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From the McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada.
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Abstract |
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METHODS. A stochastic global motion stimulus was used, comprising spatially narrow elements with varied spatial frequency, density, contrast, and area distribution. To determine threshold, a two-alternate, forced-choice direction discrimination task was used.
RESULTS. There was a selective deficit for global motion processing that was not due to the visibility of the stimuli and was nonselective for spatial scale. The eye with the more complete recovery (acuity 20/20) from pattern deprivation in childhood exhibited the more severe global motion deficit.
DISCUSSION. The results suggest a primary extrastriate deficit in the dorsal pathway, possibly involving the middle temporal (MT) and the medial superior temporal (MST) cortical areas, that is unrelated to the acuity deficit thought to be in area V1. A similar deficit has recently been shown in strabismic amblyopia.
The cortical deficit in amblyopia is not well understood. There is good evidence from recent functional imaging that, in the case of strabismic amblyopia, a large part of the visual cortex is affected.11 Recent psychophysical studies12 have shown that global tasks are affected in a way that makes it unlikely that the problem is restricted to V1. The nature of the deficit suggests that regions of the extrastriate cortex may be primarily affected, including both the dorsal, motion-processing and the ventral, form-processing extrastriate pathways.13 In form–deprivation amblyopia a similar loss of global form and motion have been reported that is more severe in bilateral than in unilateral cases.14 15
We report on a person who had reduced vision in both eyes in childhood due to congenital cataracts that were removed at ages 5 and 6. As an adult, the patient had the acuity in one eye return to normal, although the other eye had a residual acuity loss. We used a global motion task similar to those previously used in MT-lesioned monkeys, the motion-blind patient, and strabismic amblyopes in an effort to see whether the extrastriate cortex that is thought to subserve this task is compromised. Our results showed a deficit in global motion processing that can best be explained by a deficiency at the level of the extrastriate cortex. It was worse in the eye with acuity that had recovered to normal.
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Methods |
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Subjects
This study adhered to the tenets of the Declaration of Helsinki. Participating were two normal subjects (RW, TC) and an amblyope (LS). RW was experienced in psychophysics experiments, whereas TC and LS were naive observers. The clinical characteristics of LS are described in Table 1 .
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All elements were Gabor elements and were in one of two populations: signal or noise elements. Signal elements either moved upward or downward, in a coherent direction. Noise elements moved in any random direction, presenting incoherent direction. A constant number of elements was maintained during each trial by adjusting the ratio of signal-to-noise elements. To prevent abrupt spatiotemporal transients, the stimulus area was contrast modulated over time by a cosine function at onset and offset.
Three conditions of spatial frequency were explored (Table 2) : very low frequency (VLF), medium frequency (MF), and very high frequency (VHF). To analyze the effect of spatial selectivity, it was necessary to maintain a narrow, constant bandwidth. In Fourier terms, the range of spatial frequencies that a Fourier analysis of a waveform would yield was of the same magnitude throughout the experiment. Therefore, bandwidth was kept constant, even as element size varied with each condition (Fig. 1) .
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Variables
The two main variables in the experiment were the size of the stimulus area, to observe the effects of summation, and the spatial frequency, to observe which channels were most active.
As well, to sample the more relevant region of each observer’s psychometric function, three sources of noise were varied: element density, element lifetime, and signal-to-noise ratio (SNR).
Element density, as mentioned earlier, was lower for the amblyope. Initially, the SNR was set to 100%, and element lifetime was increased until the observer began to see the stimulus better by learning what to look for. Then, the element lifetime was lowered as much as possible, resulting in the smallest possible value of 2 in normal subjects, and ranging from 5 to 20 in the amblyope. Subsequently, with element density and element lifetime thus fixed, the SNR was varied to obtain the best sample of each observer’s psychometric function and determine thresholds.
Psychophysics
Using the method of constant stimuli, the proportion of signal elements (the SNR) was varied to establish psychometric functions from which detection thresholds were estimated (Table 3) . The data were fitted with a cumulative Gaussian function by using a least-squares algorithm with the fit being weighted by the standard deviations of each empiric data point. A Monte Carlo simulation was performed by computer (MatLab; The MathWorks, Natick, MA) to estimate the threshold and its variability using the Psignifit software package.16 17 Detection thresholds were defined to be the stimulus value corresponding to 75% correct performance on the psychometric function.
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Results |
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20% of all the elements. Under these conditions, it is difficult to imagine, on statistical grounds, that the task could be accomplished by anything other than a mechanism that integrates over the sparse signal elements. Combining signal in noise with short lifetimes was intended to ensure further that to detect a globally coherent pattern, observers had to integrate over many dot motions that were individually uninformative.4 18 Thus, even if observers were able to identify individual signal elements, the motion of any one of these, owing to its short lifetime, would be too weak to support performance. Many such signal elements would have to be integrated.
Under these stringent conditions that ensure that performance is being driven by a global, integrative operation, we could not measure a reliable threshold in either of LS’s eyes. LS’s amblyopic eye could not see the VHF condition due to the patient’s contrast sensitivity deficit, as the contrast sensitivity was biased to lower sensitivity and lower spatial frequencies. Therefore, we attempted to collect data at only the VLF and MF conditions. Although these stimulus conditions fell well within the visibility range of the amblyopic eye, to be able to measure threshold performance at all, we had to increase the element lifetime to 5 for the amblyopic eye and to 20 for the better (i.e., visual acuity), fellow eye. Even this failed to allow us to get reliable data from LS’s fellow eye, even at signal strengths of 100%. The threshold of the amblyopic eye was measurable, but the signal level had to be 40%, double the norm, even under the most favorable stimulus conditions (i.e., at MF 225). Examples of these data are presented in Figure 3 for the two normal subjects and in Figure 4 for both eyes of LS.
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Discussion |
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Because we had ensured that the stimulus elements were well within the window of visibility for each eye, this deficiency was not due to visibility. That the less amblyopic eye (20/20 acuity) displayed the more severe motion deficit further reinforces this conclusion. Pattern deprivation in early life leads to reduced correctable acuity, a finding reinforced by numerous previous studies on animals19 and humans.20 21 It also leads to motion deficits,15 and the present study adds further support to the conclusion that global motion is specifically affected. The only conditions under which performance on this task was measurable were ones that invalidate any conclusion based on global integrative function. The use of long lifetimes and minimal noise favors detection by low-level local motion detectors. Unlike those in previous studies, our stimuli were not spatially broadband. We used spatially narrowband Gabors that enabled us to investigate further the global deficit at a number of different spatial scales and to ensure that, at each scale, the contrast of the stimuli was always suprathreshold for the amblyopic eye. Our results show that the deficit is, to a first approximation, independent of spatial scale (i.e., similar results at medium and low spatial frequencies). The other novel feature of the present study is that we show that area summation for global motion detection is absent in the deprived visual system, further suggesting detection by a local rather than a global mechanism. It seems that global sensitivity was so poor in this deprivation amblyope that it did not make any contribution to the task we used. Thus, there is a selective deficit for global motion in this bilateral deprivation amblyope. Of interest, one eye, although it was deprived in early life, exhibited normal visual acuity, and yet the motion deficit was greater in this eye. Not only does this suggest that the motion deficit is unrelated to the acuity loss but it also suggests that acuity and motion-processing follow different courses of development.
Deficits in global motion-processing have been reported in several clinical cases in which cortical disease is involved. A motion-blind patient who had a bilateral lesion to area MT/MST exhibited a similar inability to detect such a stimulus when it contained even a small degree of noise.22 Similarly, monkeys with lesions to area MT/MST in the dorsal extrastriate pathway also exhibited performance limited to very high signal coherence.4 The close similarity of the present results to those in these two cases suggests a processing deficit of MT/MST in the extrastriate cortex of LS.
More recently, it has been shown that strabismic amblyopes exhibit global motion deficits that are not explicable on the basis of the visibility deficit thought to reside in V1.12 Such a global deficit is not restricted to motion and has been shown also to involve spatial processing13 ; therefore, both dorsal and ventral pathways are similarly affected. Form deprivation amblyopia shows similar losses14 15 in which the motion deficit is greater when the less affected eye is stimulated. This suggests that the present case, in which the loss in the less affected eye is absolute, is not an isolated curiosity.
So far, we have considered deficient global processing of motion solely in terms of an inability to integrate signal elements, and we present evidence for this being the case for our deprivation amblyope LS. However, the segregation of signal from noise is also an important, though often overlooked, part of this task. It is not in the interest of best performance for the visual system to integrate blindly all the local motion signals contained within our stimulus. Ideally, signal should first be segregated from noise and then integrated. That we had to reduce the element density for LS to perform the task at all with the amblyopic eye is consistent with deficient segregation of signal from noise. Our more recent results suggest that segregation processes are abnormal when the more amblyopic eye of this deprivation amblyope is used and that it mimics the segregation loss that we have also revealed in the other, more common form of functional amblyopia.23
An interesting false-correspondence effect was observed in each of LS’s eyes. During a practice period, when the stimulus extent was 225 x 225 pixels, 50% to 100% SNR, and an element lifetime of five frames, LS consistently reported clearly seeing motion in the direction opposite the one presented. There are two possible explanations.
The first is element spacing and receptor size. As a signal element moves to its second location across a given distance, LS does not detect that jump as a fluid motion because she may not have receptors for that size in area V1, perhaps due to spatial undersampling at the level of the local detector.
The second is relative motion. As a set of signal elements moves in one direction, the noise elements appear to be "left behind," and they contribute to a percept of relative motion effect in the opposite direction, although they are incoherent. Because the noise elements often outnumber the signal elements, they may be more conspicuous and may be mistaken for signal.
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Footnotes |
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Submitted for publication February 22, 2005; revised April 8, 2005; accepted April 14, 2005.
Disclosure: T. Constantinescu, None; L. Schmidt, None; R. Watson, None; R.F. Hess, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. 
1734 solely to indicate this fact.
Corresponding author: Robert F. Hess, McGill Vision Research, Department of Ophthalmology, McGill University, Montreal, Quebec, Canada; robert.hess{at}mcgill.ca.
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This article has been cited by other articles:
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  A. R. Davis, J. J. Sloper, M. M. Neveu, C. R. Hogg, M. J. Morgan, and G. E. Holder Differential Changes in Color and Motion-Onset Visual Evoked Potentials from Both Eyes in Early- and Late-Onset Strabismic Amblyopia Invest. Ophthalmol. Vis. Sci., October 1, 2008; 49(10): 4418 - 4426. [Abstract] [Full Text] [PDF]
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