as the

difference between MVA for near target and the VA of

each far target trial right before motion onset (VA at T2).

Despite the short latency of TVOR responding to the

stimulation of vestibular apparatus (less 13 ms; Angelaki and

McHenry 1999; Zhou et al. 2002, 2003), the stabilization

mechanism for visual targets may have up to 60 ms latency

during translational motion in monkeys (see Miles 1988 for

review). Thus, we measured eye velocities between 65 ms

and 100 ms after motion onset (at time points every 5 ms,

e.g., T3 in Fig. 2b) for attaining steady stabilization responses

to analyze the influence of proprioceptive feedback.

The left eye velocity declined before motion onset in

most microstimulation trials. To eliminate the influence of

the residual drift induced by microstimulation on the result,

we corrected the drift of left eye velocity by subtracting the

mean value at the same time from stationary trials with

microstimulation. However, there was no significant dif-

ference between data before and after correction. There-

fore, we used the eye velocity without any correction in

subsequent analysis.

For ease of comparison of data from both directions of

movement, the horizontal eye velocity at each point during

each stimulation and non-stimulation motion trials was

normalized by dividing by the mean velocity at that time

point for the near viewing distance (12 cm) in the control

trials. Regression lines were computed for both normalized

control and stimulated velocities as a function of CLEP. To

understand whether eye velocity in response to translation

took into account either the original left eye position

(corollary discharge hypothesis) or the new left eye posi-

tion (proprioceptive hypothesis) for each stimulation trial,

Fig. 2 Compensatory eye movement scaled by target distance during

lateral motion. Superimposed left eye (Leye, gray) and right eye

(Reye, black) position (Epos) and velocity (Evel) responses are

aligned at motion onset. Thin dotted lines are linear sled acceleration.

Data from M1 for the rightward translation. Upward indicates the eye

moves to the left. a Steady fixation of a far target (96 cm) or a near

target (12 cm) in control trials. Eye velocity depends on target

distance and position, with left eye responses being larger than those

of the right eye during motion to the right, and the reverse being true

during motion to the left. b Steady fixation on a near target (12) cm

with microstimulation applied to the left abducens nerve. Uprightthick arrows showing where data are taken for analysis: 10 ms before

target-off (T1), right before motion onset (T2), and after motion onset

(T3). Target on/off conditions are shown at the bottom of the panel

80 Exp Brain Res (2011) 215:77–87

123

we plotted the normalized stimulated velocity versus the

velocity predicted for that CLEP, based on the regression

line of the normalized control velocity versus CLEP plot

described above.

Results

The TVOR was measured in two rhesus monkeys during

lateral transient movements without intervention (control

trials) or after (stimulated trials) the left eye position was

unpredictably altered by electrical stimulation which chan-

ged proprioceptive feedback but not internal eye movement

control signals. In control trials (Fig. 2a), as typical of TVOR

responses studied by others (Angelaki and McHenry 1999;

Paige 1989; Schwarz et al. 1989; Zhou et al. 2002), eye

velocities varied inversely to the target distance, i.e., the

further the target, the smaller the deviation of eye position

from fixation position and the smaller the eye velocity

amplitude. Figure 2b shows eye movement responses in

stimulated trials to identical motion profiles as shown in

Fig. 2a. Motion delay was 120 ms after stimulation initiation

(three stimulation intensities, 1.5, 2.0, and 2.5 times the

threshold current level). When the left eye was brought away

from its fixation position and held at or near a new position by

stimulating the left abducens nerve, the TVOR response

magnitude of the right eye on movement to the left appears

similar with what would be expected from the original eye

position rather than the perturbed eye position, though the

left eye velocity appears slightly lower.

Figure 3 shows that eye velocities induced by sled

movement (TVOR) varied as a function of CLEP before

motion onset for both animals. TVOR eye velocities are

lower in response to the same translational stimulus when the

eyes are fixated on far targets as opposed to near targets, as

has been showed repeatedly in other studies (control trials,

square symbols in the figure). Viewing distance dependence

of the TVOR is seen for sled motion in either direction (left or

right). In contrast, for both the right (Fig. 3a) and left eyes

(Fig. 3b), the microstimulation-induced passive eye dis-

placement impacted TVOR eye velocities differently

depending on the direction of the sled movement. TVOR

responses were almost independent of the passive eye dis-

placement when the left eye moved to the left during

Fig. 3 Comparison of eye

velocities between normal

TVOR responses (control trials,

squares and dotted lines) and

the responses with

microstimulation (stimulation

trials, circles and dashed lines)

for two animals. The eye

velocities plotted as a function

of the change of left eye

position (CLEP) from the near

target fixation, sled movement

rightward (upper half, black) or

leftward (lower half, gray) and

separated for the right eye

(a) and the left eye (b). Velocity

measured at 80 ms after motion

onset

Exp Brain Res (2011) 215:77–87 81

123

translation to the right and when the right eye moves to the

right during the head moving to the left (abductive eye

movement). However, there was a vergence angle (as rep-

resented by CLEP) effect in the stimulation trials seen in the

adductive TVOR for both eyes (right eye during rightward

head translation—Fig. 3a and left eye during leftward head

translation—Fig. 3b) similar to the control trials.

Because the left abducens nerve was subject to contin-

uous stimulation throughout the duration of the trials,

which potentially impacts the left eye’s response to trans-

lation artificially, we primarily concentrate our discussion

here on the responses of the right eye. The right eye

velocities in Fig. 3a were normalized by dividing the eye

velocity in each trial by the mean of the TVOR eye

velocities in the control trials with near target fixation (see

‘‘Methods’’) and were re-plotted in Fig. 4a. This figure

again shows that TVOR responses to leftward translation

did not appear to be impacted by the microstimulation-

induced CLEP (gray cycles). However, responses to

rightward head motion were modulated by microstimula-

tion-induced CLEP (black circles). The normalized data

were plotted as stimulated trials versus the predicted non-

stimulated (control trial) response at the same CLEP in

Fig. 4b. In this figure, if the TVOR responses were com-

pletely dependent on the proprioceptive information, data

points should fall along the unity slope line, meaning that

eye velocity is dependent on the actual CLEP. If the TVOR

were completely independent of proprioceptive feedback in

these experiments, data points should fall along a hori-

zontal line, ideally intercepting the ordinate at 1. Our

results show that when the head moved to the left, right eye

data from both monkeys fell along a line parallel or close to

parallel to the horizontal axis (gray circles). However,

when the head moved in the opposite direction, data points

fell along a line with a slope between 0 and 1 (black cir-

cles), a result that reflects the influence of proprioceptive

feedback. When these analyses were repeated for eye

velocity taken at different times after motion onset, results

were similar (factorial regression analysis, P [ 0.05) and

results have been summarized in Fig. 5, which plots slopes

of regression lines (±95% confidence intervals) computed

from eye velocity at 65, 70, 75, 80, 85, 90, 95, and 100 ms

after motion onset. In the figure, slopes for the abductive

movement are around zero, but for the adductive move-

ment shift toward 1. Significant differences were seen

between movements in these two directions (factorial

regression analysis, P \ 0.05).

Similar results were obtained if the motion was delayed

70 ms or 170 ms rather than 120 ms after microstimulation

applied (see Fig. 6a for example). Results summarized in

Fig. 4 a Normalized velocities

of right eye for both animals.

Eye velocities plotted as a

function of the change of left

eye position (CLEP) relative to

the near target fixation. Plotted

for both subjects moving

rightward (black) and leftward

(gray). Control trials—squaresand dotted lines; from

microstimulation trials—circlesand dashed lines. b Re-plotted

right eye velocity for

stimulation trials versus control

(expected) eye velocity for the

CLEP at the point in time.

Dotted lines indicate

proprioceptive prediction. Eye

velocity measured at 80 ms

after motion onset

82 Exp Brain Res (2011) 215:77–87

123

Fig. 6b are slopes of regression lines for the right eye

computed similar to those in Fig. 5. Data were collected at

80 ms after motion onset. For all three motion delays,

abductive movements are all independent of the CLEP

(slopes close to zero) and the adductive movements are

partially affected by the passive eye displacement. Despite

some variation observed among the slopes of the adductive

components, we did not find systematic change and sig-

nificant difference among motion delays (factorial regres-

sion analysis, P [ 0.05) in both animals.

Fig. 5 Regression slopes

(±95% confidence intervals) for

the right eye for plots like 4b,

but taken at different times

(65–100 ms) after onset of sled

motion. Data are plotted

separately for subject moving

leftward (gray) and rightward

(black)

Fig. 6 Comparison of eye

movement responses to

different motion delays.

a Samples of left and right eye

velocity (mean ± SD), aligned

at motion onset (motion

delays = 70, 120, 170 ms)

during fixation of a target at

12 cm. Top panel no

stimulation; lower paneldemonstrates microstimulation

trials. Thin horizontal dashedlines—zero velocity. Thindotted curve—average sled

acceleration. Data from M1

during translation to the right

and 2.0 times threshold

stimulation. b Regression slopes

(±95% confidence intervals) as

in Fig. 5 plotted as a function of

motion onset delay (right eye,

80 ms after motion onset)

Exp Brain Res (2011) 215:77–87 83

123

Discussion

Abducting one eye involuntarily with microstimulation of

the abducens nerve while moving the animal laterally, we

found differences between the TVOR responses when the

animal was moved rightward versus leftward. Abductive

eye movement responses to interaural translation were not

affected by the passive, stimulation-induced eye displace-

ment, which supports the widely accepted hypothesis that

corollary discharge plays a dominant role in TVOR mod-

ulation. However, adductive movement consistently chan-

ged as a function of the passive displacement of left eye

position. This result provides evidence that proprioceptive

information may contribute to TVOR responses and sug-

gests that proprioceptive feedback may influence responses

of medial rectus motor neurons during translation motion.

TVOR modulation depends on both viewing distance

and viewing direction. While eye position may determine

viewing direction, it is still unclear how viewing distance is

calculated centrally. Sensory visual cues may contribute to

the estimation of viewing distance in perception (e.g.,

Rogers and Bradshaw 1993; Predebon 1993; Gibson 1950;

Glennerster et al. 1998). However, vergence angle seems

more likely to play a role in determining viewing distance

used by VOR mechanisms as TVOR responses appear to be

proportional to VA (Angelaki 2004; Angelaki and Hess

2001; McHenry and Angelaki 2000; Paige 1991; Paige and

Tomko 1991b; Schwarz and Miles 1991; Wei et al. 2003).

Vergence changes made when voluntarily changing fixa-

tion from near and far targets induce dramatic changes in

the TVOR. Motor commands from the midbrain or cere-

bellum may serve as original signals in the TVOR modu-

lation as abundant vergence neurons were found in these

areas and the short latency of the reflex argues against

higher levels of control (Judge and Cumming 1986; Mays

1984; Nitta et al. 2008; Zhang et al. 1992).

The current experiment and previous reports (Angelaki

and McHenry 1999; Paige and Tomko 1991b for example)

show that each eye responds to the same translational

motion with different velocity amplitudes (see example in

Fig. 2a). This is because despite being at the same VA,

each eye starts at a different viewing direction in the orbit.

As vergence angle appears to be a factor in scaling the

TVOR responses (Angelaki 2004; Paige 1991; Schwarz

and Miles 1991), the geometry of visual stabilization still

requires that each eye be modulated based upon its indi-

vidual position relative to the target (Angelaki and Hess

2001; Hess and Angelaki 2003; Virre et al.1986).

With microstimulation, the ‘‘target position’’ and, thus,

the vergence angle were changed when the left eye position

was altered, so we made comparisons between the control

and microstimulation trials based on vergence angle (as

measured by CLEP) since exactly matching both vergence

angle and target position in the two tasks would be very

difficult. In the vast majority of stimulation trials, the left

eye position did not cross the straight ahead position (zero

angle) from an initial position of 6 to 7� to the right as

required to fixate the 12 cm target. Geometrically, with our

experimental protocol (5 cm translation in either direction),

there is less than a 5% difference in the required angular

excursion of either eye to stay on a target at a vergence

angle of 7� when the target is straight ahead (between the

eyes) compared with a target aligned with the left eye. Thus,

we feel our comparison of the control to microstimulation

trials as we have done is an acceptable approximation.

We have considered the possibility that our paradigm

might influence corollary discharge representations of eye

position. Many of the vestibular nucleus and nucleus pre-

positus hypoglossi neurons believed to be involved in

corollary discharge mechanisms influence bilateral eye

movements. Microstimulation of the abducens nerve did

not elicit movement of the contralateral eye but abducted

the ipsilateral eye, suggesting that the only effect was on

the ipsilateral lateral rectus muscle. However, it is still

conceivable that co-contraction of the right medial and

lateral rectus might occur with brainstem stimulation in a

way that does not result in right eye movement, but

influences the movement of the eye in response to trans-

lation. This possibility cannot be completely dismissed

without addition experiments, such as recording from the

right abducens or oculomotor nucleus or nerve during left

abducens stimulation.

While we discuss the abducens nerve stimulation as a

mechanism merely to move the eye laterally, consideration

must be given to the physiology of the nerve. King et al.

(1994; Zhou and King 1998) noted that some abducens’s

fibers modulate with movement of the contralateral eye.

However, these fibers still innervate the ipsilateral lateral

rectus, so their correlation with contralateral eye’s move-

ments during bilateral eye movement may be irrelevant for

the current experiments. Additionally, abducens fibers may

innervate either twitch or non-twitch muscle fibers. The

non-twitch fibers would be those expected to provide

sensory feedback (Buttner-Ennever and Horn 2002). Our

assumption is that both twitch and non-twitch fibers are

stimulated in our protocol. Since we found an influence of

left abducens stimulation on right eye response, the idea

that we effectively stimulated the non-twitch fibers is

supported by the finding of a proprioceptive effect. Alter-

natively, we might somehow be directly stimulating sen-

sory fibers. However, though sensory fibers have been

reported to travel in motor nerves to the extraocular mus-

cles (Gentle and Ruskell 1997), these fibers are believed to

cross over from the ophthalmic division of the Vth cranial

nerve and would not be stimulated by our protocol, where

the stimulation electrode is in the brain, just 2 mm anterior

84 Exp Brain Res (2011) 215:77–87

123

to the abducens nucleus. While not directly demonstrated,

our assumption that microstimulation contracted the lateral

rectus muscle influencing proprioceptive feedback without

influencing central oculomotor command signals is at least

the most parsimonious explanation.

Anatomically, palisade endings are thought to provide

proprioceptive information to the brain from extraocular

muscles (Buttner-Ennever and Horn 2002; Donaldson 2000;

Eberhorn et al. 2005; Ruskell 1999). These endings are

exclusive to extraocular muscles and associated with non-

twitch fibers (Buttner-Ennever and Horn 2002; Niechwiej-

Szwedo et al. 2006). The role of orbital proprioception in

eye movement control is still uncertain (see Ruskell 1999;

Donaldson 2000 for reviews). To date, proprioceptive

feedback has not been thought to be directly involved in eye

movement control (Sommer and Wurtz 2008). During rapid

eye movement, corollary discharge provides enough eye

position information to control saccadic eye movements

(Guthrie et al. 1983; Keller and Robinson 1971; Sommer

and Wurtz 2008) and perturbation of eye position by

stimulation of ocular motoneurons during saccades does not

influence the subsequent eye movement (Schiller and San-

dell 1983; Sparks and Mays 1983; Sparks et al. 1987).

However, accumulated evidence supports that propriocep-

tive information is important at least for a long-term cali-

bration of corollary discharge, perception of target location,

and eye position (Balslev and Miall 2008; Gauthier et al.

1990; Lewis et al. 1994; Skavenski 1972; Wang et al. 2007;

Zhang et al. 2008; Steinbach and Smith 1981; Steinbach

1987; Weir et al. 2000). Removal of proprioceptive input in

rabbits compromised RVOR responses (Kashii et al. 1989)

as did perturbation of eye position by external force to the

eye in pigeons (Knox and Donaldson 1993). However,

deafferentation of the orbits in macaques did not influence

ocular alignment or oculomotor function during saccades,

pursuit, or RVOR in the dark (Lewis et al. 2001). The

authors of the study concluded that proprioception’s role in

oculomotor control is probably limited to long-term cali-

bration of the efference copy of eye movement signals in the

brain. While we did see effects of proprioception on the

TVOR, it is possible that the delay used in this study is not

long enough to allow us to observe the full influence of

proprioception. However, our technique is limited by the

time that a monkey can maintain fixation in the dark. Fur-

ther investigation would be needed to discover longer

latency proprioceptive effects on TVOR modulation.

Our results are consistent with having more than one

pathway responsible for scaling eye movement responses

in the TVOR and having one of those pathways involve

proprioceptive feedback to the oculomotor nucleus. An

anatomical substrate for such feedback has been speculated

upon in the literature. King and Zhou (2000) proposed that

the central nervous system may encode monocular

movement commands independently and that binocular

coordination may be achieved through a network including

abducens internuclear neurons to control the responses of

medial rectus motor neurons of the contralateral eye for

conjugate eye movements and near response neurons in the

mesencephalon to control medial rectus motor neurons for

vergence eye movements. Buttner-Ennever and Horn

(2002) added that the proprioceptive system may also

participate in the binocular coordination adjustment pro-

posed by King and Zhou (2000). Centrally, they hypothe-

size that proprioceptive fibers innervate the spinal

trigeminal nucleus, the superior colliculus, and the central

mesencephalic reticular formation where the near response

cells, which express an internal representation of vergence

angle, reside (Mays 1984; Buttner-Ennever et al. 2002).

Non-twitch motor neurons have been shown to receive

inputs from areas involved with neural integration, ver-

gence, and smooth pursuit (Buttner-Ennever et al. 2002;

Wasicky et al. 2004), including the near response regions

in the pretectum and parvocellular regions of the vestibular

nuclei (Buttner-Ennever et al. 2002). Representative areas

of proprioceptive input from the eye plant have been

revealed in cortex (Balslev and Miall 2008; Wang et al.

2007). In theory, therefore, the proprioceptive effects on

adductive TVOR gain scaling that we observed in these

experiments might be mediated through near response cells

in the central mesencephalic reticular formation projecting

to medial rectus motor neurons. However, despite the

appeal of such a pathway to account for our data, there is

no direct evidence to illustrate such a proprioceptive

feedback loop yet. While our data show a dominant

influence of corollary discharge but a significant influence

of proprioception as well on TVOR scaling, the mechanism

of influence of each is speculative at this time.

Acknowledgments We thank Dr. W. Michael King for valuable

comments on this manuscript and Rong Chu for his technical assis-

tance in the experiment. The work was supported by NIH grants R01

DC006429 (to S.D.N.).

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Does orbital proprioception contribute to gaze stability during translation?

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