- Email: [email protected]
Plasticity in human blindsight
OO42-6989/82/091
Vision Rrs. Vol. 22, pp. I199 to 1203, 1982 Printed in Great Britain
l99-05W3.00/0
Pergamon Press Ltd
PLASTICITY
IN HUMAN
BLINDSIGHT
BRUCE BRIDGEMAN and DAVID STAGGS
Psychology Board of Studies, Clark Kerr Hall, University of California, Santa Cruz, Santa Cruz, CA 95064, U.S.A. (Recked
29 Octohrr
1981; in rrvised ,form 4 February 1982)
subject with an unusually large cortical scotoma, leaving a 9” hemifield of vision in each improvement with practice in pointing to an oscillating target positioned within the scotoma. The practice effect transferred to low-contrast targets and to stationary ones, though oscillating targets were always located more accurately. Following practice. the subject reported improved confidence in visual orientation. Results are interpreted in the context of the contrast between the functions of two visual systems (subcortical and cortical) present in normal humans.
Abstract-A
eye. showed
INTRODUCTION damage to the striate cortex in man causes complete lack of visual experience in the topographic visual field of the affected area, it is now clear that some visual function remains in that area. A patient with a striate cortex lesion cannot report the presence of a target in the scotoma, but he can direct his gaze to it (Poppel et al., 1973) or point to it (Weiskrantz et al., 1974; Perenin and Jeannerod, 1978) if forced to guess the target’s position; pointing or looking are not as accurate as they would be to targets in the intact fields. Similar results follow striate cortex lesions in monkeys, where lasting discrimination deficits are accompanied by accurate reaching behavior (Humphrey and Weiskrantz, 1967; Weiskrantz et al., 1977; Feinberg et al., 1978). Weiskrantz has labeled this ability “blindsight,” because visually guided behavior coexists with lack of visual experience. Several questions remain about the characterization of blindsight in humans. Most of the patients in the above studies had large remaining visual fields, frequently consituting half or more of the normal fields. The extent of damage to extrastriate cortex is less well documented, but in most cases it was probably equal to or less than striate damage. Thus it is possible that the remaining undamaged occipital cortical systems can still participate, perhaps in a nonspecific way, in mediating some abilities. Does residual visual function remain in cases involving extensive striate and extrastriate damage? A second question addresses the possible extent of plasticity or learning in the subcortical visual system. Learning is classically assigned to the cortex more than to subcortical centers, though there is some evidence of plasticity in the reaching responses of striate lesioned monkey (Weiskrantz et al., 1977; Feinberg et al., 1978) and in saccadic eye movement response to stimuli in cortical scotomata in man (Zihl, 1980). If the same plasticity exists for pointing responses in man, which are less closely tied to the superior colli-
Though
culus (SC) than are eye movements, the generality of subcortical plasticity would be expanded to include somatic motor systems.
METHODS Subject
The opportunity to address these questions arose with the availability of a subject who was exceptionally well suited to studies of blindsight. As a result of a traffic accident he sustained a blow to the occipital pole resulting in bilateral subdural hematomas over the occipital lobe. He regained consciousness with apparent cortical blindness, but regained use of right hemifields about 9” in radius in each eye, with some macular sparing. Trauma were confirmed by X-ray tomography and by a clinical electroencephalogram, showing normal short-latency visual evoked potentials but loss of long-latency potentials. The pattern is consistent with a diagnosis of damage to occipital cortex. In man, the extrastriate visual areas (18 and 19) largely overlie the striate area (area 17), which is protected in the calcarine sulcus. The nature of the accident (mechanical rather than cerebrovascular) means that extensive damage to extrastriate visual cortex occurred in addition to the striate cortex lesion demonstrated with perimetry. The subject’s scotoma has remained stable for 4yr following his initial clinical examination, as shown by the close match between the original perimetry and the perimetry we performed in our laboratory at the start of our experiments (Fig. 1). Our perimetry was completed before the clinical perimetry records were obtained. Fortunately, our subject remains alert and intelligent, and was well motivated and interested in the results of the study. The exceptionally large scotomas are the only remaining clinical sign of brain damage. Such subjects are rare; we have not encountered another in our limited population.
1199
1200
BRUCE BRIDGEMAN and DAVID STAGS
1976
1980
Fig. I. Visual perimetry shortly after brain injury (1976) and before beginning the current experiments (1980). The hatched area represents the remaining visual field in the right eye. The scotoma in the left eye is similar in size and shape to the one illustrated here.
Apparatus
Procedure
The subject sat before a uniform white hemicylindrical screen 130 cm high and 59 cm in radius. During experiments he immobilized his head at the center of curvature of the screen by biting a dental impression molded onto a fixed bar, resulting in a clear 180” field equidistant from the exposed eye. An infrared monitor (Bahill et al., 197.5) and a chart recorder were used to record horizontal movements of the right eye at a resolution of 20’ and a l/bamplitude bandwidth of O-65 Hz. Response latency and position were also recorded on the chart recorder. The visual stimulus was a triangular patch of white light 2” wide and 3” high, projected from a tungsten halogen lamp onto the screen along the horizontal plane level with the fixation point. Three image conditions were used in the experiment. (1) In the moving image condition, the triangular target moved horizontally in sinusoidal motion a distance of 2” peak to peak at 5 Hz. (2) The stationary condition used the same image without movement. (3) The control condition was the same in execution as conditions one and two. However, a drape was noiselessly lowered in front of the shutter before the start of the trial to obscure the target. The image was presented randomly in one of eight positions (left 15, 30”, 45”; center; right 5”, 15”, 30”, 45”). Of these positions, only the center and 5” right positions were reported as visible. These two positions allow a comparison of error in pointing to visible targets with error in pointing within the scotoma, Three lighting conditions were used: screen luminantes and contrasts were 52.70 cd/m* (0.66 log units) in the bright condition, l.l34cd/m* (3.01 log units) in the dim condition, or 0.018 cd/m2 (3.87 log units) in the dark condition. Stray light, assessed with a digital photometer with its telescope head aimed at the center of the screen, did not reach measurable levels with four significant figures of accuracy when the stimulus was at 15” eccentricity.
Before each group of trials, the subject’s left eye was covered and the eye monitor calibrated to equal gains for 5” eye movements left and right of center. A second calibration at the end of each trial block was compared to the starting CaIibration. At the start of a trial, the subject opened his right eye and fixated on a point at the center of the screen. Once steady fixation was confirmed in the eye position record, a shutter was opened to expose the target. After hearing the shutter open, the subject would swing the tip of a pointer along the base of the screen to indicate the position below the image, while maintaining eye fixation. A baffle prevented the subject from seeing either the pointer or his hand. Response was measured as the voltage across a potentiometer attached to the axis of the pointer. When satisfied with the judgment, the subject would press a button to record the pointer position on a computer, return the pointer to the left edge of the screen, and close his eyes. Data were discarded and the trial repeated in trials where eye movements were greater than 2”. In most trials, eye movements were less than 0.5”. The experiments totaled 627 trials performed over 36 calendar days. RESULTS
Perimetry (Fig. 1) was performed before any of the experimental sessions. When asked to judge the appearance of a target in the retinal periphery, the subject frequently made saccades into the blind field, even when asked not to do so. Only after practice with feedback about saccades were these eye movements eliminated, a result which shows the importance of eye movement monitoring in subjects with large scotomas. Spontaneous fixation patterns included more frequent saccades than found in normal subjects, with many movements of small magnitude. The saccades had normal dynamics,
Plasticity in human blindsight
01
I
I
I
I
I
2
3
4
5
Trial
I 6
I 7
block
Fig. 2. Change in variance with training. averaged across all stimulus positions. Each trial block was run on a different day. N > 30 trials/block. Oscillating target, contrast 3.01 log units. Triangles: blind fields. Circles: sighted fields. Solid lines show least-squares linear regressions.
The subject showed ability to point to unseen oscillating targets at all light intensities, though errors were large, Mean errors for all trials of pointing into the blind field were 9.1” for the bright condition, 7.6” for the dim condition, and 6.7” for the dark condition (N > 30 trials for each condition). Thus, pointing accuracy increased slightly as contrast increased, but remained high even for very high-contrast stimuli. Mean errors were increased by occasional trials where the subject pointed to a position symmetrically opposite the target position. These reversal responses disappeared with further practice, even though the subject received no feedback about errors during the trials and was never told of the reversal phenomenon.
1201
targets until the number of trials in the oscillating and fixed conditions was about equal. Accuracy in pointing to fixed targets was always less than accuracy with oscillating targets at the same stage in training: sometimes the subject remarked that he was inaccurate after the pointing estimate to the fixed target had been made and the target extinguished. A possible explanation for this realization is that superior colliculus receptive fields are sensitive to moving stimuli, but are responsive to fixed stimuli only at light onset and offset. In fixed-stimulus trials our subject would have received some position information at target onset, used this information for pointing, and received more information at offset after pointing had been completed. LBW contrast. Practice in the high-contrast “dim” background condition transferred to the low-contrast “bright” condition, as shown in Fig. 4. This graph shows median error for each position on each of the last three days of pointing trials. Other results. Control trials (Fig. 5) show a tendency to point about 30” to the left in the absence of visual information. This is in the direction of the blind hemifield, and may reflect the subject’s best guess if no sign of the stimulus is present. Many of the points in this figure are close to those in Fig. 3, where the initial estimations of position were all close to 30” left except for the visible points and the 45” right point. Comparison of the initial blindsight curve with the control curves of Fig. 5 shows that the initial ability was even more limited than it first appeared, and shows more clearly the improvement with training. Response latencies were much longer for pointing than for the saccadic eye movements into the blind field reported by Zihl (1980) because the mechanical
Training Oscikzting target. The pointing task was repeated in the dim condition for several days, resulting in a gradual reduction of both mean error and variance, the two independent measures of pointing accuracy. Figure 2 shows the decrease in variability of the pointing during 243 trials. The decrease in standard deviations across trial blocks was statistically significant (r = 067; P < 0.05) for the scotoma positions, while there was no significant change for the visible positions (r = 0.43; NS). A comparison of mean errors at each target position on the first and last trial blocks (Fig. 3) shows that performance improved more in the blind fields than in the intact fields (0’ and 5”) because of a ceiling effect: initial errors were already very small in the intact fields. Mean error in the scotoma decreased to about one-third of its original value after these trials. Pointing in the seventh session was more accurate than in the first for every position except 30” left, where the differences were insignificant, Fixed target. After completion of the trials illustated in Fig. 2, the subject practiced pointing to fixed V.R. 22:9--n
1 45
30
14
05
15
30
45
Stimulus position, degrees Fig. 3. Pointing to moving targets in the first trial block (open circles) and after 205 trials (open triangles). Only the 0” and 5” positions were reported as seen by the subject. Diagonal solid line represents accurate response. Targets were presented in random order, and points give median responses in this and subsequent figures to prevent a few grossly inaccurate responses from skewing the data.
BRUCE BRIDGEMAN and DAVID STAGGS
1202
45
30
15
05
Stimulus position,
15
30
45
degrees
Fig. 4. Pointing to moving targest under the low-contrast condition (0.66 log units) on the final three days of the experiment, after completion of the trials illustrated in Fig. 2. Squares:
day 12; triangles:
day 13; circles:
day 14.
pointing system took some time to operate. The mean latency of our subject in pointing into the blind field was 3.60s while the latency in the intact field was 2.78 s. Latency during control trials was 3.29 s. Latenties varied from day to day while the pattern of relative latencies remained consistent. Differences between pointing to the blind field and to the intact field may reflect the greater confidence and lack of hesitation in pointing to the intact field: the subject remarked that pointing in this field was “easier.” Zihl (1980) reported the opposite bias in eye movement latencies to blind vs intact fields: the greater possibility of cognitive intrusions into the pointing task probably explains the dominance of these factors in our data. The lower latency for stimulus-off control trials than for blind trials may be an artifact of the physical arrangement of the apparatus, for the pointer required less movement for responses on the left side of the screen where most of the control points were made. Following the extensive practice with simple targets, the subject reported an improved ability to recognize movement within the scotomas, giving him an ability to sense approaching objects when walking and reducing his anxiety in crowds. In summary, we have confirmed the existence of “blindsight” in a subject with exceptionally large scotomata, and have shown in addition that the ability can be improved with specific training.
calibration than of discrimination or episodic learning in which the cortical system dominates. Thus it is reasonable that subcortical centers could mediate plasticity in our simple task. Our success at training blindsight where others have failed is probably due to several circumstances. First, our subject was younger (27) than most subjects in blindsight experiments, and was not suffering from the vascular diseases which frequently cause strokes and resulting cortical scotoma. Second, though his scotomata are exceptionally large, the remainder of our subject’s brain is in good condition, as shown by his above-average general intelligence and success in undergraduate studies. The success of Cowey (1967) and Humphrey and Weiskrantz (1967) at training blindsight in monkeys may be due to these variables: the monkeys are typically young and in good condition. Our experimental design was intended to maximize the possibility of learning. During training the subject saw oscillating targets at high contrast. Goldberg and Wurtz (1977) showed that blindsight is effective only at high contrasts; cortically lesioned monkeys could saccade to targets at 3.2 log units contrast but not at 1.0 log units. Goldberg and Wurtz (1977) also show that most superior colliculus cells respond to movement only at 20’ sect ’ or more, the mean velocity for our target oscillation. Perenin and Jeannerod (1978) found no significant human sensitivity to target movement in a cortical scotoma. but their targets moved at only 4’ sY’. Other characteristics of the experiment which may have facilitated development of blindsight include use of a very large homogeneous screen. lack of time pressure. a l-dimensional task, and training distributed over many days. Our subject’s improvement suggests the possibility of a systematic therapy for scotoma patients who are otherwise in good condition. Usefulness of stimuli falling on cortical scotomata does not improve in either monkeys or humans without formal training in
DlSCUSSlON
The improvement of blindsight raises the issue of plasticity in subcortical centers, for open-loop pointing tasks are handled by the subcortical “motor” or ambient visual system even in normal humans (Bridgeman et al., 1979; Bridgeman et al., 1981). Improved performance in a task where the response is isomorphic with the stimulus has more the nature of a
45
30
15
0 5
I5
30
45
Stimulus position, degrees
Fig. 5. Pointing in the control condition, with no target projected on the screen. Symbols as in Fig. 4.
Plasticity a simplified
in human
but highly structured environment, where information demands on the subject are minimized so that what was complex and chaotic input gradually comes to indicate visual location. An alternative explanation to subcortical processing for our subject’s pointing ability is that signals could travel laterally in the intact retina from the area projecting to the scotomic field into the central intact field. The two phenomena mediating such lateral spread of signals are the McIlwain effect (McIlwain, 1964) and the “Far-out Jerk Effect” (Breitmeyer and Valberg, 1979). Both mechanisms, however, require a large moving target to be effective, while our target was small and could be located (though with diminished accuracy) even when not oscillating. There remains a possibility that the subject learned to use stray light falling within the intact field rather than information from the scotomic field. Stray light can come from two sources: light reflected from the stimulus onto the central part of the screen, and light scattered within the eye. Direct photometric measurements showed that the screen luminance was not detectably different to four significant figures in target-on vs target-off conditions. Light scatter within the eye was assessed using the data of Flamant (1955) as reviewed by Westheimer (1972). In our worst case, the 15” condition ipsilateral to the intact hemifield, the nearest edge of our stimulus is 5” from the edge of the intact field, resulting in light scatter -5.1 log units as intense as the stimulus. Assuming the width of the sighted field to be lo”, the attenuation on the other side of the field is -5.8 log units. This results in a gradient across the sighted field (ratio of most intense to least intense light) of -5.2 log units or 1 part in 158,000 in the high-contrast condition (neglecting reduction of the gradient due to the uniform background illumination). In the low-contrast, bright-background condition (Fig. 2) the gradient drops to - 5.86 log units or 1 part in 724,000. Several empirical controls reinforce the theoretical conclusion that stray light was negligible. First, a stray-light interpretation predicts better performance for less eccentric targets, since scatter falls off monotonically with eccentricity, but in our observations there was no consistent trend in the relationship between variance and eccentricity. Second, performance was consistently superior with oscillating targets, even though position was inherently more ambiguous in this condition because the target oscillated in the plane of the response measure. Third, the subject reported receiving more information about position at the off-transient with fixed targets (but not with oscillating ones), and finally, the subject could not discriminate control trials from experimental trials. All of these characteristics are consistent with the interpretation that position information was being mediated in the superior colliculus and other subcor-
1203
blindsight
tical centers, reinforcing human blindsight.
our finding
Acknowledgements-Supported BNS-7906858. We thank Professor technical advice.
by Gerald
of plasticity
in
Grant NSF Westheimer for
REFERENCES
Bahill A., Clark M. and Stark L. (1975) Dynamic overshoot in saccadic eye movements is caused by neurological control signal reversals. Exp. Neural. 48, 95112. Breitmeyer B. and Valberg A. (1980) Local fovea1 inhibitory effects of global peripheral excitation. Science 203, 463465. Bridgeman B., Kirch M. and Sperling A. (1980) Segregation of cognitive and motor aspects of visual function using induced motion. Percept. Psychophys. 29, 336-342. Bridgeman B., Lewis S., Heit G. and Nagle M. (1979) The relationship between cognitive and motor-oriented systems of visual position perception. J. Expl Psycho/.. Hum Percept. Perform 5, 692-700. Butter C. M., Weinstein C., Bender D. B. and Gross C. G. (1978) Localization and detection of visual stimuli following superior colliculus lesions in rhesus monkeys. Brain Res. 156, 33-49. Cowey A. (1967) Perimetric study of field defects in monkeys after cortical and retinal ablation. Q. JI. exp. Psycho/. 19, 232-245. Feinberg T. E., Pasik T. and Pasik P. (1978) Extrageniculostriate vision in the monkey. VII. Visually guided accurate reaching behavior. Bruin Res. 152, 422-428. Flamant F. (1955) Etude de la repartition de lumitre dans I’image retinenne dune fente. Rec. Opt. 34, 433459. Goldberg M. E. and Wurtz R. H. (1972) Activity of superior colliculus in behaving monkeys. I. Visual receptive fields of single neurons. J. Neurophysio/. 35. 542-559. Humphrey N. K. and Weiskrantz L. (1967) Vision in monkeys after removal of the striate cortex. Nature 215, 595-597. McIlwain J. (1964) Receptive fields of optic tract axons and lateral geniculuate cells: peripheral extent and barbiturate sensitivity. J. Neurophysiol. 27, 1154-I 173. Perenin M. T. and Jeannerod M. (1975) Residual vision in cortically blind hemifields. Neuropsychologia 13, l-7. Poppel E., Held R. and Frost D. (1973) Residual visual function after brain wounds involving the central visual pathways. Nature 243, 295-296. Schneider G. E. (1967) Contrasting visuomotor functions of tectum and cortex in golden hamster. Psq’chol. Forsch. 31, 52-68. Trevarthen C. B. (1968) Two mechanisms of vision in primates. Psycho/. Forsch. 31, 299-337. Weiskrantz L., Cowey A. and Passingham C. (1977) Spatial responses to brief stimuli by monkeys with striate cortex ablations. Brain 100, 655-670. Weiskrantz L., Warrington E. K., Sanders M. D. and Marshall J. (1974) Visual capacity in the hemianopic field following a restricted occipital ablation. Brain 97, 709-728. Westheimer G. (1972) Optical properties of vertebrate eyes. In Handbook of Sensory Physiology, Vol. VII/ 2: Physiology of Photoreceptor Organs (Edited by Fuortes M.), pp. 4499482. Springer. Berlin. Zihl J. (1980) “Blindsight”: improvement of visually guided eye movements by systematic practice in patients with cerebral blindness. Neuropsychologia 18, 71-77.
Vision Rrs. Vol. 22, pp. I199 to 1203, 1982 Printed in Great Britain
l99-05W3.00/0
Pergamon Press Ltd
PLASTICITY
IN HUMAN
BLINDSIGHT
BRUCE BRIDGEMAN and DAVID STAGGS
Psychology Board of Studies, Clark Kerr Hall, University of California, Santa Cruz, Santa Cruz, CA 95064, U.S.A. (Recked
29 Octohrr
1981; in rrvised ,form 4 February 1982)
subject with an unusually large cortical scotoma, leaving a 9” hemifield of vision in each improvement with practice in pointing to an oscillating target positioned within the scotoma. The practice effect transferred to low-contrast targets and to stationary ones, though oscillating targets were always located more accurately. Following practice. the subject reported improved confidence in visual orientation. Results are interpreted in the context of the contrast between the functions of two visual systems (subcortical and cortical) present in normal humans.
Abstract-A
eye. showed
INTRODUCTION damage to the striate cortex in man causes complete lack of visual experience in the topographic visual field of the affected area, it is now clear that some visual function remains in that area. A patient with a striate cortex lesion cannot report the presence of a target in the scotoma, but he can direct his gaze to it (Poppel et al., 1973) or point to it (Weiskrantz et al., 1974; Perenin and Jeannerod, 1978) if forced to guess the target’s position; pointing or looking are not as accurate as they would be to targets in the intact fields. Similar results follow striate cortex lesions in monkeys, where lasting discrimination deficits are accompanied by accurate reaching behavior (Humphrey and Weiskrantz, 1967; Weiskrantz et al., 1977; Feinberg et al., 1978). Weiskrantz has labeled this ability “blindsight,” because visually guided behavior coexists with lack of visual experience. Several questions remain about the characterization of blindsight in humans. Most of the patients in the above studies had large remaining visual fields, frequently consituting half or more of the normal fields. The extent of damage to extrastriate cortex is less well documented, but in most cases it was probably equal to or less than striate damage. Thus it is possible that the remaining undamaged occipital cortical systems can still participate, perhaps in a nonspecific way, in mediating some abilities. Does residual visual function remain in cases involving extensive striate and extrastriate damage? A second question addresses the possible extent of plasticity or learning in the subcortical visual system. Learning is classically assigned to the cortex more than to subcortical centers, though there is some evidence of plasticity in the reaching responses of striate lesioned monkey (Weiskrantz et al., 1977; Feinberg et al., 1978) and in saccadic eye movement response to stimuli in cortical scotomata in man (Zihl, 1980). If the same plasticity exists for pointing responses in man, which are less closely tied to the superior colli-
Though
culus (SC) than are eye movements, the generality of subcortical plasticity would be expanded to include somatic motor systems.
METHODS Subject
The opportunity to address these questions arose with the availability of a subject who was exceptionally well suited to studies of blindsight. As a result of a traffic accident he sustained a blow to the occipital pole resulting in bilateral subdural hematomas over the occipital lobe. He regained consciousness with apparent cortical blindness, but regained use of right hemifields about 9” in radius in each eye, with some macular sparing. Trauma were confirmed by X-ray tomography and by a clinical electroencephalogram, showing normal short-latency visual evoked potentials but loss of long-latency potentials. The pattern is consistent with a diagnosis of damage to occipital cortex. In man, the extrastriate visual areas (18 and 19) largely overlie the striate area (area 17), which is protected in the calcarine sulcus. The nature of the accident (mechanical rather than cerebrovascular) means that extensive damage to extrastriate visual cortex occurred in addition to the striate cortex lesion demonstrated with perimetry. The subject’s scotoma has remained stable for 4yr following his initial clinical examination, as shown by the close match between the original perimetry and the perimetry we performed in our laboratory at the start of our experiments (Fig. 1). Our perimetry was completed before the clinical perimetry records were obtained. Fortunately, our subject remains alert and intelligent, and was well motivated and interested in the results of the study. The exceptionally large scotomas are the only remaining clinical sign of brain damage. Such subjects are rare; we have not encountered another in our limited population.
1199
1200
BRUCE BRIDGEMAN and DAVID STAGS
1976
1980
Fig. I. Visual perimetry shortly after brain injury (1976) and before beginning the current experiments (1980). The hatched area represents the remaining visual field in the right eye. The scotoma in the left eye is similar in size and shape to the one illustrated here.
Apparatus
Procedure
The subject sat before a uniform white hemicylindrical screen 130 cm high and 59 cm in radius. During experiments he immobilized his head at the center of curvature of the screen by biting a dental impression molded onto a fixed bar, resulting in a clear 180” field equidistant from the exposed eye. An infrared monitor (Bahill et al., 197.5) and a chart recorder were used to record horizontal movements of the right eye at a resolution of 20’ and a l/bamplitude bandwidth of O-65 Hz. Response latency and position were also recorded on the chart recorder. The visual stimulus was a triangular patch of white light 2” wide and 3” high, projected from a tungsten halogen lamp onto the screen along the horizontal plane level with the fixation point. Three image conditions were used in the experiment. (1) In the moving image condition, the triangular target moved horizontally in sinusoidal motion a distance of 2” peak to peak at 5 Hz. (2) The stationary condition used the same image without movement. (3) The control condition was the same in execution as conditions one and two. However, a drape was noiselessly lowered in front of the shutter before the start of the trial to obscure the target. The image was presented randomly in one of eight positions (left 15, 30”, 45”; center; right 5”, 15”, 30”, 45”). Of these positions, only the center and 5” right positions were reported as visible. These two positions allow a comparison of error in pointing to visible targets with error in pointing within the scotoma, Three lighting conditions were used: screen luminantes and contrasts were 52.70 cd/m* (0.66 log units) in the bright condition, l.l34cd/m* (3.01 log units) in the dim condition, or 0.018 cd/m2 (3.87 log units) in the dark condition. Stray light, assessed with a digital photometer with its telescope head aimed at the center of the screen, did not reach measurable levels with four significant figures of accuracy when the stimulus was at 15” eccentricity.
Before each group of trials, the subject’s left eye was covered and the eye monitor calibrated to equal gains for 5” eye movements left and right of center. A second calibration at the end of each trial block was compared to the starting CaIibration. At the start of a trial, the subject opened his right eye and fixated on a point at the center of the screen. Once steady fixation was confirmed in the eye position record, a shutter was opened to expose the target. After hearing the shutter open, the subject would swing the tip of a pointer along the base of the screen to indicate the position below the image, while maintaining eye fixation. A baffle prevented the subject from seeing either the pointer or his hand. Response was measured as the voltage across a potentiometer attached to the axis of the pointer. When satisfied with the judgment, the subject would press a button to record the pointer position on a computer, return the pointer to the left edge of the screen, and close his eyes. Data were discarded and the trial repeated in trials where eye movements were greater than 2”. In most trials, eye movements were less than 0.5”. The experiments totaled 627 trials performed over 36 calendar days. RESULTS
Perimetry (Fig. 1) was performed before any of the experimental sessions. When asked to judge the appearance of a target in the retinal periphery, the subject frequently made saccades into the blind field, even when asked not to do so. Only after practice with feedback about saccades were these eye movements eliminated, a result which shows the importance of eye movement monitoring in subjects with large scotomas. Spontaneous fixation patterns included more frequent saccades than found in normal subjects, with many movements of small magnitude. The saccades had normal dynamics,
Plasticity in human blindsight
01
I
I
I
I
I
2
3
4
5
Trial
I 6
I 7
block
Fig. 2. Change in variance with training. averaged across all stimulus positions. Each trial block was run on a different day. N > 30 trials/block. Oscillating target, contrast 3.01 log units. Triangles: blind fields. Circles: sighted fields. Solid lines show least-squares linear regressions.
The subject showed ability to point to unseen oscillating targets at all light intensities, though errors were large, Mean errors for all trials of pointing into the blind field were 9.1” for the bright condition, 7.6” for the dim condition, and 6.7” for the dark condition (N > 30 trials for each condition). Thus, pointing accuracy increased slightly as contrast increased, but remained high even for very high-contrast stimuli. Mean errors were increased by occasional trials where the subject pointed to a position symmetrically opposite the target position. These reversal responses disappeared with further practice, even though the subject received no feedback about errors during the trials and was never told of the reversal phenomenon.
1201
targets until the number of trials in the oscillating and fixed conditions was about equal. Accuracy in pointing to fixed targets was always less than accuracy with oscillating targets at the same stage in training: sometimes the subject remarked that he was inaccurate after the pointing estimate to the fixed target had been made and the target extinguished. A possible explanation for this realization is that superior colliculus receptive fields are sensitive to moving stimuli, but are responsive to fixed stimuli only at light onset and offset. In fixed-stimulus trials our subject would have received some position information at target onset, used this information for pointing, and received more information at offset after pointing had been completed. LBW contrast. Practice in the high-contrast “dim” background condition transferred to the low-contrast “bright” condition, as shown in Fig. 4. This graph shows median error for each position on each of the last three days of pointing trials. Other results. Control trials (Fig. 5) show a tendency to point about 30” to the left in the absence of visual information. This is in the direction of the blind hemifield, and may reflect the subject’s best guess if no sign of the stimulus is present. Many of the points in this figure are close to those in Fig. 3, where the initial estimations of position were all close to 30” left except for the visible points and the 45” right point. Comparison of the initial blindsight curve with the control curves of Fig. 5 shows that the initial ability was even more limited than it first appeared, and shows more clearly the improvement with training. Response latencies were much longer for pointing than for the saccadic eye movements into the blind field reported by Zihl (1980) because the mechanical
Training Oscikzting target. The pointing task was repeated in the dim condition for several days, resulting in a gradual reduction of both mean error and variance, the two independent measures of pointing accuracy. Figure 2 shows the decrease in variability of the pointing during 243 trials. The decrease in standard deviations across trial blocks was statistically significant (r = 067; P < 0.05) for the scotoma positions, while there was no significant change for the visible positions (r = 0.43; NS). A comparison of mean errors at each target position on the first and last trial blocks (Fig. 3) shows that performance improved more in the blind fields than in the intact fields (0’ and 5”) because of a ceiling effect: initial errors were already very small in the intact fields. Mean error in the scotoma decreased to about one-third of its original value after these trials. Pointing in the seventh session was more accurate than in the first for every position except 30” left, where the differences were insignificant, Fixed target. After completion of the trials illustated in Fig. 2, the subject practiced pointing to fixed V.R. 22:9--n
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Stimulus position, degrees Fig. 3. Pointing to moving targets in the first trial block (open circles) and after 205 trials (open triangles). Only the 0” and 5” positions were reported as seen by the subject. Diagonal solid line represents accurate response. Targets were presented in random order, and points give median responses in this and subsequent figures to prevent a few grossly inaccurate responses from skewing the data.
BRUCE BRIDGEMAN and DAVID STAGGS
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Fig. 4. Pointing to moving targest under the low-contrast condition (0.66 log units) on the final three days of the experiment, after completion of the trials illustrated in Fig. 2. Squares:
day 12; triangles:
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pointing system took some time to operate. The mean latency of our subject in pointing into the blind field was 3.60s while the latency in the intact field was 2.78 s. Latency during control trials was 3.29 s. Latenties varied from day to day while the pattern of relative latencies remained consistent. Differences between pointing to the blind field and to the intact field may reflect the greater confidence and lack of hesitation in pointing to the intact field: the subject remarked that pointing in this field was “easier.” Zihl (1980) reported the opposite bias in eye movement latencies to blind vs intact fields: the greater possibility of cognitive intrusions into the pointing task probably explains the dominance of these factors in our data. The lower latency for stimulus-off control trials than for blind trials may be an artifact of the physical arrangement of the apparatus, for the pointer required less movement for responses on the left side of the screen where most of the control points were made. Following the extensive practice with simple targets, the subject reported an improved ability to recognize movement within the scotomas, giving him an ability to sense approaching objects when walking and reducing his anxiety in crowds. In summary, we have confirmed the existence of “blindsight” in a subject with exceptionally large scotomata, and have shown in addition that the ability can be improved with specific training.
calibration than of discrimination or episodic learning in which the cortical system dominates. Thus it is reasonable that subcortical centers could mediate plasticity in our simple task. Our success at training blindsight where others have failed is probably due to several circumstances. First, our subject was younger (27) than most subjects in blindsight experiments, and was not suffering from the vascular diseases which frequently cause strokes and resulting cortical scotoma. Second, though his scotomata are exceptionally large, the remainder of our subject’s brain is in good condition, as shown by his above-average general intelligence and success in undergraduate studies. The success of Cowey (1967) and Humphrey and Weiskrantz (1967) at training blindsight in monkeys may be due to these variables: the monkeys are typically young and in good condition. Our experimental design was intended to maximize the possibility of learning. During training the subject saw oscillating targets at high contrast. Goldberg and Wurtz (1977) showed that blindsight is effective only at high contrasts; cortically lesioned monkeys could saccade to targets at 3.2 log units contrast but not at 1.0 log units. Goldberg and Wurtz (1977) also show that most superior colliculus cells respond to movement only at 20’ sect ’ or more, the mean velocity for our target oscillation. Perenin and Jeannerod (1978) found no significant human sensitivity to target movement in a cortical scotoma. but their targets moved at only 4’ sY’. Other characteristics of the experiment which may have facilitated development of blindsight include use of a very large homogeneous screen. lack of time pressure. a l-dimensional task, and training distributed over many days. Our subject’s improvement suggests the possibility of a systematic therapy for scotoma patients who are otherwise in good condition. Usefulness of stimuli falling on cortical scotomata does not improve in either monkeys or humans without formal training in
DlSCUSSlON
The improvement of blindsight raises the issue of plasticity in subcortical centers, for open-loop pointing tasks are handled by the subcortical “motor” or ambient visual system even in normal humans (Bridgeman et al., 1979; Bridgeman et al., 1981). Improved performance in a task where the response is isomorphic with the stimulus has more the nature of a
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Fig. 5. Pointing in the control condition, with no target projected on the screen. Symbols as in Fig. 4.
Plasticity a simplified
in human
but highly structured environment, where information demands on the subject are minimized so that what was complex and chaotic input gradually comes to indicate visual location. An alternative explanation to subcortical processing for our subject’s pointing ability is that signals could travel laterally in the intact retina from the area projecting to the scotomic field into the central intact field. The two phenomena mediating such lateral spread of signals are the McIlwain effect (McIlwain, 1964) and the “Far-out Jerk Effect” (Breitmeyer and Valberg, 1979). Both mechanisms, however, require a large moving target to be effective, while our target was small and could be located (though with diminished accuracy) even when not oscillating. There remains a possibility that the subject learned to use stray light falling within the intact field rather than information from the scotomic field. Stray light can come from two sources: light reflected from the stimulus onto the central part of the screen, and light scattered within the eye. Direct photometric measurements showed that the screen luminance was not detectably different to four significant figures in target-on vs target-off conditions. Light scatter within the eye was assessed using the data of Flamant (1955) as reviewed by Westheimer (1972). In our worst case, the 15” condition ipsilateral to the intact hemifield, the nearest edge of our stimulus is 5” from the edge of the intact field, resulting in light scatter -5.1 log units as intense as the stimulus. Assuming the width of the sighted field to be lo”, the attenuation on the other side of the field is -5.8 log units. This results in a gradient across the sighted field (ratio of most intense to least intense light) of -5.2 log units or 1 part in 158,000 in the high-contrast condition (neglecting reduction of the gradient due to the uniform background illumination). In the low-contrast, bright-background condition (Fig. 2) the gradient drops to - 5.86 log units or 1 part in 724,000. Several empirical controls reinforce the theoretical conclusion that stray light was negligible. First, a stray-light interpretation predicts better performance for less eccentric targets, since scatter falls off monotonically with eccentricity, but in our observations there was no consistent trend in the relationship between variance and eccentricity. Second, performance was consistently superior with oscillating targets, even though position was inherently more ambiguous in this condition because the target oscillated in the plane of the response measure. Third, the subject reported receiving more information about position at the off-transient with fixed targets (but not with oscillating ones), and finally, the subject could not discriminate control trials from experimental trials. All of these characteristics are consistent with the interpretation that position information was being mediated in the superior colliculus and other subcor-
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tical centers, reinforcing human blindsight.
our finding
Acknowledgements-Supported BNS-7906858. We thank Professor technical advice.
by Gerald
of plasticity
in
Grant NSF Westheimer for
REFERENCES
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