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Facilitation of the spinal H-reflex by auditory stimulation in dyslexic adults
Neuroscience Letters 327 (2002) 213–215 www.elsevier.com/locate/neulet
Facilitation of the spinal H-reflex by auditory stimulation in dyslexic adults Katariina Saarelma a, Hanna Renvall a,*, Veikko Jousma¨ki a, Tero Kovala b, Riitta Hari a,b a
Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, P.O. Box 2200, 02015 HUT, Espoo, Finland b Division of Clinical Neurophysiology, Helsinki University Central Hospital, 00290 Helsinki, Finland Received 18 February 2002; received in revised form 9 April 2002; accepted 9 April 2002
Abstract Dyslexic subjects show a variety of mild sensory and motor deficits that have been assumed to reflect dysfunction of the large-diameter ‘magnocells’ in different parts of the brain. Hearing as a warning sense relies on rapidly-conducting fibers, and on the basis of the magnocellular deficit theory, we wondered whether auditory alerting would be weakened in dyslexic adults. We quantified the strength of sound-induced spinal facilitation in seven dyslexic and eight normalreading adults by measuring the amplitudes of H-reflex, a monosynaptic spinal reflex, after loud binaural sounds. The audiospinal facilitation was of similar strength in dyslexic and control adults, indicating normal auditory alerting via cerebrospinal pathways. The slightly prolonged facilitation in dyslexics agrees with the dyslexics’ general sluggishness of sensorimotor processing. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Dyslexia; Audiospinal facilitation; Auditory startle reaction; Magnocellular
Dyslexic children and adults display various small sensory and motor deficits besides impaired reading-related skills. A prominent abnormality is the sluggishness in processing auditory, visual, and tactile stimuli presented in rapid succession [6,7,10,11,19,21]. Some of the multisystem effects have been attributed to a general deficit of large-diameter magnocellular (M) pathways [6,19]. The Mdeficit has been proposed to arise in the early life of genetically predisposed subjects [5], possibly as a result of immunoreactive damage to cell-surface substances common to all M-cells [3,18]. It is worth noting that we do not relate sluggishness of dyslexic subjects to slower conduction velocities of M-cell fibers but rather to the weaker overall activity of this fiber group. We have recently shown that dyslexic adults suffer from a left-sided ‘minineglect’, i.e. weakened triggering of automatic attention by visual stimuli in the left hemifield [9]. In the framework of the magnocellular theory, such a disorder could reflect deficient M-input to the parietal lobe and the resulting weakening in the parietal-lobe-supported functions, as the parietal lobe seems to receive predominantly * Corresponding author. Tel.: 1358-9-451-2982; fax: 1358-9451-2969. E-mail address: [email protected] (H. Renvall).
M-input [14]. We have proposed that the M-deficit could via sluggish capture of automatic attention slow down processing of stimuli presented in rapid succession [8,9]. In the same framework, one may wonder whether dyslexic subjects would be alerted less efficiently than normal readers by external stimuli. One good indicator of automatic alerting is the startle reaction elicited by abrupt loud sounds. The startle reaction involves sound-induced spinal facilitation, transmitted through large-diameter reticulospinal pathways. The spinal facilitation is affected by cortical auditory areas, as is demonstrated by findings that sounds presented to the ear contralateral to a lesioned auditory cortex fail to produce the spinal facilitation [12]; in normal conditions, the corticocortical pathways from the auditory to the frontal premotor areas could exert facilitatory control on the spinal motoneurons [12]. As dyslexic subjects often have deficits in their central auditory pathways [1,4,15], and because the M-neurons of the thalamic auditory relay nuclei are smaller in dyslexic than normal-reading individuals [4], we envisioned that the strength of sound-induced spinal facilitation might be abnormal in dyslexic subjects. To test this possibility, we monitored amplitude changes of the monosynaptic H-reflex of the gastrocnemius muscle. The H-reflex can be triggered by submaximal electric stimulation of the tibial nerve, and it
0304-3940/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S03 04 - 394 0( 0 2) 00 38 8- 9
214
K. Saarelma et al. / Neuroscience Letters 327 (2002) 213–215
Table 1 The behavioral profile of control and dyslexic subjects in reading-related tests a
Oral-reading speed (words/min) Word recognition (ms) Digit span (forwards) Digit span (backwards) Naming (ms/item)
Control subjects (n ¼ 8)
Dyslexic subjects (n ¼ 7)
P
155 ^ 8 544 ^ 31 6.6 ^ 0.4 6.0 ^ 0.7 467 ^ 23
109 ^ 6 811 ^ 66 5.1 ^ 0.3 4.3 ^ 0.3 667 ^ 66
, 0.001 , 0.01 , 0.01 , 0.04 , 0.03
a The values refer to mean ^ SEM. In the oral-reading task, the subject had to quickly read aloud a Finnish story, and reading speed was measured during 1 min in the middle of the task. In a computerized word recognition task, the subject had to decide, as fast as possible, whether a word presented on a computer screen was a real Finnish word or an orthographically legal pseudoword. Correctly recognized words were used for calculating the word recognition speed. Working memory was tested with digit spans forwards and backwards by using the standard Wechsler Adult Intelligence Scale procedure [22]. Naming speed was measured with a 5 £ 10 matrix consisting of numbers, letters and colors. The reading speeds and word recognition times were in all dyslexic subjects at least one standard deviation below the mean values of the control subjects.
is analogous to the mechanical Achilles tendon reflex tested in a routine neurological examination. In normal subjects, the H-reflex increases in amplitude 50 ms after the onset of a loud sound and the effect lasts for about 200 ms, reflecting sound-induced facilitation of the spinal-level monosynaptic reflex arch. The facilitation typically reaches its peak amplitude 100 ms after the sound onset [12,16]. We tested, with informed consent, seven dyslexic adults (age range 19–40 years; mean 31.3 years; five females, two males) and eight healthy control subjects (24–39 years; mean 28.8 years; five females, three males). The dyslexics were selected on the basis of a childhood history of difficulties in learning to read; all of them had a stated diagnosis of developmental dyslexia, and five of them had participated in special tutoring during school age. One of the subjects has after our recordings got an additional diagnosis of attentional deficit disorder. The highest level of education in dyslexics was 13.0 ^ 1.0 years; all of them had the minimum of two years of formal education after 9-year comprehensive school. One dyslexic subject had a university degree, and one was studying for an academic-level professional degree. At the time of measurement, the subjects performed five reading-related behavioral tasks. The tasks and results are presented in Table 1. The H-reflex was recorded from the gastrocnemius muscle with surface electrodes (spaced by about 5 cm) by applying 0.2-ms electric stimuli to the tibial nerve in the popliteal fossa while the subject was lying supine and relaxed on a bed. Brief square-wave sounds (95–100 dB sound pressure level, 100 ms, 1 kHz) preceded the electric pulse at random intervals of 0–320 ms in 10–40 ms steps. The sounds were led to the subject binaurally via headphones. The interstimulus interval was 14.3 s. Efforts were made to ensure a stable H-reflex amplitude, with direct muscular responses essentially absent. The test for each subject was repeated once or twice, and the set with the most stable baseline responses before and after facilitation (tone-pulse lags 0, 20, 280, and 320 ms) was chosen for further analysis. Results from the behavioral tests were compared between
the groups with two-tailed t-tests. The deviance of the Hreflex mean amplitude from baseline was computed against the baseline at 90–100 ms and at 160–240 ms with twotailed t-tests. The group differences in the H-reflex amplitudes were analyzed with mixed-model analysis of variance (ANOVA; ‘subject group’ as between-subjects factor, and ‘latencies between 40 and 240 ms’ as within-subjects factors). Although the sounds were loud, no overt startle responses were observed. The insert of Fig. 1 shows the responses of one control subject. The H-reflex amplitude increased after the sound, with the maximum amplitudes at time lags of about 100 ms. Fig. 1 shows the mean ^ SEM amplitudes for the two groups as a function of the sound-pulse delay; the 100%-
Fig. 1. Sound-induced changes in the H-reflex amplitudes as a function of the sound-pulse delay. The values are means ^ SEM of the normalized amplitudes, calculated with respect to the mean values of amplitudes at time delays of 0 and 20 ms. The insert shows original H-reflex recording from one control subject in arbitrary units; the black horizontal bar shows the duration of the 100-ms sound. Due to the conduction time, the first H-reflex (sound-pulse delay, 0 ms) starts around 30 ms. Note that no direct muscle response was elicited at the stimulus intensity level applied in the tests.
K. Saarelma et al. / Neuroscience Letters 327 (2002) 213–215
level was determined as the average H-reflex amplitude at the 0 and 20 ms sound-pulse delays. Both subject groups showed a significant (200–250%) facilitation of the Hreflex, with the maximum around 90–100 ms (P , 0:02 for dyslexics; P , 0:002 for controls). The mean values were larger in dyslexics than in the control subjects at all time lags; however, this difference between the groups was not significant (ANOVA; P ¼ 0:38) and no group £ latency interaction emerged (P ¼ 0:997). Dyslexic subjects showed a tendency for prolonged facilitation, significant still at 160–240 ms (P , 0:001) in dyslexics but not in controls (P ¼ 0:12). The strengths and time courses of the observed soundinduced H-reflex changes are in good agreement with previous results on audiospinal facilitation [12,16]. The facilitation was of similar strength in both groups, indicating normal auditory startle reaction in the dyslexic adults. However, the facilitation tended to last longer in dyslexic than normal-reading individuals. Such a prolongation would be in line with the frequently observed general sluggishness of sensorimotor processing and the proposed prolonged attentional dwell time in dyslexic subjects (for a review, see Ref. [8]). Thus, in spite of minor deficits in the auditory pathways, well documented in dyslexic subjects [1,4,15], the possible M-cell deficits in the involved neural pathways were subtle enough to remain undetected in the audiospinal facilitation that relies on fast-conducting large-diameter reticulospinal pathways. Similarly, many M-deficits in the visual system seem relatively mild [2] so that their direct effects on, for example, reading are heavily disputed [17,20]. However, even a mild M-deficit could cause a significant impairment of reading-related skills via sluggish attention shifting [8,9]. In further studies, the specificity of the recordings might be enhanced by using separate left- and right-ear sounds [4], and by testing the short-term and long-term habituation of the H-reflex after conditioning sounds [13]. This work was supported by the Academy of Finland. The authors would like to thank Juhani Partanen for the possibility to use the EMG amplifiers, and Ronny Schreiber and Erika Kirveskari for technical assistance. [1] Baldeweg, T., Richardson, A., Watkins, S., Foale, C. and Gruzelier, J., Impaired auditory frequency discrimination in dyslexia detected with mismatch evoked potentials, Ann. Neurol., 45 (1999) 495–503. [2] Cornelissen, P., Richardson, A., Mason, A., Fowler, S. and Stein, J., Contrast sensitivity and coherent motion detection measured at photopic luminance levels in dyslexics and controls, Vis. Res., 35 (1995) 1483–1494.
215
[3] Galaburda, A. and Livingstone, M., Evidence for a magnocellular defect in developmental dyslexia, Ann. N. Y. Acad. Sci., 682 (1993) 70–82. [4] Galaburda, A.M., Menard, M.T. and Rosen, G.D., Evidence for aberrant auditory anatomy in developmental dyslexia, Proc. Natl. Acad. Sci. USA, 91 (1994) 8010–8013. [5] Gilger, J.W., Pennington, B.F. and Defries, J.C., Risk for reading disability as a function of parental history in three family studies, Reading Writing: Interdisciplinary J., 3 (1991) 205–217. [6] Habib, M., The neurological basis of developmental dyslexia – an overview and working hypothesis, Brain, 123 (2000) 2373–2399. [7] Hari, R. and Kiesila¨ , P., Deficit of temporal auditory processing in dyslexic adults, Neurosci. Lett., 205 (1996) 138–140. [8] Hari, R. and Renvall, H., Impaired processing of rapid stimulus sequences in dyslexia, Trends Cogn. Sci., 5 (2001) 525– 532. [9] Hari, R., Renvall, H. and Tanskanen, T., Left minineglect in dyslexic adults, Brain, 124 (2001) 1373–1380. [10] Helenius, P., Uutela, K. and Hari, R., Auditory stream segregation in dyslexic adults, Brain, 122 (1999) 907–913. [11] Laasonen, M., Tomma-Halme, J., Lahti-Nuuttila, P., Service, E. and Virsu, V., Rate of information segregation in developmentally dyslexic children, Brain Lang., 75 (2000) 66–81. [12] Lie´ geois-Chauvel, C., Morin, C., Musolino, A., Bancaud, J. and Chauvel, P., Evidence for a contribution of the auditory cortex to audiospinal facilitation in man, Brain, 112 (1989) 375–391. [13] Maschke, M., Drepper, J., Kindsvater, K., Kolb, F.P., Diener, H.-C. and Timmann, D., Involvement of the human medial cerebellum in long-term habituation of the acoustic startle response, Exp. Brain Res., 133 (2000) 359–367. [14] Merigan, W.H. and Maunsell, J.H.R., How parallel are the primate visual pathways, Annu. Rev. Neurosci., 16 (1993) 369–402. [15] Nagarajan, S., Mahncke, H., Salz, T., Tallal, P., Roberts, T. and Merzenich, M.M., Cortical auditory signal processing in poor readers, Proc. Natl. Acad. Sci. USA, 96 (1999) 6483– 6488. [16] Rossignol, S. and Jones, G.M., Audio-spinal influence in man studied by the H-reflex and its possible role on rhythmic movements synchronized to sound, Electroenceph. clin. Neurophysiol., 41 (1976) 83–92. [17] Skottun, B.C., On the conflicting support for the magnocellular-deficit theory of dyslexia. Response to Stein, Talcott and Walsh (2000), Trends Cogn. Sci., 4 (2000) 211–212. [18] Stein, J. and Richardson, A., A question of misattribution, Curr. Biol., 9 (1999) R374–R376. [19] Stein, J. and Walsh, V., To see but not to read; the magnocellular theory of dyslexia, Trends Neurosci., 20 (1997) 147– 152. [20] Stein, J., Talcott, J. and Walsh, V.V., Controversy about the visual magnocellular deficit in developmental dyslexics, Trends Cogn. Sci., 4 (2000) 209–211. [21] Tallal, P., Auditory temporal perception, phonics, and reading disabilities in children, Brain Lang., 9 (1980) 182–198. [22] Wechsler, D., Wechsler Adult Intelligence Scale. Manual, Psychological Corporation, New York, 1955.
Facilitation of the spinal H-reflex by auditory stimulation in dyslexic adults Katariina Saarelma a, Hanna Renvall a,*, Veikko Jousma¨ki a, Tero Kovala b, Riitta Hari a,b a
Brain Research Unit, Low Temperature Laboratory, Helsinki University of Technology, P.O. Box 2200, 02015 HUT, Espoo, Finland b Division of Clinical Neurophysiology, Helsinki University Central Hospital, 00290 Helsinki, Finland Received 18 February 2002; received in revised form 9 April 2002; accepted 9 April 2002
Abstract Dyslexic subjects show a variety of mild sensory and motor deficits that have been assumed to reflect dysfunction of the large-diameter ‘magnocells’ in different parts of the brain. Hearing as a warning sense relies on rapidly-conducting fibers, and on the basis of the magnocellular deficit theory, we wondered whether auditory alerting would be weakened in dyslexic adults. We quantified the strength of sound-induced spinal facilitation in seven dyslexic and eight normalreading adults by measuring the amplitudes of H-reflex, a monosynaptic spinal reflex, after loud binaural sounds. The audiospinal facilitation was of similar strength in dyslexic and control adults, indicating normal auditory alerting via cerebrospinal pathways. The slightly prolonged facilitation in dyslexics agrees with the dyslexics’ general sluggishness of sensorimotor processing. q 2002 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Dyslexia; Audiospinal facilitation; Auditory startle reaction; Magnocellular
Dyslexic children and adults display various small sensory and motor deficits besides impaired reading-related skills. A prominent abnormality is the sluggishness in processing auditory, visual, and tactile stimuli presented in rapid succession [6,7,10,11,19,21]. Some of the multisystem effects have been attributed to a general deficit of large-diameter magnocellular (M) pathways [6,19]. The Mdeficit has been proposed to arise in the early life of genetically predisposed subjects [5], possibly as a result of immunoreactive damage to cell-surface substances common to all M-cells [3,18]. It is worth noting that we do not relate sluggishness of dyslexic subjects to slower conduction velocities of M-cell fibers but rather to the weaker overall activity of this fiber group. We have recently shown that dyslexic adults suffer from a left-sided ‘minineglect’, i.e. weakened triggering of automatic attention by visual stimuli in the left hemifield [9]. In the framework of the magnocellular theory, such a disorder could reflect deficient M-input to the parietal lobe and the resulting weakening in the parietal-lobe-supported functions, as the parietal lobe seems to receive predominantly * Corresponding author. Tel.: 1358-9-451-2982; fax: 1358-9451-2969. E-mail address: [email protected] (H. Renvall).
M-input [14]. We have proposed that the M-deficit could via sluggish capture of automatic attention slow down processing of stimuli presented in rapid succession [8,9]. In the same framework, one may wonder whether dyslexic subjects would be alerted less efficiently than normal readers by external stimuli. One good indicator of automatic alerting is the startle reaction elicited by abrupt loud sounds. The startle reaction involves sound-induced spinal facilitation, transmitted through large-diameter reticulospinal pathways. The spinal facilitation is affected by cortical auditory areas, as is demonstrated by findings that sounds presented to the ear contralateral to a lesioned auditory cortex fail to produce the spinal facilitation [12]; in normal conditions, the corticocortical pathways from the auditory to the frontal premotor areas could exert facilitatory control on the spinal motoneurons [12]. As dyslexic subjects often have deficits in their central auditory pathways [1,4,15], and because the M-neurons of the thalamic auditory relay nuclei are smaller in dyslexic than normal-reading individuals [4], we envisioned that the strength of sound-induced spinal facilitation might be abnormal in dyslexic subjects. To test this possibility, we monitored amplitude changes of the monosynaptic H-reflex of the gastrocnemius muscle. The H-reflex can be triggered by submaximal electric stimulation of the tibial nerve, and it
0304-3940/02/$ - see front matter q 2002 Elsevier Science Ireland Ltd. All rights reserved. PII: S03 04 - 394 0( 0 2) 00 38 8- 9
214
K. Saarelma et al. / Neuroscience Letters 327 (2002) 213–215
Table 1 The behavioral profile of control and dyslexic subjects in reading-related tests a
Oral-reading speed (words/min) Word recognition (ms) Digit span (forwards) Digit span (backwards) Naming (ms/item)
Control subjects (n ¼ 8)
Dyslexic subjects (n ¼ 7)
P
155 ^ 8 544 ^ 31 6.6 ^ 0.4 6.0 ^ 0.7 467 ^ 23
109 ^ 6 811 ^ 66 5.1 ^ 0.3 4.3 ^ 0.3 667 ^ 66
, 0.001 , 0.01 , 0.01 , 0.04 , 0.03
a The values refer to mean ^ SEM. In the oral-reading task, the subject had to quickly read aloud a Finnish story, and reading speed was measured during 1 min in the middle of the task. In a computerized word recognition task, the subject had to decide, as fast as possible, whether a word presented on a computer screen was a real Finnish word or an orthographically legal pseudoword. Correctly recognized words were used for calculating the word recognition speed. Working memory was tested with digit spans forwards and backwards by using the standard Wechsler Adult Intelligence Scale procedure [22]. Naming speed was measured with a 5 £ 10 matrix consisting of numbers, letters and colors. The reading speeds and word recognition times were in all dyslexic subjects at least one standard deviation below the mean values of the control subjects.
is analogous to the mechanical Achilles tendon reflex tested in a routine neurological examination. In normal subjects, the H-reflex increases in amplitude 50 ms after the onset of a loud sound and the effect lasts for about 200 ms, reflecting sound-induced facilitation of the spinal-level monosynaptic reflex arch. The facilitation typically reaches its peak amplitude 100 ms after the sound onset [12,16]. We tested, with informed consent, seven dyslexic adults (age range 19–40 years; mean 31.3 years; five females, two males) and eight healthy control subjects (24–39 years; mean 28.8 years; five females, three males). The dyslexics were selected on the basis of a childhood history of difficulties in learning to read; all of them had a stated diagnosis of developmental dyslexia, and five of them had participated in special tutoring during school age. One of the subjects has after our recordings got an additional diagnosis of attentional deficit disorder. The highest level of education in dyslexics was 13.0 ^ 1.0 years; all of them had the minimum of two years of formal education after 9-year comprehensive school. One dyslexic subject had a university degree, and one was studying for an academic-level professional degree. At the time of measurement, the subjects performed five reading-related behavioral tasks. The tasks and results are presented in Table 1. The H-reflex was recorded from the gastrocnemius muscle with surface electrodes (spaced by about 5 cm) by applying 0.2-ms electric stimuli to the tibial nerve in the popliteal fossa while the subject was lying supine and relaxed on a bed. Brief square-wave sounds (95–100 dB sound pressure level, 100 ms, 1 kHz) preceded the electric pulse at random intervals of 0–320 ms in 10–40 ms steps. The sounds were led to the subject binaurally via headphones. The interstimulus interval was 14.3 s. Efforts were made to ensure a stable H-reflex amplitude, with direct muscular responses essentially absent. The test for each subject was repeated once or twice, and the set with the most stable baseline responses before and after facilitation (tone-pulse lags 0, 20, 280, and 320 ms) was chosen for further analysis. Results from the behavioral tests were compared between
the groups with two-tailed t-tests. The deviance of the Hreflex mean amplitude from baseline was computed against the baseline at 90–100 ms and at 160–240 ms with twotailed t-tests. The group differences in the H-reflex amplitudes were analyzed with mixed-model analysis of variance (ANOVA; ‘subject group’ as between-subjects factor, and ‘latencies between 40 and 240 ms’ as within-subjects factors). Although the sounds were loud, no overt startle responses were observed. The insert of Fig. 1 shows the responses of one control subject. The H-reflex amplitude increased after the sound, with the maximum amplitudes at time lags of about 100 ms. Fig. 1 shows the mean ^ SEM amplitudes for the two groups as a function of the sound-pulse delay; the 100%-
Fig. 1. Sound-induced changes in the H-reflex amplitudes as a function of the sound-pulse delay. The values are means ^ SEM of the normalized amplitudes, calculated with respect to the mean values of amplitudes at time delays of 0 and 20 ms. The insert shows original H-reflex recording from one control subject in arbitrary units; the black horizontal bar shows the duration of the 100-ms sound. Due to the conduction time, the first H-reflex (sound-pulse delay, 0 ms) starts around 30 ms. Note that no direct muscle response was elicited at the stimulus intensity level applied in the tests.
K. Saarelma et al. / Neuroscience Letters 327 (2002) 213–215
level was determined as the average H-reflex amplitude at the 0 and 20 ms sound-pulse delays. Both subject groups showed a significant (200–250%) facilitation of the Hreflex, with the maximum around 90–100 ms (P , 0:02 for dyslexics; P , 0:002 for controls). The mean values were larger in dyslexics than in the control subjects at all time lags; however, this difference between the groups was not significant (ANOVA; P ¼ 0:38) and no group £ latency interaction emerged (P ¼ 0:997). Dyslexic subjects showed a tendency for prolonged facilitation, significant still at 160–240 ms (P , 0:001) in dyslexics but not in controls (P ¼ 0:12). The strengths and time courses of the observed soundinduced H-reflex changes are in good agreement with previous results on audiospinal facilitation [12,16]. The facilitation was of similar strength in both groups, indicating normal auditory startle reaction in the dyslexic adults. However, the facilitation tended to last longer in dyslexic than normal-reading individuals. Such a prolongation would be in line with the frequently observed general sluggishness of sensorimotor processing and the proposed prolonged attentional dwell time in dyslexic subjects (for a review, see Ref. [8]). Thus, in spite of minor deficits in the auditory pathways, well documented in dyslexic subjects [1,4,15], the possible M-cell deficits in the involved neural pathways were subtle enough to remain undetected in the audiospinal facilitation that relies on fast-conducting large-diameter reticulospinal pathways. Similarly, many M-deficits in the visual system seem relatively mild [2] so that their direct effects on, for example, reading are heavily disputed [17,20]. However, even a mild M-deficit could cause a significant impairment of reading-related skills via sluggish attention shifting [8,9]. In further studies, the specificity of the recordings might be enhanced by using separate left- and right-ear sounds [4], and by testing the short-term and long-term habituation of the H-reflex after conditioning sounds [13]. This work was supported by the Academy of Finland. The authors would like to thank Juhani Partanen for the possibility to use the EMG amplifiers, and Ronny Schreiber and Erika Kirveskari for technical assistance. [1] Baldeweg, T., Richardson, A., Watkins, S., Foale, C. and Gruzelier, J., Impaired auditory frequency discrimination in dyslexia detected with mismatch evoked potentials, Ann. Neurol., 45 (1999) 495–503. [2] Cornelissen, P., Richardson, A., Mason, A., Fowler, S. and Stein, J., Contrast sensitivity and coherent motion detection measured at photopic luminance levels in dyslexics and controls, Vis. Res., 35 (1995) 1483–1494.
215
[3] Galaburda, A. and Livingstone, M., Evidence for a magnocellular defect in developmental dyslexia, Ann. N. Y. Acad. Sci., 682 (1993) 70–82. [4] Galaburda, A.M., Menard, M.T. and Rosen, G.D., Evidence for aberrant auditory anatomy in developmental dyslexia, Proc. Natl. Acad. Sci. USA, 91 (1994) 8010–8013. [5] Gilger, J.W., Pennington, B.F. and Defries, J.C., Risk for reading disability as a function of parental history in three family studies, Reading Writing: Interdisciplinary J., 3 (1991) 205–217. [6] Habib, M., The neurological basis of developmental dyslexia – an overview and working hypothesis, Brain, 123 (2000) 2373–2399. [7] Hari, R. and Kiesila¨ , P., Deficit of temporal auditory processing in dyslexic adults, Neurosci. Lett., 205 (1996) 138–140. [8] Hari, R. and Renvall, H., Impaired processing of rapid stimulus sequences in dyslexia, Trends Cogn. Sci., 5 (2001) 525– 532. [9] Hari, R., Renvall, H. and Tanskanen, T., Left minineglect in dyslexic adults, Brain, 124 (2001) 1373–1380. [10] Helenius, P., Uutela, K. and Hari, R., Auditory stream segregation in dyslexic adults, Brain, 122 (1999) 907–913. [11] Laasonen, M., Tomma-Halme, J., Lahti-Nuuttila, P., Service, E. and Virsu, V., Rate of information segregation in developmentally dyslexic children, Brain Lang., 75 (2000) 66–81. [12] Lie´ geois-Chauvel, C., Morin, C., Musolino, A., Bancaud, J. and Chauvel, P., Evidence for a contribution of the auditory cortex to audiospinal facilitation in man, Brain, 112 (1989) 375–391. [13] Maschke, M., Drepper, J., Kindsvater, K., Kolb, F.P., Diener, H.-C. and Timmann, D., Involvement of the human medial cerebellum in long-term habituation of the acoustic startle response, Exp. Brain Res., 133 (2000) 359–367. [14] Merigan, W.H. and Maunsell, J.H.R., How parallel are the primate visual pathways, Annu. Rev. Neurosci., 16 (1993) 369–402. [15] Nagarajan, S., Mahncke, H., Salz, T., Tallal, P., Roberts, T. and Merzenich, M.M., Cortical auditory signal processing in poor readers, Proc. Natl. Acad. Sci. USA, 96 (1999) 6483– 6488. [16] Rossignol, S. and Jones, G.M., Audio-spinal influence in man studied by the H-reflex and its possible role on rhythmic movements synchronized to sound, Electroenceph. clin. Neurophysiol., 41 (1976) 83–92. [17] Skottun, B.C., On the conflicting support for the magnocellular-deficit theory of dyslexia. Response to Stein, Talcott and Walsh (2000), Trends Cogn. Sci., 4 (2000) 211–212. [18] Stein, J. and Richardson, A., A question of misattribution, Curr. Biol., 9 (1999) R374–R376. [19] Stein, J. and Walsh, V., To see but not to read; the magnocellular theory of dyslexia, Trends Neurosci., 20 (1997) 147– 152. [20] Stein, J., Talcott, J. and Walsh, V.V., Controversy about the visual magnocellular deficit in developmental dyslexics, Trends Cogn. Sci., 4 (2000) 209–211. [21] Tallal, P., Auditory temporal perception, phonics, and reading disabilities in children, Brain Lang., 9 (1980) 182–198. [22] Wechsler, D., Wechsler Adult Intelligence Scale. Manual, Psychological Corporation, New York, 1955.