Optometry - Journal of the American Optometric Association
Volume 81, Issue 3 , Pages 129-136, March 2010

Static and dynamic aspects of accommodation in mild traumatic brain injury: A review

State University of New York State College of Optometry, New York, New York

Article Outline

Abstract 

Accommodation refers to the process of obtaining and maintaining a focused foveal retinal image of an object of interest. It involves optical, sensory, motor, perceptual, cognitive, pharmacologic, and biomechanical aspects, and hence represents a complex, multilevel neurologic control process. In patients with mild traumatic brain injury (mTBI), this process frequently is disrupted and compromised neurologically because of the pervasiveness of the coup-contrecoup, swelling, and shearing aspects of the brain injury. In this report, we review the earlier literature on accommodation in mTBI and then present several new findings from our clinical research unit, along with their clinical implications.

Keywords: Accommodation, Accommodative dysfunction, Acquired brain injury, Optometric vision therapy, Vision rehabilitation, Traumatic brain injury

 

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Overview of accommodation 

Accommodation refers to the change in shape and curvature of the crystalline lens in an attempt to obtain and maintain a focused, high-resolution retinal image of an object of regard at the fovea.1 Once positioned at the fovea, the object can be accurately identified, and a detailed visual analysis of its attributes can be performed.

There are 4 components of accommodation.1, 2, 3 Blur-driven, or reflex accommodation, likely provides a large contribution to the overall response. This involves the automatic and nonvoluntary focusing ability when changing fixate from one object to another at different distances in response to the correlated blurred retinal image. Vergence accommodation refers to that accommodation driven by the neurologic crosslink between fusional (i.e., disparity) vergence and accommodation per the vergence accommodation-to-vergence ratio (i.e., the CA/C ratio). This too is a major contributor to the global accommodative response. Proximal accommodation is that perceptual component of accommodation related to knowledge of the apparent or perceived nearness of an object in one's surroundings. Because of the direct feedback control nature of the accommodative and vergence loops,3 however, proximal accommodation can only contribute a small amount to the actual motor response, although its perceptually based context provides critical directional information to the accommodative system.4, 5 Lastly, tonic accommodation refers to the default accommodative response that occurs in the absence of blur, disparity, and proximal stimuli, as might occur in a large, totally darkened room.5, 6 It is commonly believed to result from baseline neural input from the dual innervation of the ciliary muscle, namely, the parasympathetic and sympathetic systems.7, 8 Under normal viewing conditions, it too contributes little to the total motor response.3, 6 These 4 components interact in a nonlinear manner to produce the overall dynamic and static accommodative response.3

The anatomic pathway for accommodation involves many brain areas and neural interconnections (see Figure 1). The change in defocus blur acts as the direct stimulus to drive the accommodative system. In a nonpresbyopic individual without an accommodative dysfunction, this initial blur-related information is transmitted efficiently and effectively along the appropriate neural pathways. This results in a corresponding time-optimal change in lens shape and curvature to provide a focused retinal image and subsequent visual clarity. This produces clear, single vision in individuals without vergence dysfunction, which is in contrast to the experiences of many patients suffering from brain injury.9, 10, 11, 12

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Overview of acquired brain injury 

Acquired brain injury (ABI) is a general term that encompasses any type of sudden-onset brain insult obtained after birth, including blunt force, penetrating injury, cerebrovascular accident or “stroke,” postsurgical brain complications, brain tumor, encephalopathy, and others.13 Traumatic brain injury (TBI) is a major category of ABI, which typically results when an external force causes either an open- or closed-head injury.14, 15 In the United States, approximately 1.4 million people suffer TBI each year.16 About 95% of them are either hospitalized or treated in emergency rooms,16 and a large number will require a range of subsequent medical and rehabilitative services.14 Furthermore, at least 5.3 million Americans have the need for long-term assistance to perform activities of daily living (ADL) as a result of their TBI.17 The highest rates of TBI occur in the young (<15 years) and elderly (>75 years) populations, with a higher incidence among men across all age groups.16 Falls and motor vehicle accidents are the primary causes of TBI.16 TBI patients with closed-head injuries incur a relatively global brain injury, which frequently results in diffuse axonal injury because of its coup-contrecoup nature.10, 18, 19 This widespread damage often leads to the development of a range of visual symptoms (see Table 1) and signs (see Table 2) relating to the accommodative and accommodative vergence systems.20, 21, 22

Table 1. Accommodatively based visual symptoms in TBI
Adapted from Ciuffreda et al.20
Eye focusing problems
Blur
Eyestrain and visual fatigue
Avoidance of near tasks
Oculomotor-based reading difficulties
Headache
Intermittent diplopia
Table 2. Accommodatively based signs in TBI
Adapted from Ciuffreda et al.20
Reduced amplitude of accommodation
Increased lag of accommodation
Slowed accommodative facility
Reduced relative accommodation
Uncorrected hyperopia/astigmatism (because of an inability to compensate accommodatively)
Restricted fusional vergence ranges at near related to accommodative interactive problems

The purpose of the current report is to review the literature regarding dynamic and static aspects of accommodation in mild TBI (mTBI), in which the individual has either an altered state of consciousness or a loss of consciousness of less than 20 minutes' duration.14 Various clinical studies have elucidated the common symptoms and signs exhibited in these patients, along with the related visual dysfunctions. Furthermore, laboratory research and carefully documented case studies and series have uncovered and assessed specific static and dynamic accommodative abnormalities found in this population. It is important for the primary eye care provider (e.g., optometrist or ophthalmologist), and others such as the physiatrist and neurologist, to be aware of the commonly found accommodative disturbances that adversely affect their patients with mTBI, as well as the associated signs and symptoms, to provide prompt and appropriate care with alleviation of symptoms as well as improving visual efficiency and quality of life with respect to re-establishing one's vocational and avocational goals.

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Prior clinical and research studies on accommodation in mTBI 

The previous literature has described 3 types of accommodative dysfunctions in mTBI. These include accommodative insufficiency, which is the most prominent; pseudomyopia; and dynamic accommodative infacility.

Accommodative insufficiency is diagnosed when a patient's accommodative response amplitude is significantly lower than the expected age-related normative value.10, 23 This parameter has been used frequently as a key clinical and laboratory measurement of accommodative function. Four prior studies of patients with mTBI, each with 46 to 62 subjects, reported a 10% to 33% incidence of accommodative insufficiency using reduced accommodative amplitude as the diagnostic parameter.24, 25, 26, 27 Another study, which used either reduced accommodative amplitude or positive relative accommodation (PRA) as the diagnostic parameter, reported that 16% of the 161 mTBI patients manifested such “poor accommodation.”28

Because whiplash injuries are similar to TBI, in that they can be conceptualized as having a coup-contrecoup injury of an indirect nature, affected individuals may be regarded as having a mild form of TBI as well as potential injury to other areas of the brain such as the vulnerable posterior thalamus.29 Various studies have reported that approximately 18% to 33% of whiplash patients exhibited reduced accommodative amplitude,30, 31 which agrees with the previously stated incidence in the more traditionally categorized mTBI patients. Lastly, 1 study found a statistically significant reduction in the accommodative amplitudes of 4 age groups of whiplash patients when compared with age-matched visually normal control groups.32 In general, these whiplash groups exhibited approximately a 35% decrease in accommodative amplitude when compared with the control groups.

Although less frequent, overaccommodation has been reported in mTBI patients, termed either accommodative excess or pseudomyopia.10 In a sample of 161 mTBI patients, 19% exhibited “pseudomyopia.”28 This was diagnosed if the patient reported blur at distance that could be corrected with minus lenses when the patient had no previous history of such a prescription, as well as a cycloplegic refraction that elicited either emmetropia, low hyperopia, or significantly less myopia.

Dynamic accommodative dysfunction in mTBI has been researched infrequently. Accommodative infacility is diagnosed when a patient exhibits a slowed dynamic accommodative response to a change in either dioptric lens power or target distance.10 Two previous case studies have provided keen insight into the possible dynamic accommodative disturbances that could result from a TBI. First, Ohtsuka and Sawa33 reported on a 29-year-old man with agenesis of the posterior vermis of the cerebellum. Using an objective, dynamic, infrared optometer, the accommodative responses of the patient and a visually normal control subject were compared when tracking a sinusoidally modulated blur stimulus (see Figure 2). The patient exhibited significantly less accuracy, including an increased lag and a decreased response amplitude (i.e., gain), at all 3 of the relatively slow temporal stimulus frequencies, than found in the control subject. Secondly, Kawasaki et al.34 reported on a 20-year-old woman with a subtentorial arachnoid cyst. Using an objective, dynamic, infrared optometer, this patient exhibited normal accommodative responses to a slowly modulated ramp stimulus (see Figure 3A); however, the patient manifested significantly abnormal accommodative responses to repetitive predictable step stimuli (see Figure 3B), including reduced and variable response amplitude. After surgical removal of the cyst, however, the patient regained a normal accommodative response to the predictable step stimuli (see Figure 3B).

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  • Figure 2 

    Examples of accommodative responses to simple sinusoidal blur stimuli at frequencies of 0.1, 0.2, and 0.3 Hz in the patient and a normal control subject. High contrast, black and white target of 3 degrees angular extent. T = target movements; A = accommodative responses.

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  • Figure 3 

    A, Preoperative accommodative response to a linear ramp stimulus in a patient with a cerebellar cyst. Solid line represents the stimulus for increasing and decreasing accommodation, and the dotted portion represents the actual dynamic accommodative response. B, Preoperative (top) and postoperative (bottom) accommodative responses to repetitive, predictable step stimuli in a patient with a cerebellar cyst.

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SUNY Brain Injury Clinical Research Group: retrospective analysis 

Previous studies have focused typically on one specific accommodative parameter (i.e., accommodative amplitude) within their TBI population relating to a single diagnostic category of accommodative abnormality (i.e., accommodative insufficiency), as described earlier. Although such investigations have served a very important purpose, they do not provide a sense of the range of possible accommodative dysfunctions and adverse effects on quality of life and activities of daily living, as well as their potential for remediation.

However, recently 2 extensive clinical, retrospective studies in mTBI patients incorporated a computer-based query to determine the incidence of various oculomotor dysfunctions,9 including accommodative abnormalities, as well as the functional outcome after conventional optometric vision therapy.11 Medical records were searched over a 3-year period at our clinic, which uncovered 160 individuals with mTBI, with 51 of them being under 40 years of age (i.e., prepresbyopic), and therefore having received extensive accommodative testing. Of these 51 patients, approximately 40% manifested an accommodative dysfunction, with accommodative insufficiency being the most common anomaly (see Table 3). Ninety percent exhibited accommodative insufficiency, 10% exhibited accommodative infacility, and 10% exhibited accommodative excess, with some patients presenting with more than one such abnormality (see Table 4).

Table 3. Percentage of individuals with TBI (n = 160) with a specific category of ocular motor dysfunction and the most common anomaly
Reprinted with permission from Ciuffreda et al., 2007.9
Ocular motor dysfunctionPercentageMost common anomaly
Accommodation41.1Accommodative insufficiency
Versional51.3Deficits of saccades
Vergence56.3Convergence insufficiency
Strabismus25.6Strabismus at near
CN palsy6.9CN III palsy

Note. The number of persons tested for accommodation included only those 51 individuals younger than 40 years (i.e., prepresbyopic).

Table 4. Number of individuals with a specific category of accommodative dysfunction
Reprinted with permission from Ciuffreda et al, 2007.9
Accommodative insufficiencyAccommodative infacilityAccommodative excessIll-sustained accommodationTotal with accommodative dysfunction
TBI (n = 51)1922021

Note. Some persons presented with more than one accommodative dysfunction. The number of persons tested for accommodation included only those 51 individuals younger than 40 years (i.e., prepresbyopic). Twenty-one of 51 = 41.1% of persons with TBI presented with an accommodative dysfunction.

Thirty-three of the above 160 mTBI patients had completed a conventional optometric vision therapy program.11 Thirty of the 33 (90%) improved markedly in at least one sign and one symptom, which was considered to represent a “successful treatment.” These findings are consistent with the results of others.12 Thus, with relatively simple therapeutic procedures, these accommodative dysfunctions can be partially/fully remediated, along with considerable symptomatic relief and improved function.

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SUNY Brain Injury Clinical Research Group: laboratory analysis 

A recent prospective study35 of 12 adult (ages 18 to 40 years) visually symptomatic mTBI patients uncovered 5 static and dynamic accommodative abnormalities as assessed in the clinical and laboratory setting using both objective and subjective techniques. These included reduced monocular amplitude of accommodation, reduced binocular amplitude of accommodation, increased time constant, decreased peak velocity, and increased fatigue.

Static findings 

Monocular and binocular push-up accommodative amplitude was assessed in the patients and compared with their specific age-matched mean Duane's normative value.23 The mTBI group exhibited a significantly decreased mean accommodative amplitude (see Table 5) for both the monocular and binocular test conditions. The patients' values should be near their age-matched Duane's normative mean value and distributed approximately equally above and below the respective mean values. However, the patients exhibited a considerably different profile (see Figure 4). Of the 36 accommodative amplitude measurements (i.e., right eye, left eye, and both eyes in the 12 subjects), only 17% (6/36) were greater than Duane's normative mean value, with none exceeding Duane's maximum normative value. Furthermore, and most importantly, 58% (21/36) of the patients' accommodative amplitude values fell below Duane's minimum normative value.

Table 5. Comparison of significantly different accommodative parameter mean values between the mTBI group and either the control group values (time constant and peak velocity) or normative literature values (accommodative amplitude)
ParameterDirection of change in mTBI groupNormal versus mTBI
Time constantIncrease259 ms vs. 384 ms
Peak velocityDecrease8.0 D/s vs. 5.6 D/s
Monocular push-up accommodative amplitudeDecrease8.23 D vs. 6.51 D
Binocular push-up accommodative amplitudeDecrease8.68 D vs. 7.15 D

D/s = diopters per second.

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  • Figure 4 

    Monocular and binocular push-up accommodative amplitudes of 12 patients with mild traumatic brain injury plotted on Duane's graph for visually normal individuals over a wide range of ages. Poly. = Polynomial fit to data.

Three other static parameters were assessed: tonic accommodation, accommodative stimulus/response function, and stimulus accommodative convergence-to-accommodation (AC/A) ratio. However, none provided a significant differentiation between the mTBI and normal control groups.

Dynamic findings 

Using an objective, infrared, open-field autorefractor (WAM 5500; Grand Seiko, Hiroshima, Japan), continuous (5 samples per second) measurements were obtained of monocular accommodative responses to a temporally nonpredictable accommodative step stimulus (targets at 2D and 4D). Accommodation was measured over approximately a 120-second period to obtain 10 to 20 high-quality accommodative step responses, with commands from the experimenter to alter focus between the 2 targets. The mean accommodative time constant (i.e., time for the exponential response to reach 63% of the final steady-state amplitude) and peak velocity (i.e., maximum velocity) was determined for the mTBI group and compared with a control group of 12 visually normal subjects. The patient group exhibited a significantly increased mean time constant and decreased mean peak velocity when compared with the normal control group mean values (see Table 5). Thus, the overall response was significantly slowed in the mTBI patients. Figure 5 portrays the qualitative and quantitative differences in accommodative step responses between a visually normal control subject and a mTBI patient exhibiting considerable response abnormality. The patient manifested a substantially longer time constant and lower peak velocity, and hence completed the accommodative response in approximately 1.6 seconds. In contrast, the normal subject took only approximately 1.0 second for completion. On average, slowed responses occurred in all 12 of the patients, with individual overall response times ranging from slightly more than 1 second to nearly 4 seconds. In comparison, the normal group exhibited individual overall response times of 1 second or less. Thus, the TBI group manifested responses that were slowed by up to 4-fold.

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  • Figure 5 

    Exponential fit to raw data (accommodative response as a function of time) for a visually normal subject (top) and a mTBI subject manifesting dynamic abnormalities (bottom) for both increasing accommodation. Tau = time constant, Ampl. = response amplitude, and PV = peak velocity.

Two additional objective dynamic parameters were assessed: accommodative response amplitude (i.e., gain) and steady-state accommodative response variability. When performing a step change in accommodation, the mTBI and normal groups exhibited similarly sized accommodative response amplitudes. This shows that the increased mean time constant and related decreased mean peak velocity between the groups was caused by neurologic damage in the mTBI patients and not simply a difference in response magnitude.36 Although the groups did not exhibit a significant difference in mean steady-state response variability, there was a trend for the mTBI patients to manifest slightly greater variability than the normal individuals (0.17D versus 0.15D, respectively).

Finally, another measure of dynamic accommodative ability, namely the clinical binocular ±1.00 diopter (D) accommodative lens flipper facility rate, was assessed before and after a continuous 3-minute test session, which attempted to induce and assess fatigue effects. The pre- and post-task was to alternate viewing between the +1.00 D and the −1.00 D lenses as rapidly as possible during a 1-minute period, while assuring target clarity before each lens alternation. These lower flipper lens values were used because of the relatively older ages of several subjects.37 The 3-minute fatigue session involved accurate sustained focus on the target, with lens alternation every 10 seconds on command of the examiner. Although visual fatigue is a common complaint among TBI patients (see Table 1), such an experiment had not been performed previously on this patient population. There was a significant effect of the 3-minute fatigue session on the mean accommodative flipper facility rate in the mTBI group. The mean decrease in flipper rate in the mTBI group was 2.5 cycles per minute (cpm), with mean pre- and postfatigue rates of 16.3 cpm and 13.8 cpm, respectively (see Figure 6A). Furthermore, 10 of the 12 (83%) patients manifested a decrease in flipper rate after the 3-minute fatigue session (see Figure 6B).

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  • Figure 6 

    A, Mean binocular accommodative lens flipper facility rate (cpm) in the mTBI group, before and after the fatigue trials. Plotted as the mean +1 SEM. B, Individual binocular accommodative lens flipper facility rates (cpm) in the mTBI group, before and after the fatigue trials.

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Discussion 

Unfortunately, a paucity of research has been devoted to elucidating the types and range of accommodative dysfunctions in the mTBI population. This review has discussed in detail appropriate literature related to this topic including both older and very recent reports, described common abnormal accommodative findings in this population, and provided brief information on the remediation of such deficits.

Our most recent clinical and laboratory research has confirmed and expanded on the previously documented findings related to accommodative deficits in mTBI. The static clinical measurement of accommodative amplitude still remains a valuable tool in revealing accommodative dysfunction in mTBI patients. Additionally, some less common measurements of accommodation, such as objective assessment of dynamic accommodative step responses and subjective assessment of fatigue using lens flippers, have proven vital in furthering our understanding of mTBI effects on the accommodative system. Fatigability, abnormally low accommodative amplitude, and slowed dynamics were all hallmarks of accommodative dysfunction in our mTBI patients. Both accommodative amplitude and accommodative flipper fatigability can be evaluated easily in any clinical setting, and thus may serve as potential simple markers for accommodative defects in mTBI. Furthermore, accommodative step responses could also be objectively measured to confirm or expand the diagnosis in selected patients using an appropriate autorefractor and test stimuli. Unfortunately, with our present laboratory set-up, accommodative latency could not be assessed. However, we would predict it to be increased, as recently found for the vergence system in this population.38

Prompt and appropriate diagnosis is imperative in maximizing the rehabilitative potential and minimizing the adverse effect on activities of daily living and quality of life. As previously mentioned, mTBI patients frequently experience accommodatively based symptoms, such as blur, intermittent diplopia, eyestrain, and headaches, which can have a profoundly negative impact on reading ability, ambulation, driving, and visual detection/discrimination tasks.20 Such limitations will likely alter the individual's ability to perform or enjoy both vocational and avocational tasks. Furthermore, untreated accommodative abnormalities have the potential to interfere with progress in other rehabilitative services (e.g., cognitive therapy) involving a range of both general and specific visual demands.39, 40 Fortunately, as previously described,11 these accommodative dysfunctions can be remediated successfully by using relatively simple optometric vision therapy protocols41, 42 involving the principles of perceptual and motor learning.43 In prepresbyopes, the vision therapy can be combined with single-vision distance corrective lenses, single-vision near corrective lenses incorporating a +1 D addition, and frequent rest periods from near work involving relaxed gazing into the distance.20 Single-vision lenses rather than any type of multifocal lenses, especially progressive addition lenses (PALs), are prescribed, as most TBI patients manifest hypersensitivity to the perceived motion in the lens periphery as related to power and magnification discontinuities.20

Given the extensive neural pathways associated with the accommodative system (see Figure 1), it is feasible that a mTBI affecting the cerebrum, cerebellum, or brainstem could directly damage accommodation-related neural sites or their axonal interconnections. Furthermore, the coup-contrecoup nature of the TBI is conducive to brain swelling and shearing forces, which may cause corollary brain damage in addition to the direct injury site.19 Human lesion case studies33, 34, 44, 45 have confirmed that injury to the area of the superior temporal and posterior parietal lobes of the cerebrum, rostral superior colliculus of the brainstem, and cerebellum can all potentially result in static and dynamic accommodative abnormalities. Several single-unit cell recording studies in monkeys46, 47, 48, 49 have described neurons in the posterior parietal cortex, mesencephalic reticular formation, and Edinger-Westphal nucleus that elicit response characteristics related to accommodative response velocity. It is likely that similar neurons are present in the human brain. Damage involving these neurons carrying accommodative velocity information may result in dynamic abnormalities, which could present as increased time constant, decreased peak velocity, or abnormalities in the clinical measurement of accommodative facility, including increased fatigability. This could result from a reduced number of neurons, weakened and easily fatigued/stressed neurons, or impaired synchronization within the individual component cell or the interaction of the cells within the neural network itself.35 Furthermore, damage to any portion of the accommodative pathway could result in a relative decrease in the number of neurons sending signals to the ciliary muscle, which could present clinically as reduced accommodative amplitude.

Although millions of individuals and their families in the United States are affected by mTBI,16, 17 the continuation of wars overseas will likely result in many more military personnel and their families (as well as civilians who are in harm's way) to also have to deal with the effects of TBI,27 mild and worse. More than ever, research into this issue is critical to provide individuals the ability to resume the lifestyle they enjoyed before their head injury. Neurophysiological50 (e.g., MATLAB-based) and bioengineering3 models are able to simulate the adverse effects of TBI on the accommodative system, which, in turn, could provide insight into the defective functional mechanism involved. Moreover, brain imaging studies involving computed tomography, standard magnetic resonance imaging, functional magnetic resonance imaging, and diffusion tensor imaging could expand on the accommodative effects associated with lesions at specific anatomical sites.51, 52 These techniques could be used in conjunction with the more traditional visually evoked cortical response,53 especially those including concurrent monitoring of alpha brain activity (e.g., Diopsys NOVA-TR, Pine Brook, New Jersey) to assess visual attention.54 Finally, confirming and expanding upon the current vision rehabilitation strategies would lead to more efficacious treatment options for this population as well as the positive impact on quality of life and activities of daily living.

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Acknowledgments 

The authors thank Drs. J. Choi-Lee, A. Cohen, J. Cohen, E. Han, L. Lowell, V. Wren, and Ms. I. Rosen for providing study patients. The authors thank Drs. S. Craig, E. Han, and D. Rutner for their participation in the retrospective studies.

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PII: S1529-1839(09)00522-3

doi:10.1016/j.optm.2009.07.015

Optometry - Journal of the American Optometric Association
Volume 81, Issue 3 , Pages 129-136, March 2010

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