Perceptual and Motor Skills, 1992, 75, 648-650. O Perceptual and Motor Skills 1992
STILL N O EVIDENCE FOR A PHOTORECEPTOR-LEVEL ABNORMALITY I N DYSLEXIA ' AND
G . W. STUART Australian National University
W. J. LOVEGROVE Wollongong Universit)l
Summary.-In reply to Grosser and Spafford's (1992) defence of their theor! that rhere is a photoreceptor-level abnormality in dyslexia we argue that (1) their original experiments d o not cap rod functions, ( 2 ) the theory fails at the quantitative level, and (3) the proposition that rod inputs generate transient responses is false.
Grosser and Spafford (1992) have recently replied to criticisms made by us (Stuart & Lovegrove, 1992) of their claim that dyslexics are more sensitive to peripheral colour contrast, and less sensitive to luminance contrast, or periphery. Very briefly, we because they have a cone-rich, r ~ d - ~ o retinal argued that at the light levels used in their experiments, cone responses should dominate both color and luminance contrast detection and attributed the abnormalities in dyslexic vision to a postreceptoral deficit in the magnocellular layers of the lateral geniculate nucleus, for which there is now direct anatomical evidence (Livingstone, Rosen, Drislane, & Galaburda, 1991). This new attempt to justify their theory of a photoreceptor level abnormality suffers from three major deficiencies: ( I ) They do not challenge the findings of Shapley and Enroth-Cugell (1984) and Koenderink, Bournan, Bueno de Mesquita, and Slappendel (1978) who showed that cones, not rods, determine luminance contrast sensitivity above purely scotopic light levels and that this is true at all eccentricities. This omission is serious, because it means that their empirical work cannot convincingly be tied to rod function. (2) They d o not directly address quantitative evidence which shows that peripheral visual sensitivity cannot be explained in terms of photoreceptor densities, even in normal observers (e.g., MuIIen, 1991; Thibos, Cheney, & Walsh, 1987). However, in a tacit admission of the importance of postreceptoral mechanisms, they argue that it is photoreceptor densities which determine the densities of different types of ganglion cells. Developmentally, this cannot be the case, because ganglion cells develop before the photoreceptors (Curcio & Hendrickson, 1991). What they fail to appreciate is that i t is the sampling of the retinal mosaic by visual neurons which provides the "bottleneck" in visual processing, because in the periphery all major types of ganglion cells have a many-to-one relationship to photoreceptors, including midget ganglion cells (Rodieck, 1988). --
-
--
--
'Address correspondence to G. W. Stuart, Victorian Transcultural Psychiatry Unit, 110 Nicholson St., Fitzroy, Victoria, Australia 3065.
REPLY TO GROSSER AND SPAFFORD
649
(3) The most serious problem of all is their new claim that "the rapid onset of earlier transient system responding (is) due to the highly light sensitive rods," a claim repeated throughout the article, but with no supporting evidence. In fact, evidence is readily available which contradicts this claim. First, it is well established that transient responses are a property of neurons, not photoreceptors. These are first seen in the amacrine layer of the retina (Rodieck, 1988). Second, if we were to accept their scheme it would seem that flicker sensitivity should be optimal under dark-adapted conditions whereas the opposite is the case. I n a classic study, Hecht and Smith (1936) demonstrated an increase in critical flicker frequency with luminance, with an obvious "rod-cone break" above which sensitivity increased rapidly. Third, under conditions where both systems operate, the cone system has the shorter latency (Walters, 1971). We reiterate-the rod system is not more sensitive than the cone system to either contrast or flicker at moderate lurninance levels. There is a large weight of evidence in the literature, which we cannot review here, against the idea that the different properties of the magnocellular ("transient") and parvocellular ("sustained") visual channels can be explained simply in terms of photoreceptor inputs. We strongly dispute Grosser and Spafford's (1992) claim to have "bridged the gap" between the two competing theories in this way. There is still no positive evidence in favour of an abnormality at the photoreceptor level in dyslexia, an idea which arose from an apparent misconception about the role of rods in contrast detection at moderate and high luminance levels. Until they directly measure photoreceptor densities in dyslexics, their claims should be viewed with a great degree of skepticism. CURCIO, C. A,,
&
REFERENCES HENDRICKSON, A. E. (1991) Organisation and development of the primate
photoreceptor mosaic. Progress in Retinal Research, 10, 89-120. & SPAFFORD, C. S. (1992) Reply to Stuart and Lovegrove's question, "Visual processing deficits in dyslexia: receptors or neural mechanisms?" Perceptual and Motor Skills, 75, 115-120. HECHT, S., & SMITH,E. L. (1936) Intermittent stimulation by light. Journal of General Physiology, 19, 979-989. KOENDERMK,J. J., BOUMAN,M. A,, BUENO DE MESQUITA,A. E., & SLAPPENDEL, S. (19781 Perimetry of contrast detection thresholds of moving spatial sine wave patterns: IV. The influence of mean retinal illuminance. Journal of the Optical Society o/ America, 68, 860-865. LNINGSTONE, M. S., ROSEN,G. D., DRISLANE, F., & GALABURDA, A. (1991) Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proceedings o/ the National Academy of Sciences, U.S.A., 88, 7943-7947. MULLEN,K. T. (1991) Colour vision as a post-receptoral specialization of the central visual field. Vision Research, 31, 119-130. RODIECK,R. W. (1988) The primate retina. In J. Erwin (Ed.), Comparative primate biology: 4. Neurosciences. New York: Liss. Pp. 203-207. S~IAPLEY, R. M., & ENROTH-CUGELL, C. (1984) Visual adaptation and retinal gain controls. Progress in Retinal Research, 3, 263-346.
GROSSER, G. S.,
650
G. W. STUART & W. J. LOVEGROVE
W. J. (1992) Visual processing deficits in dyslexia: receptors or STUART,G. W., & LOVEGROVE, neural mechanisms? Perceptual and Motor Skills, 74, 187-192. THIBOS,L. N., CHENEY, F, E., & WALSFI, D. J. (1987) Retinal limits to the detection and resolution of gratings. journal o/the Optical Society of America, A4, 1524-1529. WALTERS, J. W. (1971) Scotopic vision a t photopic levels? Vision Research, 11, 787-798.
Accepted August 19, 1992.
STILL N O EVIDENCE FOR A PHOTORECEPTOR-LEVEL ABNORMALITY I N DYSLEXIA ' AND
G . W. STUART Australian National University
W. J. LOVEGROVE Wollongong Universit)l
Summary.-In reply to Grosser and Spafford's (1992) defence of their theor! that rhere is a photoreceptor-level abnormality in dyslexia we argue that (1) their original experiments d o not cap rod functions, ( 2 ) the theory fails at the quantitative level, and (3) the proposition that rod inputs generate transient responses is false.
Grosser and Spafford (1992) have recently replied to criticisms made by us (Stuart & Lovegrove, 1992) of their claim that dyslexics are more sensitive to peripheral colour contrast, and less sensitive to luminance contrast, or periphery. Very briefly, we because they have a cone-rich, r ~ d - ~ o retinal argued that at the light levels used in their experiments, cone responses should dominate both color and luminance contrast detection and attributed the abnormalities in dyslexic vision to a postreceptoral deficit in the magnocellular layers of the lateral geniculate nucleus, for which there is now direct anatomical evidence (Livingstone, Rosen, Drislane, & Galaburda, 1991). This new attempt to justify their theory of a photoreceptor level abnormality suffers from three major deficiencies: ( I ) They do not challenge the findings of Shapley and Enroth-Cugell (1984) and Koenderink, Bournan, Bueno de Mesquita, and Slappendel (1978) who showed that cones, not rods, determine luminance contrast sensitivity above purely scotopic light levels and that this is true at all eccentricities. This omission is serious, because it means that their empirical work cannot convincingly be tied to rod function. (2) They d o not directly address quantitative evidence which shows that peripheral visual sensitivity cannot be explained in terms of photoreceptor densities, even in normal observers (e.g., MuIIen, 1991; Thibos, Cheney, & Walsh, 1987). However, in a tacit admission of the importance of postreceptoral mechanisms, they argue that it is photoreceptor densities which determine the densities of different types of ganglion cells. Developmentally, this cannot be the case, because ganglion cells develop before the photoreceptors (Curcio & Hendrickson, 1991). What they fail to appreciate is that i t is the sampling of the retinal mosaic by visual neurons which provides the "bottleneck" in visual processing, because in the periphery all major types of ganglion cells have a many-to-one relationship to photoreceptors, including midget ganglion cells (Rodieck, 1988). --
-
--
--
'Address correspondence to G. W. Stuart, Victorian Transcultural Psychiatry Unit, 110 Nicholson St., Fitzroy, Victoria, Australia 3065.
REPLY TO GROSSER AND SPAFFORD
649
(3) The most serious problem of all is their new claim that "the rapid onset of earlier transient system responding (is) due to the highly light sensitive rods," a claim repeated throughout the article, but with no supporting evidence. In fact, evidence is readily available which contradicts this claim. First, it is well established that transient responses are a property of neurons, not photoreceptors. These are first seen in the amacrine layer of the retina (Rodieck, 1988). Second, if we were to accept their scheme it would seem that flicker sensitivity should be optimal under dark-adapted conditions whereas the opposite is the case. I n a classic study, Hecht and Smith (1936) demonstrated an increase in critical flicker frequency with luminance, with an obvious "rod-cone break" above which sensitivity increased rapidly. Third, under conditions where both systems operate, the cone system has the shorter latency (Walters, 1971). We reiterate-the rod system is not more sensitive than the cone system to either contrast or flicker at moderate lurninance levels. There is a large weight of evidence in the literature, which we cannot review here, against the idea that the different properties of the magnocellular ("transient") and parvocellular ("sustained") visual channels can be explained simply in terms of photoreceptor inputs. We strongly dispute Grosser and Spafford's (1992) claim to have "bridged the gap" between the two competing theories in this way. There is still no positive evidence in favour of an abnormality at the photoreceptor level in dyslexia, an idea which arose from an apparent misconception about the role of rods in contrast detection at moderate and high luminance levels. Until they directly measure photoreceptor densities in dyslexics, their claims should be viewed with a great degree of skepticism. CURCIO, C. A,,
&
REFERENCES HENDRICKSON, A. E. (1991) Organisation and development of the primate
photoreceptor mosaic. Progress in Retinal Research, 10, 89-120. & SPAFFORD, C. S. (1992) Reply to Stuart and Lovegrove's question, "Visual processing deficits in dyslexia: receptors or neural mechanisms?" Perceptual and Motor Skills, 75, 115-120. HECHT, S., & SMITH,E. L. (1936) Intermittent stimulation by light. Journal of General Physiology, 19, 979-989. KOENDERMK,J. J., BOUMAN,M. A,, BUENO DE MESQUITA,A. E., & SLAPPENDEL, S. (19781 Perimetry of contrast detection thresholds of moving spatial sine wave patterns: IV. The influence of mean retinal illuminance. Journal of the Optical Society o/ America, 68, 860-865. LNINGSTONE, M. S., ROSEN,G. D., DRISLANE, F., & GALABURDA, A. (1991) Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proceedings o/ the National Academy of Sciences, U.S.A., 88, 7943-7947. MULLEN,K. T. (1991) Colour vision as a post-receptoral specialization of the central visual field. Vision Research, 31, 119-130. RODIECK,R. W. (1988) The primate retina. In J. Erwin (Ed.), Comparative primate biology: 4. Neurosciences. New York: Liss. Pp. 203-207. S~IAPLEY, R. M., & ENROTH-CUGELL, C. (1984) Visual adaptation and retinal gain controls. Progress in Retinal Research, 3, 263-346.
GROSSER, G. S.,
650
G. W. STUART & W. J. LOVEGROVE
W. J. (1992) Visual processing deficits in dyslexia: receptors or STUART,G. W., & LOVEGROVE, neural mechanisms? Perceptual and Motor Skills, 74, 187-192. THIBOS,L. N., CHENEY, F, E., & WALSFI, D. J. (1987) Retinal limits to the detection and resolution of gratings. journal o/the Optical Society of America, A4, 1524-1529. WALTERS, J. W. (1971) Scotopic vision a t photopic levels? Vision Research, 11, 787-798.
Accepted August 19, 1992.
