Current Eye Research
Volume 9 number 3 1990
The influence of alpha-adrenergic agents on tonic accommodation
Mark Rosenfield, Bernard Gilmartin', Elizabeth Cunningham' and Nutan Dattani'
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Schnurmacher Institute for Vision Research, SUNY/State College o f Optometry, 100, East 24th Street, New York, NY ' 10010, USA and 'Department of Vision Sciences, Aston University, Aston Triangle, Birmingham B4 7ET, UK
ABSTRACT This study has examined the effect of an alpha-1 adrenergic agonist (phenylephrineHCI, 2.5%) and a non-selective alpha antagonist (thymoxamine HCI, 0.5%) on tonic accommodation (TA). TA was measured at 1 min intervals throughout a 45 min period using an objective infra-red optometer (Canon Autoref R-1). Additionally pupil diameter and the near-point of accommodation(NPA) were monitored in order to assess the efficacy of the instilled drug. A double-blindprotocol was adopted between thymoxamine, phenylephrine and a saline control for 7 emmetropic subjects. There was no significant difference between the values of TA obtained under the three pharmacologicalconditions. However, both adrenergic agents induced changes in pupil diameter and NPA. Furthermore in all conditions TA increased by approximately 0.25D while the subject sat passively in darkness. The data indicates that alpha-adrenergic innervation alters the closed-loop accommodative response independently of TA.
receptors(7-9),predominantly of the beta-2 sub-group (10-12). However the alpha-adrenergicinnervationto the ciliary body may also be responsible for some variation in the accommodative response. Morgan (2), Fleming and Hall (13) and Chin et al. (14) suggested that increased alpha-innervationaltone to the ciliary vasculature would produce peripheral vasoconstriction, leading to a reduction in ciliary body volume with consequent alteration of the crystalline lens curvature. However, a recent investigation by Zetterstrdm and Hahnenberger (12) examined the effect of topical adrenergic agents on strips of human ciliary muscle in vitro. They demonstratedthat phenylephrine (an alpha-1 agonist) produced a relaxation of the ciliary muscle in 3 out of the 8 eyes examined. Since these responses were demonstrated in the absence of the muscle vascular
INTRODUCTION There is substantial support for the proposal that the ciliary muscle
system, ZetterstrOm and Hahnenberger concluded that the adrenergic responses were produced by direct action on the ciliary
receives a dual autonomic innervational supply, i.e. from both
muscle rather than being due to an indirect effect on the ciliary
Parasympathetic and sympathetic nervous systems (1). Whilst the
vasculature.
precise role of sympathetic innervation in the control of accommodation is unclear, it would appear to play a relatively minor
Several in-vivo investigations (15-20) have also demonstrated the eflect of topical alpha-adrenergic agents on the accommodative
role in a rapidly changing visual environment. Evidencefor this
response. They have demonstrated that instillationof phenylephrine
proposal may be drawn from observations on the time course and
will induce a reduction in the dioptric value of the near-point of
amplitude of the sympathetically-mediatedresponse. Morgan (2)
accommodation (NPA). Additionally, Leibowitz and Owens (21) and
reported that in cats, parasympatheticstimulation produced a diptric
Garner et al. (22) examined the effect of phenylephrine on the
change 10 times greater than that induced by the equivalent degree
accommodative response in darkness. It is well establishedthat
of sympathetic stimulation. Later TOrnqvist (3) demonstrated that the
under stimulus-free conditions, accommodation adopts a relatively
maximum inhibitory response in young adult cynomlgus monkeys
stable value of around 0.50-1.50D (21,23). The term tonic
(Macaca irus) was only around 1.5D. Furthermore the temporal
accommodation (TA) has been adopted to describe this intermediate
response is relatively slow, reaching a maximum around 10-45s (3-5).
bias of accommodation (23-26). Leibowitz and Owens (21) examined
Clearly this observed time-course is too slow to contribute to the
the effect of 2 drops of 10% phenylephrine on both TA and the
rapid changes in accommodative stimulus which are encountered in
far-point of accommodation;TA being measured using a laser
the typical visual environment. In contrast, parasympathetically
optometer. They observed that for 7 subjects, phenylephrine did
mediated accommodative responses are normally completed in
not produce any Significant change in either of the parameters
approximately 1s (6).
measured. However Garner et al. (22) pointed out that in the study of
A number of studies have demonstrated that sympathetic input to the ciliary muscle is primarily mediatedvia beta-adrenergic
Leibowitz and Owens, the NPA was not assessed and therefore it was not possible to confirm that the ciliary body had been affected by
Received on November 2, 1989; accepted on January 25. 1990
0 Oxford University Press
267
Current Eye Research the drug treatment. Garner et al. recorded TA, using a laser
astigmatism not exceeding 0.50D). All subjects signed a consent
optometer, for 6 hours following the instillation of phenylephrine
form prior to taking part in the study and following a full explanation of
(loo/.) in three subjects. Additionally NPA was measured during the
all experimental procedures.
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6 hour period. They observed that phenylephrine produced a
The accommodative response was measured objectively using a
significant reduction in the near point (mean = 2.75D) in all 3
Canon Autoref R-1 infra-red optometer. This instrument was
subjects, the maximum reduction in NPA occurring approximately 60
modified so that the refractive state could be measured at 1s
mins following drug instillation. Furthermore Garner et al. observed
intervals. The optometer measures 3 meridians in 0.2s to provide
no significant change in TA in the 3 subjects examined. Their data on
sphere and cylinder powers to an accuracy of +0.12D and has been
the NPA indicated that the efficacy of phenylephrine reached a
fully described and evaluated by McBrien and Millodot (29). All
maximum during the first hour following drug instillation. However
measures of accommodationwere taken from the left eye and
during this initial 60min period only one measure of TA was taken on
readings were calculated as mean spheres (i.e. sphere + half cylinder
subject RB and no assessment of TA was made on subject BB.
power). No calibration factor has been added to the optometer
Zetterstrbm (19) used a laser optometer to examine the effect of phenylephrine (10%) and thymoxamine (0.5%) on TA. She reported
reading. The initial part of each experimental sessior?consisted of the
that the instillation of phenylephrine produced a myopic shift in TA of
measurement of pre-task TA. This was done according to the
0.90D while thymoxamine failed to induce any significant change in
method described by Gilmartin and Bullimore (30). The subject sat in
TA. Additionally Mordi et al. (27) indirectly assessed the level of TA
total darkness for a period of 10 mins in order to dissipate any
by examining the accommodation stimuluslresponse function for
transient changes in accommodation initiated prior to the start of the
their 5 subjects. TA was taken as the intersection of the
experimental session. This also served to ensure that TA had
stimuludresponse plot with the unit-ratio or 45" line. Examination of
regressed to a base-line level. After this period 50 readings of the
their data indicates that 3 of the 5 subjects demonstrated a reduction
refractive error were taken over a 5 min period. These were then
in TA of the order of 0.4D one hour following drug instillation, whilst a
averaged to give the mean value of pre-task TA.
further subject showed a shift in TA of approximately -0.6D. However
After measurement of pre-task TA, the left pupil diameter was
the findings of Tan and OLeary (28) would bring into question the
measured directly from the optometer video monitor. This provides
proposal that the intersection of the stimulus/responseplot with the
an 8x magnificationof the eye and allowed the pupil diameter to be
unit-ratio line is equivalent to the dioptric value of TA.
assessed using a calibrated rule mounted on the screen. Pupil
In view of these equivocal findings, the present study has sought
diameter could therefore be assessed to an accuracy of k O.lmm and
to examine the effect of phenylephrine, an alpha -1 adrenergic
was measured under darkroom conditions. Additionally NPA was
agonist, and thymoxamine, a non-selectivealpha antagonist, on TA
assessed using a "push-up" technique. The target consisted of a
at one minute intervals over a 45min period. The instillation of both
line of high contrast (=8O%) letters, size N5 (31) mounted on a
agonist and antagonistic agents will provide greater information
near-point rule. Target luminance was approximately 50 cd/m2. The
concerning the alpha-adrenergic effect when compared with the use
NPA was measured from the left eye under monocular conditions
of an agonist alone. Measurement of accommodationcommenced
and the mean of three readings recorded.
20 mins following drug instillation in order to encompass the period of
A double-blindprotocol was adopted between phenylephrine
maximum drug efficacy. Additionally the mydriatic effect was
hydrochloride (2.5%)*,thymoxamine hydrochloride (0.5%) and a
monitored throughout the course of the 45min interval and the NPA
saline control. Instillations of phenylephrine,thymoxamine or saline
was assessed both before and after the measurement period.
were made using a precision micropipette delivering 25yl of drug.
MATERIALS AND METHODS
Benoxinate (0.4%) in order to inhibit reflex lacrimation, each subject
Following the instillation of one drop of the topical anaesthetic A total of seven emmetropic subjects were used (4 male, 3
female), all of whom were students in the Department of Vision
was given two instillationsof drug separated by a period of 5 mins i.e. 50y1 of drug per eye. Twenty minutes following the first drug
Sciences, Aston University. All subjects were Caucasian, aged between 18 and 2lyears of age and had unaided distance visual acuity of at least 616 with either eye and a mean spherical refractive error not greater than 0.50D of myopia or hypermetropia (with
268
* Phenylephrine (2.5%), thymoxamine (0.5%), Benoxinate (0.4%) and normal saline: Smith & Nephew single dose applicators ("Minims").
Current Eye Research instillation, the subject returned to the optometer and the room lights
period. These values were averaged into 5min intervals and are
were extinguished. Following an initial 60s period, 10 readings of the
illustrated in Fig. 1. Clearly the instillation of either thymoxamine
refractive error were taken each minute for 45mins. The subject
(0.5%) or phenylephrine (2.5%) did not produce any significant
remained in darkness throughout the measurement interval.
change in TA. Two factor (drug, time) anatysis of variance was carried
Pupillary diameter was also assessed at 1min intervals over the 45min
out on the data illustrated in Fig. 1. This indicated that neither factor
period. At the end of the 45min session the assessment of NPA was
was significant (drug: F=0.04;df=2,162; p=0.96; time: F=0.89; df=
repeated. The order of the three drug trials was randomized and
8,162; p=0.58). The second order interaction was not significant.
each trial was separated by a period of at least 48hrs.
The values of pupil diameter during the course of the 45min period are illustrated in Fig. 2. Two factor (drug,time) analysis Of
RESULTS
variance indicated that the drug effect on pupillary diameter was
The mean pre-task values of TA and pupillary diameter are shown Curr Eye Res Downloaded from informahealthcare.com by University of Newcastle on 12/28/14 For personal use only.
in Table 1. One factor analysis of variance on the pre-task TA data
significant (drug: F=70.25; df=2,162; p0.05). The shift in TA, measured with respect to the pre-task level, was calculated at 1 min intervals throughout the 45min assessment
Table 1. Pre-task measures of tonic accommodation (TA) and pupil diameter. All values are recordedfrom the left eye. Figures in parentheses indicate f 1 SEM. Phenylephrine
Thymoxamine
E
1 1 1
a,
c
a,
1
I
0.41
0.77
0.76
(D)
(0.25)
(0.17)
(0.18)
Pre-task pupil
7.44
7.05
7.32
diameter (mm)
(0.42)
(0.46)
(0.33)
5
15
25
35
45
Time (mins)
Fig. 2. Mean values of pupil diameter for the three drug conditions during a 45 minute period in darkness. The measurementperiod commenced 20 mins following the first drug instillation. Error bars represent f1 SEM.
1
1
Phenylephrine
G
1
c
//
.6-.
'
U
E
- 0 . 25
Thymoxamine
Saline
Pre-task TA
+ 0.50
-E
I,
5 2 0
15
25
35
45
-
.-
z
a Time (mins)
Post-task
8 6
4
U a, + .
5
Pre-task
10
2 0
PHENYLEPHRINE THYMOXAMINE
Fig. 1. Mean dioptric shift in tonic accommodation(TA), measured with respect to the pre-task level, for the three drug conditions during a 45 minute period in darkness. The measurement period commenced 2Omins following the first drug instillation. Error bars have been omitted for clarity but SEMs for the phenylephrine, thymoxamine and saline conditions were of the order of 0.15, 0.1 1 and 0.23 respectively.
SALINE
Experimental condition
Fig. 3. Mean pre- and post-task values of amplitude of accommodation. These responses were taken from the left eye under monocular conditions using a "push-up" technique. Error bars represent f l SEM.
269
Current Eye Research for the 3 drug conditions are illustrated in Fig. 3. One factor analysis
her findings and those of Leibowitz and Owens (21) and Garner et a\.
of variance indicated that the drug effect on the amplitude of
(22). However Zetterstrdm and Hahnenberger(12) also reported
accommodation was significant ( F = l I .37; df=2,18; p~0.01).
considerable individual variation in the effect of alpha-adrenergic agents on the ciliary muscle.
DISCUSSION
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Instillationof an alpha-1 adrenergic agonist (phenylephrine, 2.5%)
The present study has demonstrated that alpha-I adrenergic innervation to the ciliary body produced a significant change in the
or non-selectivealpha antagonist (thymoxamine, 0.5%) does not
amplitude of accommodation. Since a subjective "push-up"
produce a significant change in TA. This supports the findings of
technique was used to assess the accommodative amplitude, the
Leibowitz and Owens (21) and Garner et al. (22) and represents an
precision of these measurements may have been attenuated at
important observation since a number of recent studies concerning
higher levels of accommodative response due to the non-linearity of
ocular accommodation have used phenylephrine (2.5%) to produce
the dioptric scale. However the observation of a reduced NPA
pupillary mydriasis (32-34).
following the instillation of phenylephrine is consistent with previous
The differences between the findings of the present study and
reports (16-19). Furthermore Mordi et al. (27) observed that the
those of Zetterstrbm (19) may relate to methodologicaldifferences in
instillation of 10% phenylephrine produced a reduction in the
the assessment of TA. Zetterstrbm used a laser optometer to
gradient of the accommodative stimulus/responsefunction. Pupillary
measure accommodationand reported that the instillationof
mydriasis cannot account for this change since the increased
phenylephrine (1Ooh) produced a mean dioptric increase (N=10) in
pupillary diameter, with concurrent reduction in depth-of-focus,
TA of +0.9D. However, a number of studies have indicated that the
would induce a steeper stimulus-responsegradient. However at the
technique associated with the operation of the laser optometer may
higher dioptric levels stimulated during either the determination of
itself influence the recorded value of TA (35-38). Both the mental
accommodative amplitude or the stimulushesponsefunction, the
effort required to judge the direction of laser speckle motion and the
increased magnitude of parasympathetically-mediated
proximal stimulus resulting from awareness of nearness of the
accommodationwill facilitate sympathetic outflow, and consequently
speckles may induce changes in the accommodative response.
the instillation of adrenergic zgents is more likely to produce a
Further evidence for this proposal comes from the investigations of
significant effect.
Gilmartin et al. (23) who reported that timolol maleate (0.5%),a
It may be observed from the data illustrated in Fig. 1 that the mean
non-selective beta-adrenergic antagonist, produced an average
value of TA increased while subjects sat passively in darkness. A
myopic shift in TA of +0.85D under darkroom conditions when
number of other studies have also reported an increase in TA under
measured with a laser optometer. However in a later study using an
sustained stimulus-free conditions (40-42). This passive drift in TA
objective, open-field, infra-red optometer, Gilmartin and Bullimore
may be analogous to the change in heterophoriawhich occurs during
(30) observed that timolol failed to produce any significant change in
prolonged monocular occlusion (43). This observation is important
TA under darkroom conditions. They noted the findings of Tdrnqvist
with regard to studies of accommodative hysteresis (44) i.e. the shifl
(3,4) that the magnitude o! sympathetic innervation to
in TA which may be observed immediately following a period of
accommodationwas related to the level of concurrent
sustained fixation. The passive drift of TA may mask the regression
parasympatheticactivity. Under truly stimulus-freeconditions, the
of task-induced accom,mdative hysteresis. Thus when investigating
degree of parasympathetic innervationwill be minimized and thus no
task-induced effects on TA, the duration of the post-task period
sympathetic effect will become manifest. However the operation of
should be kept to a minimum in order to reduce the contaminating
the laser optorneter may itself stimulate a parasympathetically
effect of this passive drift in the accommodativeresponse.
mediated accrrmmodative response and thereby initiate sympathetic
A further consideratbn relates to the role of TA within the
activity. Furthermorethe laser speckle exposure duration adopted
closed-loop accommbdativeresponse. This study has demonstrated
by ZetterstrOm (750ms) was longer than that used in the studies of
that alpha-adrenergic agents will alter the closed-bop response
Leibowitz and Owens (21) and Garner et al. (22). In the latter two
independent of any change in TA. One implication which may be
investigations,the laser speckles were presented for only 500ms.
drawn from this finding is that the contributionof TA to the aggregate
Hogan and Gilmartin (39) noted that the average accommodative
reponse is small. Such an observation is supported by the model of
response time was 358ms. The longer speckle presentation time
accommodation proposed by Hung et al. (45). They noted that TA
adopted by Zetterstrdm (750ms) may explain the daference between
(referred to in their paper as ABIAS) would produce a constant
270
Current Eye Research biasing or offsetting of the accommodationstimulus-responsecurve. However it may be demonstratedfrom their equations that marked changes in the value of TA produce very small variation in the closed-loop accommodative response. Using equation #2 from the study of Hung et al., if the accommodative stimulus (AS)=3D, accommodative controller gain (ACG)=8 (46) and the dead space of accommodation (DSP)=0.5D, then a change in TA (ABIAS) from 1 to 3D will result in a change in accommodative response from 2.33D to 2.56D respectively, i.e. a shift of only 0.22D. Furthermore Ciuffreda
et al. (26) demonstratedthat in amblyopic eyes the accommodation stimulus-responsefunction was different from that observed in Curr Eye Res Downloaded from informahealthcare.com by University of Newcastle on 12/28/14 For personal use only.
normal eyes although the values of TA (ABIAS) were similar. This would confirm the observation that the contribution of TA to the closed-loop accommodative response is small. ACKNOWLEDGEMENT This study was conducted as part of the final year Optometry course in the Department of Vision Sciences, Aston University, Birmingham, U.K. CORRESPONDING AUTHOR Mark Rosenfield Ph.D., Schnurmacher Institute for Vision Research, SUNY/State College of Optometry, 100 East 24th Street, New York, New York 10010.
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