C 2005) Applied Psychophysiology and Biofeedback, Vol. 30, No. 4, December 2005 ( DOI: 10.1007/s10484-005-8424-1
An Instrument for Biofeedback Applied to Vision Dario Giorgi,1,2 Maria Teresa Contestabile,1 Elena Pacella,1 and Corrado Balacco Gabrieli1
One hundred and ten patients (179 eyes) with reduced visual acuity caused by different ocular disorders underwent visual rehabilitation with an instrument for biofeedback: improved biofeedback integrated system (Ibis). One hundred and fourteen eyes had age-related macular degeneration, 39 eyes had myopic macular degeneration, and 26 eyes were affected by different ocular disorders. A placebo training was developed on 34 patients (47 eyes). Thirty-three eyes had age-related macular degeneration and 15 eyes had myopic macular degeneration. Visual acuity was found to be improved in 130/179 eyes (72.62%). Mean visual acuity was 0.24 before training and 0.36 at the last follow-up. A review of the literature and possible mechanisms are discussed. KEY WORDS: biofeedback; low vision; macular degeneration; central scotoma; visual rehabilitation; improved biofeedback integrated system (Ibis).
Various forms of biofeedback have been applied to vision in the past. In particular, biofeedback has been employed in patients with ametropia (myopia, astigmatism, presbyopia) and in those patients who are suffering from different ocular diseases such as maculopathy, amblyopia, and nystagmus (Abadi, Carden, & Sinpson, 1980; Ciuffreda, Goldrich, & Neary, 1982; Fossetti, 1962; Iorio et al., 1998; Leung, Wick, & Bedell, 1996; Moncada, 1995; Trachtman, 1978). In our previous study, we found an amelioration in visual acuity in a group of patients with low vision who underwent visual rehabilitation with an instrument for BF applied to vision (Improved Biofeedback Integrated System: Ibis) (Contestabile et al., 2002). These encouraging results prompted us to extend this research with the aim of further establishing the efficacy of this method of visual rehabilitation. MATERIALS AND METHODS One hundred and seventy-nine eyes of 110 patients (49 females and 61 males) were enrolled in this study. They were affected by different ocular diseases: 114 eyes had 1 Department
of Ophthalmological Science, “La Sapienza” University, Rome, Italy. all correspondence to Dr. Dario Giorgi, “La Sapienza” University, Via Guglielmo degli Ubertini 64, 00176 Roma, Italy; e-mail:
[email protected].
2 Address
389 C 2005 Springer Science+Business Media, Inc. 1090-0586/05/1200-0389/0
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age-related macular degeneration (mean age: 72.6 years), 39 eyes had myopic macular degeneration (mean age: 58.0 years), 4 eyes had glaucoma, 2 eyes had central retinal vein thrombosis, 7 eyes had retrobulbar optic neuropathy, 4 eyes had retinitis pigmentosa (all with the classical rod–cone-versus type), 5 eyes had amblyopia, 2 eyes had diabetic retinopathy, and finally 2 eyes were of a patient with low vision caused by a cortical ischemic damage. All patients had received pharmacological, laser, or occlusive treatment in the past on the basis of specific pathology or amblyopic disorder. The most important criteria chosen for inclusion in this study were the following: (1) reduction of visual acuity caused by ocular disorders where traditional treatments cannot offer further results; (2) stability of visual acuity for at least 1 year before training; and (3) no history of epilepsy and good patient collaboration. All these patients underwent visual training with infrared photo-stimulation using a specially designed biofeedback instrument, termed the “improved biofeedback integrated system” (Ibis). Ibis is composed of an optical and an electronic unit as reported in our previous paper (Figs. 1 and 2) (Contestabile et al., 2002). Training was performed in a darkened room. During each session, after having aligned the patient’s eye, the instrument was switched on, thus starting infrared photostimulation and also foveal flicker stimulation. The latter was performed by turning on the internal foveal stimulator consisting of a red intermittent light inside the eyepiece. The intensity of the foveal stimulus was chosen on the basis of visual acuity in each case. The frequency was set at the value immediately lower than that at which the patient could see a fixed red light (critical fusion frequency). Thus, the volume switch was turned on by the operator. The patient was initially asked to look at the light inside the eyepiece. The operator made fine movements when the auditory signal reached the highest volume. Then the patient had to maintain this volume, which corresponded to the highest level of biofeedback. The increase in volume was shown both by the digital display of information and the rise of the peak on the monitor. Each patient was trained twice a week for a total of 16 sessions. Every session involved three applications lasting for 3 min each with a brief pause in between. Refraction was performed in a standardized fashion and visual acuity was measured at a distance of 5 m using standard Snellen charts. Particularly, the best corrected visual acuity was tested after every eight sessions using the same charts. During the last follow-up, a visual acuity chart with a different arrangement of letters was employed. A placebo training was performed, enrolling 34 patients with low vision (19 females and 15 males; 47 eyes total) with the same inclusion criteria as the forementioned cases. There were 14 bilateral and 20 unilateral cases. Thirty-three eyes were affected by age-related macular degeneration while 15 eyes were suffering from myopic macular degeneration. The placebo training was developed to mimic the attention, equipment, and time involved in the technique of biofeedback. During each session, the patient was asked to look at the red light located in the occluder of the instrument. This light, that could be used at different frequency levels, was set at the maximum level in order to be perceived as a fixed red light. Similar to the experimental training, visual acuity was tested after every eight sessions. Statistical analysis of these data was performed using the t-test.
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Fig. 1. Optical unit of the improved biofeedback integrated system (Ibis). (1) internal foveal stimulator; (2) eyepiece; and (3) joystick.
RESULTS The mean value of visual acuity before training was 0.24 (SD = 0.13) and 0.36 (SD = 0.24) at the last follow-up. The statistical analysis showed a significant improvement in visual acuity (t = 3.53; p ≤ 0.01). Table I shows the mean value of visual acuity for each ocular disorder before training, after eight sessions, and after termination of training. Visual acuity was improved in 130 eyes (72.62%). The mean value of visual acuity before training of patients who responded to visual rehabilitation was 0.21 (SD = 0.11)
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Fig. 2. Electronic unit of the improved biofeedback integrated system (Ibis). (1) ON/OFF switch; (2) switch for alignment led; (3) indicator of intensity of environment light; (4) indicator of period of intermittence of foveal stimulus; (5) selectors of period of intermittence of foveal stimulus; (6) monitor to control alignment, level of biofeedback and direction of gaze; (7) regulator of the volume of feedback sound (headset) and regulator of the volume of feedback sound (environment); (8) selector/indicator of feedback sound; (9) digital indicator of feedback level; (10) timer; (11) commands for timer; (12) timer reset; (13) switch for internal foveal stimulator; (14) selector of background light of internal fixation point; and (15) indicator of luminous intensity of foveal stimulus.
and 0.37 (SD = 0.15) at the last follow-up. This group was composed of 83 eyes with age-related macular degeneration, 32 eyes with myopic macular degeneration, 5 eyes with amblyopia, 4 eyes with retrobulbar optic neuropathy, 3 eyes with glaucoma, 2 eyes with central retinal vein thrombosis, and 1 eye with diabetic retinopathy. At 4 months after termination of training, the visual acuity was stable in all eyes but in two eyes with glaucoma, two with amblyopia, and six with age-related macular degeneration, regression occurred. Conversely, 49 eyes (27.37%) did not show an amelioration of visual acuity both after 8 and 16 training sessions. The mean value of visual acuity before Table I. Mean Values of Visual Acuity (Detected with Standard Snellen Charts) Found in Each Type of Ocular Disease Before Training, After Eight Sessions and After Termination of Training Mean visual acuity Pre-training 8th session 16th session
ARMD
MMD
DR
AMB
RON
GLA
CRVT
RP
CLV
0.15 0.22 0.25
0.29 0.38 0.42
0.10 0.10 0.15
0.36 0.62 0.62
0.28 0.28 0.45
0.26 0.39 0.42
0.40 0.50 0.60
0.33 0.33 0.33
0.02 0.02 0.02
Note. Using Standard Snellen Charts, the best visual acuity is 1.1 in healthy subjects; ARMD: age-related macular degeneration; MMD: myopic macular degeneration; DR: diabetic retinopathy; AMB: amblyopia; RON: retrobulbar optic neuropathy; GLA: glaucoma; CRVT: central retinal vein thrombosis; RP: retinitis pigmentosa; CLV: cortical low vision.
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training was 0.16 (SD = 0.11) for these individuals. Particularly, all eyes with retinitis pigmentosa did not show an amelioration of visual acuity after termination of training. After placebo training, the visual acuity was found to be improved for only two eyes, both of which experienced myopic macular degeneration. DISCUSSION Biofeedback may be defined as any technique that increases the ability of a person to control voluntarily physiological activities by providing information about those activities (Rotberg, 1983). Several studies have suggested the utility of biofeedback in the treatment of different ophthalmologic disorders, such as blefarospasm, strabismus, nystagmus, amblyopia, refractive error correction, reduction of intraocular pressure, and in the visual rehabilitation of patients with macular degeneration (Abadi, Carden, & Sinpson, 1980; Allen, 1954; Balliet & Nakayama, 1978; Ciuffreda et al., 1982; Contestaible et al., 2002; Flom, Kirschen, & Bedell, 1980; Fossetti, 1962; Iorio et al., 1998; Leung et al, 1996; Rowan & Sedlacek, 1981; Roxanas, Thomas, & Rapp, 1978; Russ, Kass, & O’Connell, 1978; Trachtman, 1978, 1987). In this paper, we studied the application of biofeedback in the management of subjects with reduced visual acutiy due to different ocular abnormalities, particularly age-related macular degeneration and myopic macular degeneration. We found a significant subjective improvment of visual acuity in 130/179 eyes (72.62%). In particular, the mean value of visual acuity before training was 0.24 and 0.36 at the last follow-up. This study illustrates that biofeedback may be a beneficial treatment for the visual rehabilitation of patients with low vision. These findings take on increased significance considering that, at the present time, there are no methods (neither medication nor laser treatments) to improve further the visual acuity of patients with advanced macular degeneration, a condition that is among the three most common causes of blindness and low vision throughout the world and a condition that is increasing in prevalence due to shifts in aging. It is not yet understood how biofeedback produces amelioration of visual function in patients with low vision. A valid theory still remains to be advanced. While many researchers are concentrating their efforts to understand whether biofeedback works for the treatment of these ophthalmologic disorders, probably the more relevant question still remains: “how does it work?” Since 1955, it has been hypothesized that the loss of macular function can be considered as the cause of eccentric fixation; patients with central visual field loss develop eccentric fixation as a direct result of their central scotomas (scotoma hypothesis) (Bangerter, 1955; B¨ohme, 1955). Particularly, the eccentrically fixating eye utilizes the retina, outside the damaged macular area, with the relatively highest resolving power. Some authors emphasize that the next fixation retinal area could be considered like a “pseudo-fovea,” and it was defined as “preferred retinal locus” (Cummings, Whittaker, Watson, & Budd, 1985; Whittaker, Budd, & Cummings, 1988). The preferred retinal locus is located in an area that is adjacent to the scotoma. Then, it could be possible that patients who underwent visual rehabilitation with biofeedack would become aware of their defect and learn to control both their fixation pattern and their oculomotor behavior. The highest level of biofeedback, expressed by the increase in volume of the auditory signal, could be reached when the fixation was modified, even if the mechanism of action is not clear. When the patient has
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learned to modify oculomotor behavior, this function is automatically controlled through practice. In our opinion, learning to use eccentric fixation could be the more reasonable mechanism contributing to the visual amelioration. From our results, some patients showed visual improvement while others did not. We noted that all patients with a visual acuity less than 0.1 reported a significantly low response to biofeedback. According to the “Eccentric Fixation” theory, this phenomenon could be due to the fact that patients with more significantly reduced visual acuity before training also have more extended central visual field loss, particularly in those affected by myopic and age-related macular degeneration. In fact, patients with macular degeneration have areas of both retinal and choroidal atrophy which reduce the central visual field. In our study group, these areas of retino-choroidal atrophy were significantly more extended in those patients with a visual acuity less than 0.1. The presence of more large central scotomas in this group could explain the reason for which these patients were unable to develop a new area for fixation outside the altered retinal area. Furthermore, still another interesting result which could confirm the leading role of the “eccentric fixation” theory to explain these results is represented by the absence of a visual amelioration in patients with retinitis pigmentosa (RP). In fact, it is well known that patients with the classical and most common type of RP (rod–cone versus) develop a progressive periferal-versus-central visual filed loss. The presence of outside macular visual field defects in these patients could explain the reason for which their visual acuity did not show signs of amelioration (Table I). Our opinion is that patients affected by RP, who underwent visual rehabilitation with Ibis, have a low capacity to find a new “fixation point” due to their visual field abnormalities. Probably, some subjecive variables, such as motivation, learning effect, psychophysical capacity, and the influence of the examiner could play a significant role in determining the visual improvment. Finally, further studies are needed to advance a valid scientific theory on the true psycho-physiological mechanisms of action which make useful training with Ibis or with other methods of biofeedback. REFERENCES Abadi, R. V., Carden, D., & Sinpson, J. (1980). A new treatment for congenital nystagmus. British Journal of Ophthalmology, 64, 2–6. Allen, M. J. (1954). Dependence of cyclophoria on convergence, elevation, and the system of axes. American Journal of Optometry, 31, 297. Balliet, R., & Nakayama, K. (1978). Training of voluntary torsion. Investigative Ophthalmology, 17, 303–314. Bangerter, A. (1955). Amblyopiebehandlung (2nd ed.). New York: Basel, Karger. B¨ohme, G. (1955). Zur Kenntnis der exzentrischen fixation im hinblick auf die behandlung der amblyopie. Klinische Monatsblatter fur Augenheilkunde, 126, 694–719. Ciuffreda, K. J., Goldrich, S. G., & Neary, C. (1982). Use of the eye movement auditory feedback in the control of nystagmus. American Journal of Optometry and Physiological Optics, 59, 396–409. Contestabile, M. T., Recupero, S. M., Palladino, D., De Stefanis, M., Abdolrahimzadeh, S., Suppressa, F., & Balacco Gabrieli, C. (2002). A new method of biofeedback in the management of low vision. Eye, 16, 472–480. Cummings, R. W., Whittaker, S. G., Watson, S. G., & Budd, J. M. (1985). Scanning characters and reading with a central scotoma. American Journal of Optometry and Physiological Optics, 62, 833–843. Flom, M. C., Kirschen, D. G., & Bedell, H. E. (1980). Control of unsteady, eccentric fixation in amblyopic eyes by auditory feedback of eye position. Investigative Ophthalmology and Visual Science, 19, 1371–1381. Fossetti, A. (1962). The management of myopia by biofeedback visual training. International Conference of Optometry, Riga. Iorio, P., Albergo, V., Bianco, G., Spadea, L., Rapinese, M., Gallenga, P. E., & Balestrazzi, E. (1998). Fotostimolazione visiva e ipovisione. Ottica Fisiopatologica, 3, 39–44.
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Leung, V., Wick, B., & Bedell, H. E. (1996). Multifaceted treatment of congenital nystagmus: A report of 6 cases. Optometry and Vision Science, 73, 114–124. Moncada, A. (1995). Il biofeedback visivo: Origini, ipotesi fisiologiche, applicazioni. Atti SIRV, Roma, Italy, pp. 6–11. Rotberg, M. H. (1983). Biofeedback for ophthalmologic disorders. Survey of Ophthalmology, 27, 381–386. Rowan, G. E., & Sedlacek, K. (1981). Biofeedback in the treatment of blefarospasm: A case study. American Journal of Psychiatry, 138, 1487–1489. Roxanas, M. R., Thomas, M. R., & Rapp, M. S. (1978). Biofeedback treatment of blefarospasm with spasmodic torticollis. Canadian Medical Association, 119, 48–49. Russ, K. L., Kass, M., & O’Connell, M. F. (1978). EMG biofeedback applied to patients with elevated intraocular pressure. Biofeedback and Self-Regulation, 3, 231. Trachtman, J. N. (1978). Biofeedback of accommodation to reduce myopia. A case report. American Journal of Optometry and Physiological Optics, 55, 400–406. Trachtman, J. N. (1987). Biofeedback of accomodation to reduce myopia: A review. American Journal of Optometry and Physiological Optics, 64, 639–643. Whittaker, S. G., Budd, J., & Cummings, R. W. (1988). Eccentric fixation with macular scotoma. Investigative Ophthalmology and Visual Science, 29, 268–278.