Proximally Induced Accommodation and Accommodative Adaptation
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1 Investigative Ophthalmology & Visual Science, Vol. 31, No. 6, June 1990 Copyright Association for Research in Vision and Ophthalmology Proximally Induced Accommodation and Accommodative Adaptation Mark Rosenfield, Kenneth J. Guffreda, Editha Ong, and Abbas Azimi To determine the effect of proximally induced accommodation (PIA) on accommodative adaptation, this study has examined the posttask shift in tonic accommodation (TA) following 5-min monocular viewing of equivalent-sized targets located at distances of 0.33 and 5 m. The distal target was viewed through a negative lens to equate the dioptric stimuli (3 D). The steady-state accommodative response was measured subjectively in 10 subjects using a Hartinger coincidence optometer. A significant correlation was observed between the degree of adaptation following the two conditions, with the magnitude of adaptation for the distal target being approximately half that for the nearer target. Furthermore, adaptation magnitude was inversely correlated with pretask TA under both conditions. These results indicate that PIA can produce accommodative adaptation. The implications of this finding are discussed with regard to models of the accommodative mechanism. Invest Ophthalmol Vis Sci 31: ,1990 Maddox 1 proposed that the total vergence response was composed of four independent components namely, tonic vergence, accommodative vergence, convergence due to knowledge of nearness (now termed proximal vergence), and fusional vergence. The aggregate accommodative response also may contain a proximal element, ie accommodation resulting from knowledge of nearness of the object of regard. 2 " 5 However, it remains unclear whether target proximity acts directly as a stimulus to both accommodation and vergence, or directly stimulates only one component of the oculomotor response, with the response of the other element resulting from the action of the oculomotor crosslinks ie, either accommodative convergence or convergent accommodation. Accordingly, the current study has adopted the term proximally induced accommodation (PIA) to describe that change in accommodative response resulting from the psychic awareness of nearness. Recent research has indicated that the potential contribution of proximal factors to the aggregate accommodative and vergence responses may be substantial. Rosenfield and Gilmartin 5 demonstrated that with both accommodation and vergence under open-loop conditions, a change in target distance from 0.2 D (5 m) to 3.0 D (0.33 m) produced an From the Schnurmacher Institute for Vision Research, Department of Vision Sciences, SUNY/State College of Optometry, New York, New York. Submitted for publication: June 23, 1989; accepted October 24, Reprint requests: Mark Rosenfield, PhD, SUNY/State College of Optometry, 100 East 24th Street, New York, NY initial mean change in accommodative response for 10 emmetropic subjects of +1.7 D. This would represent a PIA/accommodative stimulus (AS) ratio of 0.60 D/D. Furthermore, Hokoda and Ciuffreda 4 suggested that proximal vergence could contribute up to 50% of the total vergence response under open-loop conditions, while Wick 6 noted that in some subjects the output of proximal vergence could exceed that of accommodative vergence. In view of these open-loop findings, one might conjecture that proximal awareness has the capability to generate a substantial proportion of the closed-loop oculomotor response. A number of workers have designed control models of accommodation/vergence interaction in an attempt to gain greater understanding of the interrelationships between the various inputs to accommodation and vergence. 7 "" However, few of these models have included a proximal input to each oculomotor system. Toates 12 did indicate a proximal input to vergence, but this was within an isolated model of vergence and did not provide any quantitative information. Later, Ebenholtz and Fisher 9 proposed a model of accommodation-vergence interactions which included a "distance operator," the latter referring to that component which determines relative distance perception from the steady-state levels of accommodation and vergence. However, this distance operator was designed to extract information from the oculomotor responses per se, and is not analogous to the perceptually derived proximal information to accommodation and vergence. Wick 6 did include a proximal component in his model of the vergence mechanism. He indicated that the proximal vergence input would be located prior to both 1162
2 No. 6 PROXIMALLY INDUCED ACCOMMODATION / Rosenfield er ol 1160 the convergent accommodation crosslink and the slow or adaptive vergence mechanism. 13 Therefore, his model would be consistent with the notion that proximal vergence can indeed stimulate vergence adaptation. However, Wick's model 6 provided little information relating to the accommodative mechanism, and did not indicate the relationship between PIA and accommodative adaptation. The current study has attempted to provide information relating to the position of PIA within models of accommodation-vergence interactions by examining the effect of PIA on accommodative adaptation. It is well established that under stimulus-free conditions, accommodation adopts a relatively stable value of around D. 14 " 16 In this study, the term tonic accommodation 1718 (TA) has been adopted to describe this intermediate bias of accommodation. Several studies have demonstrated that the level of TA may be modified by exogenous stimuli such as a sustained near-vision task, 19 " 24 the term accommodative adaptation being used to describe this posttask shift in TA. 24 " 27 Determination of the relationship between PIA and accommodative adaptation may also clarify the interaction between PIA and the other accommodative components, eg, convergent and blur-driven accommodation, within the combined closed-loop response. A previous investigation 24 demonstrated that an increase in disparity vergence under closed-loop conditions produced a mean reduction in accommodative adaptation for emraetropic subjects. It was suggested that the increase in disparity-induced accommodation, ie, accommodation driven by vergence under closed-loop conditions, would be accompanied by a reduction in blurdriven accommodation, in order to maintain the overall accommodative response. The decreased accommodative adaptation may then have resulted from this reduction in the output of blur-driven accommodation. This result was consistent with the investigation of Kran and Ciuffreda, 28 who reported that an increase in blur-driven accommodation under closed-loop viewing produced a reduction in vergence adaptation. These findings would indicate that the primary stimulus to accommodative and vergence adaptation is derived from blur-driven accommodation and disparity vergence respectively, rather than from the output of the appropriate oculomotor crosslink. Two subsequent investigations 26 ' 29 examined accommodative adaptation under both monocular and binocular viewing conditions. It would be predicted that under binocular viewing, the output of convergent accommodation would reduce the requirement for blur-driven accommodation with respect to monocular fixation. Thus, if the amplitude of accommodative adaptation reflects the output of blur-driven accommodation, one would predict reduced adaptation after binocular viewing, when compared with monocular conditions. However, both studies reported no significant difference in accommodative adaptation after monocular or binocular viewing. The apparent discrepancy that exists between the two sets of findings ' 29 described above may be accounted for by the output of PIA. Both Ogle and Martens 30 and Wick 6 noted that the value of the proximal convergence/accommodation (PC/A) ratio differed depending on whether the heterophoria was measured under conditions of total dissociation (Maddox rod technique) or partial dissociation (fixation disparity method). In both studies, the PC/A ratio was more than 50% larger for partial dissociation, with respect to the total dissociation technique. Ogle and Martens 30 suggested that the larger (binocular) field of view provided by the fixation disparity method may enhance the stimulus for psychic awareness of distance. Thus, the suspension of binocular vision may alter the proximal input to accommodation and vergence. Under monocular viewing, one would predict increased blur-driven accommodation (due to the decreased level of convergent accommodation) and decreased PIA. If PIA does in fact stimulate accommodative adaptation, then the changes in blur-driven and PIA under monocular and binocular conditions may cancel each other out, resulting in similar levels of adaptation. Clearly, it is important to determine whether PIA induces accommodative adaptation. Kran and Ciuffreda 28 demonstrated that proximal vergence initiated vergence adaptation. Adaptation was induced by subjects viewing a 4D, 4-m angle (MA) target either in free space or within a synoptophore. The latter condition would provide enhanced proximal stimulation while maintaining the same disparity and blurstimulus levels. The magnitude of vergence adaptation was significantly increased when viewing the synoptophore targets, presumably due to the increased proximal innervation. 31 The current study examined the influence of PIA on accommodative adaptation by comparing the task-induced shift in TA after sustained fixation of targets having differing proximal stimulus levels but similar dioptric values. Materials and Methods Accommodative adaptation was examined in ten visually normal subjects (five male, five female) having a mean age of 28.1 yr (SD = 4.0; range = yr). All subjects had corrected visual acuity of at least 6/6 (20/20). The mean spherical equivalent refractive error was 1.4 D (SD = 2.1). Informed consent was
3 1164 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / June 1990 Vol. 31 obtained from each subject prior to the commencement of the experimental session and after a full explanation of all experimental procedures. The experimental apparatus is illustrated in Figure 1. The steady-state accommodative response was measured subjectively from the right eye using a Hartinger coincidence optometer (Seilor, St. Louis, MO). 32 ' 33 The left eye was fully occluded throughout the experimental session. The optometer target consisted of two sets of three dimly illuminated, vertically oriented bars, with the vertical and horizontal angular subtense of these bars being 1.6 and 0.8, respectively. The Scheiner principle 34 was used to provide the subject with two vertically displaced images of the optometer bars. Since the exit pupil of the optometer was approximately 1 mm in diameter, the vernier target was effectively viewed open-loop, and therefore did not provide a blur stimulus to accommodation. For a full description of this instrument see Henson. 35 The initial part of the experimental session consisted of the measurement of TA. The subject sat in total darkness for a period of 5 min to allow the dissipation of transient changes in accommodation prior to the commencement of the experimental session. 36 ' 37 After this period, six measurements of the accommodative response were taken with the Hartinger optometer. The operator adjusted the relative position of the optometer vernier target until the subject indicated precise alignment by means of a hand-held clicker. Only the optometer target was visible to the subject during this procedure. These six measurements then were averaged to give the mean value of pretaskta. Following the assessment of pretask TA, subjects were required to view a 5 X 5 matrix of high contrast Far target (~80%) Snellen letters at a viewing distance of either 5 or 0.33 m. Each letter subtended 15' arc with an interletter separation of 5'. The far target was viewed through a -4.00DS lens located 10 cm from the eye. Thus, the resulting dioptric stimulus of the far target was 2.96 D, dioptrically equivalent to the near target (3 D). The actual size of the letters used for the far target were adjusted to subtend an equal angle to the near target, with compensation being made for the magnification of the -4.00D lens. In both conditions, the target was illuminated by a tungsten filament lamp, which provided a target luminance of approximately 50 cd/m 2. To provide information regarding the physical location of the target, and thereby to obtain the optimal PIA response, subjects were shown the actual location of the individual target being used for that trial, prior to the start of the experimental session. Subjects were required initially to fixate a particular letter selected by the experimental operator for a period of 60 sec. The optometer target then was superimposed over the letter matrix, immediately adjacent to thefixatedletter, and six measurements of the within-task accommodative response were recorded. After completion of these measurements, which took approximately 60 sec, the optometer target was extinguished, and subjects were required to view the letter matrix continuously for an additional 3-min period. The subjects were instructed to keep the letters "sharply focused" at all times, and to report if the letters blurred at any time during the experimental session. Immediately after the completion of this 5-min fixation period, target illumination was extinguished, and six measurements of posttask TA were recorded. The recording of posttask TA took approximately 60 sec to complete. The order of the two experimental sessions (near or far fixation target) was counterbalanced, and each session was separated by a period of at least 24 hr. Occluder Hartinger optometer -4.00D lens Near target Fig. 1. The experimental apparatus. The subject viewed the target with his right eye (RE) through a partial-reflection mirror (PRM). The solid lines refer to the near-target (0.33 m) condition, and the dashed lines refer to the far (5.0-m) target condition; the far target was viewed through a 4.00D lens to equate the dioptric stimuli of the two targets. The left eye (LE) was fully occluded. FRM, fully reflecting mirror. Results All measurements of accommodation were referenced to the eye's principal plane, with appropriate compensation for the dioptric power of any spectacle correction, to yield values of ocular accommodation. 34 The mean value of pretask TA for the far and near conditions was 1.74 (SEM = 0.23) and 1.66 D (SEM = 0.25) respectively. A paired t-test indicated that this difference was not significant (t = 0.61; df = 9; P = 0.56). This value was similar to other measurements of TA recorded with a Hartinger coincidence optometer. 23 ' 29 The mean values of accommodative response during the far and nearfixationstasks were 2.79 (SEM = 0.11) and 2.96 D (SEM = 0.13),
4 No. 6 PROXIMALLY INDUCED ACCOMMODATION / Rosenfield er ol 1165 respectively. Again, this difference was not statistically significant (t = 1.00; df = 9; P = 0.33). Furthermore, there was no correlation between the distance and near, within-task, accommodative responses (r = 0.17;df=9;i> = 0.64). The mean values of pre- and posttask TA for the distance and near adapting conditions are illustrated in Figure 2. The mean values of posttask TA for the distance and near conditions were 1.91 (SEM = 0.17) and 1.92 D (SEM = 0.22) respectively. The mean posttask shifts in TA (distance = D; near = D) illustrated in Figure 2 were not significant (distance: t = 0.92; df = 9; P = 0.38; near: t = 0.88; df = 9; P = 0.40). Furthermore, no significant correlation was demonstrated between subject's refractive error and either pretask TA (distance, r = 0.07; near, r = 0.21) or the degree of accommodative adaptation (distance, r = 0.06; near, r = 0.02), respectively. A comparison of the individual subject shifts in TA after the distance-adapting condition with that observed after completion of the near task is illustrated in Figure 3. A significant (P = 0.01) correlation existed between the degree of adaptation for the two conditions. The slope of the regression line was 0.47, indicating that the magnitude of distance adaptation was approximately half of that observed after the near task. Additionally, a correlation was found between the degree of accommodative adaptation and the level of pretask TA (Fig. 4). This was significant for both the distance (r = 0.67; df = 9; P = 0.03) and near (r = 0.65; df = 9; P = 0.04) conditions. Discussion During monocular fixation of the distant target, it is likely that the primary stimulus to accommodation resulted from target blur. However, when viewing the >^ i i i i i Near adaptation (D) >^ r-0.75; df-9; p-0.01 Fig. 3. Relation between the degree of adaptation observed after the distance- and near-adapting conditions, respectively. The equation of the regression line was y = 0.47x near target, the response was produced probably by a combination of blur-driven and proximally induced accommodation. There was no significant difference in magnitude of the within-task accommodative response between the distance and near conditions. This would imply that the value of blur-induced accommodation is greater at distance than at near. However, the degree of accommodative adaptation after the near task was approximately twice that observed after the distance task (Fig. 3). If adaptation were stimulated by the output of blur-driven accommodation alone, one would predict greater adaptation at distance than at near. Alternatively, if the degree of adaptation is related to the magnitude of the aggregate accommodative response, one would predict equivalent degrees of adaptation after the distance and near tasks. The fact that adaptation was greater at near suggests that PIA may indeed act as a stimulus to accommodative adaptation. Therefore, in (N=10) Q Pre-task TA Post-task TA DISTANCE Adapting condition NEAR Fig. 2. Mean values of pre- and posttask TA for the near and far adapting conditions. Error bars indicate 1 SEM. Pre-task TA (D) Fig. 4. Relation between the value of pretask TA and the degree of adaptation observed after the distance- and near-adapting conditions, respectively. The equations of the regression lines for the distance and near conditions were y = x and y = x, respectively.
5 1166 INVESTIGATIVE OPHTHALMOLOGY & VISUAL SCIENCE / June 1990 Vol. 31 control models of the accommodative mechanism, the input of PIA should occur prior to the adaptation loop. The observation that the magnitude of adaptation at near is twice that observed after the distance condition implies that PIA may play a major role in the process of accommodative adaptation. A number of studies 19 " 27 have demonstrated an increase in TA after a sustained closed-loop, near-vision task. Under such conditions, both blur-driven accommodation and PIA can initiate adaptation. However, in investigations of accommodative adaptation after distance fixation, conflicting results have been obtained. For example Ebenholtz 19 reported a significant decrease in TA of 0.21 D after an 8-min fixation period at the far point of accommodation. However, both Gilmartin and Bullimore 21 and Fisher et al 23 did not observe any significant changes in TA when subjects viewed targets located either at 0.3 D or the accommodative far point, respectively. When viewing a far target, adaptation is stimulated primarily by blur-driven accommodation, and the reduction of the proximal component may result in a more variable adaptation response. The observation that PIA does stimulate accommodative adaptation may also explain the previous finding of equivalent accommodative adaptation after monocular and binocular viewing conditions For binocular viewing, one would predict increased convergent accommodation, increased PIA, 6 ' 30 and decreased blur-driven accommodation when compared with monocular viewing. The latter two components stimulate adaptation under closedloop conditions In a comparison of monocular versus binocular fixation, if the change in blur input to adaptation were equal in magnitude but opposite in sign to the proximal stimulus, then no significant change in adaptation would be observed between these two viewing conditions. The data illustrated in Figure 4 indicated that those subjects demonstrating negative adaptation for either of the conditions examined had values of pretask TA greater than 1.75 D. Previous studies 15 ' 21 ' 38 have examined the effect of a nonselective, beta-adrenergic receptor antagonist (timolol maleate, 0.5%) on accommodative adaptation. The results indicated that subjects having higher levels of pretask TA were more susceptible to the effect of the sympathetic antagonist. This vvould imply that subjects having higher levels of pretask TA have greater access to betaadrenergic innervation to the ciliary muscle. Gilmartin and Hogan 39 proposed that a role of sympathetic innervation was to attenuate the accommodative adaptation after periods of sustained near vision. Thus, the negative adaptation (Figs. 3, 4) observed in the current study in subjects having higher levels of pretask TA may reflect the activity of inhibitory, betaadrenergic innervation to the ciliary muscle. Additionally, this negative adaptation was equivalent after both distance and near conditions (Fig. 3). Tornqvist 40 ' 41 observed that the magnitude of sympathetic innervation to accommodation was related to the level of concurrent parasympathetic activity. The data illustrated in Figure 4 imply that the adrenergic output is related to the aggregate parasympathetically mediated accommodative response, and is not restricted solely to the level of blur-driven accommodation. The current study has demonstrated that PIA does indeed stimulate accommodative adaptation. Furthermore, the magnitude of the proximal effect, doubling the degree of adaptation at near when compared with an equivalent blur stimulus at distance, suggests that the contribution of PIA to the closed-loop accommodative response is potentially substantial. Key words: accommodation, near-vision, oculomotor adaptation, proximal accommodation, tonic accommodation References 1. Maddox EE: The Clinical Use of Prisms and the Decentering of Lenses, 2nd ed. Bristol, John Wright & Sons, 1893, p Hofstetter HW: The proximal factor in accommodation and convergence. Am J Optom Arch Am Acad Optom 19:67, Ittleson WH and Ames A: Accommodation, convergence, and their relation to apparent distance. J Psychol 30:43, Hokoda SC and Ciuffreda KJ: Theoretical and clinical importance of proximal vergence and accommodation. In Vergence Eye Movements: Basic & Clinical Aspects, Schor CM and Ciuffreda KJ, editors. Boston, Butterworths, 1983, pp Rosenfield M and Gilmartin B: The effect of target proximity on open-loop accommodation. ARVO Abstracts. Invest Ophthalmol Vis Sci 30(Suppl):135, Wick B: Clinical factors in proximal vergence. Am J Optom Physiol Opt 62:1, Westheimer G: Amphetamine, barbiturates and accommodative-convergence. Arch Ophthalmol 70:830, Hung GK and Semmlow JL: Static behavior of accommodation and vergence: Computer simulation of an interactive dual-feedback system. IEEE Trans Biomed Eng BME-27:439, Ebenholtz SM and Fisher SK: Distance adaptation depends upon plasticity in the oculomotor control system. Percept Psychophys 31:551, Schor CM: Adaptive regulation of accommodative vergence and vergence accommodation. Am J Optom Physiol Opt 63:587, Rosenfield M and Gilmartin B: The effect of vergence adaptation on convergent accommodation. Ophthal Physiol Opt 8:172, Toates FM: Vergence eye movements. Doc Ophthalmol 37:153, Schor CM: Fixation disparity and vergence adaptation. In Vergence Eye Movements: Basic & Clinical Aspects, Schor CM
6 No. 6 PROXIMALLY INDUCED ACCOMMODATION / Rosenfield er ol 1167 and Ciuffreda KJ, editors. Boston, Butterworths, 1983, pp Leibowitz HW and Owens DA: New evidence for the intermediate position of relaxed accommodation. Doc Ophthalmol 46:133, Gilmartin B, Hogan RE, and Thompson SM: The effect of timolol maleate on tonic accommodation, tonic vergence, and pupil diameter. Invest Ophthalmol Vis Sci 25:763, McBrien NA and Millodot M: The relationship between tonic accommodation and refractive error. Invest Ophthalmol Vis Sci 28:997, Luckiesh M and Moss FK: The avoidance of dynamic accommodation through the use of a brightness-contrast threshold. Am J Ophthalmol 20:469, Heath GG: Components of accommodation. Am J Optom Arch Am Acad Optom 33:569, Ebenholtz SM: Accommodative hysteresis: A precursor for induced myopia? Invest Ophthalmol Vis Sci 24:513, Ebenholtz SM: Accommodative hysteresis: Relation to resting focus. Am J Optom Physiol Opt 62:755, Gilmartin B and Bullimore MA: Sustained near-vision augments inhibitory sympathetic innervation of the ciliary muscle. Clin Vision Sci 1:197, Owens DA and Wolf-Kelly K: Near work, visual fatigue, and variations of oculomotor tonus. Invest Ophthalmol Vis Sci 28:743, Fisher SK, Ciuffreda KJ, and Levine S: Tonic accommodation, accommodative hysteresis and refractive error. Am J Optom Physiol Opt 64:799, Rosenfield M and Gilmartin B: Accommodative adaptation induced by sustained disparity-vergence. Am J Optom Physiol Opt. 65:118, Schor CM and Tsuetaki TK: Fatigue of accommodation and vergence modifies their mutual interactions. Invest Ophthalmol Vis Sci 28:1250, Rosenfield M and Gilmartin B: Accommodative adaptation to monocular and binocular stimuli. Am J Optom Physiol Opt 65:862, Wolfe JM and O'Connell KM: Adaptation of the resting states of accommodation. Invest Ophthalmol Vis Sci 28:992, Kran BS and Ciuffreda KJ: Noncongruent stimuli and tonic adaptation. Am J Optom Physiol Opt 65:703, Fisher SK, Ciuffreda KJ, and Bird JE: The effect of monocular versus binocular fixation on accommodative hysteresis. Ophthal Physiol Opt 8:438, Ogle KN and Martens TG: On the accommodative convergence and the proximal convergence. Arch Ophthalmol 57:702, Franceschetti AT and Burian HM: Proximal convergence: An evaluation by comparison of major amblyoscope and alternate prism and cover test measurements and by AC/A ratio determinations. In Strabismus 69. St. Louis, CV Mosby Co. 1970, pp Hartinger H: Uber sin neves refraktometer. Deutsch Optisch Gesellschaft 57:105, Duke-Elder S and Abrams D: System of Ophthalmology, Vol 5: Ophthalmic Optics and Refraction. St. Louis, CV. Mosby, 1970, pp Bennett AG and Rabbetts RB: Clinical Visual Optics. London, Butterworths, 1984, pp Henson DB: Optometric Instrumentation. London, Butterworths, pp Phillips SR: Ocular neurological control systems: Accommodation and the near response triad. PhD thesis. Berkeley, University of California Department of Mechanical Engineering Krumholtz DM, Fox RS, and Ciuffreda KJ: Short-term changes in tonic accommodation. Invest Ophthalmol Vis Sci 27:552, Rosenfield M and Gilmartin B: Temporal aspects of accommodative adaptation. Optom Vis Sci 66:229, Gilmartin B and Hogan RE: The role of the sympathetic nervous system in ocular accommodation and ametropia. Ophthal Physiol Opt 5:91, Tornqvist G: Effect of cervical sympathetic stimulation on accommodation in monkeys. Acta Physiol Scand 67:363, Tornqvist G: The relative importance of the parasympathetic and sympathetic nervous systems for accommodation in monkeys. Invest Ophthalmol 6:612, 1967.
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