- Email: [email protected]
Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans
Neuroscience Letters 264 (1999) 53–56
Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans Brigitte Ro¨der a ,*, Frank Ro¨sler a, Helen J. Neville b a
Experimental and Biological Psychology, Philipps-University Marburg, Gutenbergstrasse 18, D-35032 Marburg, Germany b Psychology Department, University of Oregon, Eugene, OR, USA Received 15 January 1999; received in revised form 25 January 1999; accepted 8 February 1999
Abstract To test the hypothesis of auditory compensation after early visual deprivation, congenitally blind and sighted adults performed an auditory discrimination task. They had to detect a rare target tone among frequent standard tones. Stimuli were presented with different interstimulus intervals (ISIs) (200, 1000, 2000 ms) and the auditory-event related potentials to all tones and reaction times to targets were recorded. Increasing ISIs resulted in an increasing amplitude of the vertex response (N1-P2) in both groups, but this amplitude recovery was more pronounced in the blind. Furthermore, targets elicited larger and more posteriorly distributed N2 responses in the blind than in the sighted. Since target detection times were shorter in the blind as well, these findings imply compensatory adaptations within the auditory modality in humans blind from birth. 1999 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Auditory-evoked potentials; Neuronal plasticity; Blindness; Sensory deprivation; Humans; Auditory processing
The idea of auditory compensation in blind people has still not been unambiguously clarified [10]. However, because of the absence of absolute sensitivity differences between sighted and blind humans [15], but superior performance of the blind in some more complex auditory tasks [11], it was suggested that compensation due to blindness takes place at higher or more central levels of information processing [15]. Electrophysiological studies have revealed shorter latencies and/or larger amplitudes for some mid-and long-latency components of the auditory event-related potential (ERP) in blind compared to sighted humans [13,15,19]. Furthermore, neuroimaging studies have provided evidence for a greater activation of posterior, polymodal or normally primarily visual brain areas during non-visual tasks in blind compared to sighted people [1,9,18–20]. This was hypothesized to be related to compensatory behavior in the blind. The purpose of our research was to gain insight into the level(s) of CNS activity that possibly mediate enhanced * Corresponding author. Tel.: +49-6421-283723; fax: +49-6421288948; e-mail: [email protected]
0304-3940/99/$ - see front matter PII: S03 04-3940(99)001 82-2
auditory abilities in blind humans. Here, we used a simple auditory discrimination paradigm to compare refractory properties of auditory ERPs between sighted and blind adults: in normal adults stimulus repetition within one modality causes an amplitude reduction of some event-related potential components and is known as relative refractoriness or recovery cycle [12]. Since synapses recover faster, it is assumed that complex neural circuits (or generators) cause these ERP effects [12]. In general, the relative refractory period has been regarded as an index of excitability of cortical neurons [14] and has been linked to processing rate or efficiency. In the context of compensatory plasticity it has been shown that N150 and P230 of visual ERPs recover faster in deaf than hearing people [14]. In the present study, sighted and blind participants listened to a series of pure tones which were preceded by different interstimulus intervals. We hypothesized that changes in the efficiency of auditory processing due to blindness should lead to a decreased refractoriness of auditory ERPs. The group of the congenitally blind consisted of 11 participants (Ps) (five females) with an average age of 35 years
1999 Elsevier Science Ireland Ltd. All rights reserved.
54
B. Ro¨der et al. / Neuroscience Letters 264 (1999) 53–56
(range 25–48 years) of whom all but one were righthanded. Eight were totally blind and three had some rudimentary sensitivity for light (without pattern vision). Blindness was caused in all cases by peripheral defects: retrolental fibroplasia (RLF) (six Ps), congenital glaucoma (two Ps), exposure to toxic substances (one P), anophthalmos (one P), rubella (one P, who had no other neurological problems). Eleven persons with normal (three Ps) or corrected to normal vision served as sighted controls; they were matched in age, sex, handedness and approximate educational level (five female and six male Ps. Average age was 35 years (range 23–48 years), all but one were right-handed). All participants reported having normal hearing. They all received monetary compensation for their participation. A series of ‘standard’ sine tones of 1500 Hz (duration: 50 ms, 65 dB SPL) was presented with headphones (TDH-39P) to the right, left or both ears (probability of each location was 0.33). Tones were presented with an interstimulus interval of 200, 1000 or 2000 ms. ‘Target’ stimuli (P = 0.1, 1000 Hz) were pseudo randomly mixed with standard stimuli and were always followed by a 2000 ms ISI. Participants were instructed to press a button as quickly as possible to each target irrespective of its location (response hand was counterbalanced across participants). The EEG was recorded with 28 tin electrodes mounted into an elastic cap (Electrocap International) from frontal, central, temporal, parietal and occipital scalp positions against the right mastoid. Offline an average mastoid reference was calculated. Impedances were maintained at 2 kQ or below. The EEG was digitized at 250 Hz and amplified with Grass amplifiers (model 7P511) using a bandpass of 0.01– 100 Hz (resolution of the A/D converter was 12 bit). The horizontal EOG was monitored using a bipolar recording of two electrodes attached at the outer canthus of each eye and the vertical eye movements were recorded separately for the left and right eye using electrodes beneath the left and right eye (against mastoid reference). The light was turned off in the recording chamber so that any visual input was eliminated for sighted participants as well. Reaction times were measured for target responses (within 100–2000 ms poststimulus). Nine separate ERPs were computed for standard stimuli dependant on the preceding ISI (short, medium or long) and the location of the tone (left, right or in both ears). Peak amplitudes were measured relative to a 100 ms prestimulus baseline within time epoch 70–150 ms (N1) and 150–250 ms (P2). ERPs to correctly detected targets were evaluated using difference waveforms, i.e. Standard and Target ERPs were averaged across ISI and Ear conditions and the difference waveform ERP (Targets) minus ERP (Standards) was calculated. N2 peak amplitudes and latencies (200–300 ms poststimulus) and P3 peak latencies and average amplitudes (300–600 ms poststimulus) were determined. These dependant variables were separately submitted to
analyses of variance (ANOVA, using the SAS program) with Group (Sighted vs. Blind) as a between participant factor and ISI (200, 1000 and 2000 ms). Ear (left, right or in both) and Electrode (28) as repeated measurement factors. To compensate for non-sphericity of the data, Huynh/ Feld-corrected P-values are reported in the result section. Blind participants (M (Blind) = 416.89 ms SE = 9.47) responded to the targets faster than sighted controls (M (Sighted) = 558.13 ms SE = 14.02: main effect Group: F(1,20) = 9.29 P = 0.0063). No further effect was significant (P . 0.12). By contrast, sighted and blind participants were equally accurate in deciding whether a tone was or was not a target (t(20) = 1.39, P = 0.1805; error percentages; M (Sighted) = 6% SE = 2.3; M (Blind) = 2% SE = 1.71). The peak amplitude of N1 showed significantly larger and faster recovery in blind than in sighted participants at
Fig. 1. Top; grand average of the event-related activity elicited by standard tones in the ISI 2000 ms condition at the posterior temporal electrodes T5 (left) and T6 (right). Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid line) are superimposed. Bottom: mean peak amplitude of the N1 (in mVol, with standard error bars) to standard stimuli as a function of the interstimulus interval measured at T5 (left) and T6 (right) for the matched sighted (white bars) and the congenitally blind (black bars). Negativity in both panels is up.
B. Ro¨der et al. / Neuroscience Letters 264 (1999) 53–56
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temporal and parieto-occipital electrodes (ISI × Group P , 0.05 and P , 0.1, respectively) (Fig. 1). The N1 latencies of standard tones (evaluated at Fz) were longest in the ISI-200 condition (main effect ISI: F(2,40) = 23.00, P = 0.0001). The latencies did not differ between groups (P . 0.45). The P2 amplitude increased with increasing ISI as well (F(2.4) = 48.84, P , 0.0001). Both this ISI effect and the P2 in general had a fronto-central distribution (Electrode; (F(27,540) = 52.06, P = 0.0001. Electrode × ISI: F(54,1080) = 19.53, P = 0.0001. This held for both groups. However, the blind had a larger P2 amplitude than the sighted at fronto-central electrodes, particularly in the binaural conditions (Electrode × Ear × Group: F(54,1080) = 2.23, P = 0.0185: main effect Group at fronto-central electrodes: P , 0.05) (Fig. 2). In addition, the overall ANOVA revealed a significant four-way interaction ElecFig. 3. Grand average difference waves: ERPs (Targets) minus ERP (Standards) at fronto-central (FC5 and FC6), parietal (P3 and P4) and temporo-occipital (TO1 and TO2) electrodes of the left and right hemisphere, respectively. Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid lines) are superimposed. P300 is indicated by a pointer at electrode P3 and the N2 at electrodes P3 and FC6.
Fig. 2. Top: grand average of the event-related activity elicited by standard tones in the ISI 2000 ms binaural condition at fronto-central electrodes FC5 (left) and FC6 (right). Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid line) are superimposed. Bottom: mean peak amplitude of the P2 (in mVol, with standard error bars) to standard stimuli as a function of the interstimulus interval measured at FC5 (left) and FC6 (right) for the sighted (stripped bars) and the congenitally blind (black bars). Negativity in both panels is up.
trode × Ear × ISI × Group (F(108,2160) = 1.70, P = 0.0450). A separate ANOVA for the three levels of factor Ear, revealed an Electrode × Group interaction (F(27,540) = 3.05, P = 0.0166) and marginal significant Electrode × ISI × Group interaction (F(54,1080) = 2.02, P = 0.0771) for the binaural presentation mode. Topographic group differences for the N1 and P2 were tested with normalized N1 and P2 peak amplitude scores (M = 100, SD = 15) (averaged across monaural and binaural conditions) as well as for the ISI effect proper, i.e. the standardized N1 and P2 difference wave ERP (3532000) − ERP (353200). None of these analyses revealed any significant effect involving the Group factor (N1: P . 0.68: P2: P . 0.37). Targets elicited in addition to the vertex potential (N1P2) a N2 and a posteriorly distributed P3 wave (Fig. 3). Due to the small number of trials, ISI effects were not analyzed for target ERPs. The N2 had a similar latency in the congenitally blind and the sighted but was more pronounced in the blind (F(1,20) = 4.39, P = 0.0491). In addition, the Electrode × Group interaction indicated a posteriorly shifted topography in the blind compared to the sighted (F(27,540) = 5.49, P = 0.0002) (Fig. 3), which was confirmed using standardized amplitude scores (F(27,540) = 3.26, P = 0.0082). Reliable amplitude differences between groups existed over the whole posterior brain (P , 0.05). There were no significant effects involving factor Group for any P300–600 parameter (latency, raw or standardized amplitude scores). Several studies have documented that multiple generators
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contribute to the N1 response. In the present study the ISI effects upon the N1 amplitude could be due to a faster recovery of the supratemporal and/or the unspecific components [12]. At long intervals the N1 distribution was found to be posteriorly shifted perhaps due to the contribution of an unspecific component [5]. Therefore, the posterior distributed ISI effect in the blind may indicate that it was mainly due to the unspecific component. The importance of posterior temporal and parietal association areas for the generation of the N1 is implied by both brain lesion data, showing that neither primary auditory nor frontal cortex lesions diminished the N1 response but lesions in the temporo-parietal cortex did [8] and anatomical data pointing towards a greater extension of auditory structures into parietal areas in humans than in monkeys [2]. ISI effects were more robust and pronounced for the P2 (as in [5]) in both groups but the recovery of the P2 was again faster in the blind. The lack of reliable topographic group differences for the N1 and P2 imply that the similar generator structures were activated in the blind and sighted participants. A greater use of and reliance on the auditory sensory system could have resulted in a grow (hypertrophy [3]), and greater excitability and therefore more efficient functioning of these neural units in the blind (intramodal plasticity). Intracranial recordings [4] and scalp recordings in brain damaged patients [7] have located the N2- generators in the temporal-parietal junction and in other parietal brain structures. Since these brain areas are known to be polymodal, it can be speculated that in the blind visual subdivisions are occupied by the intact modalities, as has been observed in visually deprived animals [6,16], leading to a stronger and more posteriorly orientated dipole [19]. Since the N2 is proposed to reflect early half-automatic classification mechanisms [17], a reorganization of the N2 generator structures could have contributed to the shorter reaction time in the blind as well (intermodal plasticity). Taken together, we found evidence that both intra- and intermodal changes follow visual deprivation in humans. Elementary auditory stimulus processing steps seem to be mediated by the same brain systems in sighted and blind individuals, but they seem to work more efficiently in the latter. Later processing steps, i.e. those associated with target classification proper, display intermodal reorganizations. The study was supported by Ro 1226/1–2 of the German Research Foundation (Deutsche Forschungsgemeinschaft) to B.R. and grants N.I.H. DC00128 to H.N. We thank the Oregon Commission for the Blind and the National Federation of the Blind in Eugene for their help in recruiting blind participants. [1] De Voder, A.G., Bol, A., Blin, J., Robert, A., Arno, P., Grandin, C., Michel, C. and Veraart, C., Brain energy metabolism in early blind subjects; neural activity in the visual cortex, Brain Res., 750 (1997) 235–244.
[2] Galaburda, A. and Sanides, F., Cytoarchitectonic organization of the human auditory cortex, J. Comp. Neurol., 190 (1980) 597–610. [3] Gyllensten, L., Mamfors, T. and Norrlin, M.-L., Growth alteration in the auditory cortex of visually deprived mice, J. Comp. Neurol., 126 (1966) 463–470. [4] Halgren, E., Baudena, P., Clark, J.M., Heit, G., Liegois, C., Chauvel, P. and Musolino, A., Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe, Electrenceph. clin. Neurphysiol., 94 (1995) 191–220. [5] Hari, R., Kaila, K., Katila, T., Tuomisto, T. and Varpula, T., Interstimulus interval dependence of the auditory vertex response and its magnetic counterpart: Implications for their neural generation, Electrenceph. clin. Neurphysiol., 54 (1982) 561–569. [6] Hyvarinen, J., Hyvarinen, L. and Linnankoski, I., Modification of parietal association cortex and functional blindness after binocular deprivation in young monkeys, Exp. Brain Res., 42 (1981) 1– 8. [7] Knight, R.T., Neuronal mechanisms of event-related potentials: Evidence from human lesion studies. In J.W. Rohrbrauch, R. Parasuraman and R.J. Johnson (Eds.), Event-related Brain Potentials: Basic Issues and Applications, ed. Vol., Oxford University Press, New York, 1990, pp. 3–18. [8] Knight, R.T., Hillyard, S.A., Woods, D.L. and Neville, H.J., The effects of frontal and temporal-parietal lesions on the auditory evoked potential in man, Electrenceph. clin. Neurphysiol., 50 (1980) 112–124. [9] Kujala, T., Alho, K., Kekoni, J., Hamalainen, H., Reinikainen, K., Salonen, O., Standertskjold-Nordenstam, C.-G. and Naatanen, R., Auditory and somatosensory event-related brain potentials in early blind humans, Exp. Brain Res., 104 (1995) 519–526. [10] Miller, L., Diderot reconsidered: visual impairment and auditory compensation, J. Vis. Impairm. Blindn., 86 (1992) 206–210. [11] Muchnik, C., Efrati, M., Nemeth, E., Malin, M. and Hildesheimer, M., Central auditory skills in blind and sighted subjects, Scand. Audiol., 20 (1991) 19–23. [12] Naatanen, R., Attention and Brain Function, Lawrence Erbaum, Hillsdale, NJ, 1992. [13] Naveen, K.V., Srinivas, R. and Nirmala, K.S., Differences between congenitally blind and normally sighted subjects in the P1 component of middle latency auditory evoked potentials, Percept. Mot. Skills, 86 (1998) 1192–1194. [14] Neville, H.J., Schmidt, A. and Kutas, M., Altered visual-evoked potentials in congenitally deaf adults, Brain Res., 266 (1983) 127–132. [15] Niemeyer, W. and Starlinger, I., Do blind hear better? Investigations on auditory processing in congenital early acquired blindness. II. Central functions, Audiology, 20 (1981) 510–515. [16] Rauscheker, J.P., Compensatory plasticity and sensory substitution in the cerebral cortex, Trends Neurosci., 18 (1995) 36–43. [17] Ritter, W., Simon, R. and Vaughan, H.G.J., Event-related potential correlates of two stages of information processing in physical and semantic discrimination task, Psychophysiology, 20 (1983) 168–179. [18] Ro¨der, B., Ro¨sler, F. and Henninghausen, E., Different cortical activation patterns in blind and sighted humans during encoding and transformation of haptic images, Psychophysiology, 34 (1997) 292–307. [19] Ro¨der, B., Ro¨sler, F., Henninghausen, E. and Nacker, F., Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects, Cogn. Brain Res., 4 (1996) 77–93. [20] Sadato, N., Pascual-Leone, A., Grafman, J., Ibanez, V., Deiber, M.-P. and Hallett, M., Braille reading in the blind activities visual cortex, Neurology, 45 (1995) A426–A427.
Effects of interstimulus interval on auditory event-related potentials in congenitally blind and normally sighted humans Brigitte Ro¨der a ,*, Frank Ro¨sler a, Helen J. Neville b a
Experimental and Biological Psychology, Philipps-University Marburg, Gutenbergstrasse 18, D-35032 Marburg, Germany b Psychology Department, University of Oregon, Eugene, OR, USA Received 15 January 1999; received in revised form 25 January 1999; accepted 8 February 1999
Abstract To test the hypothesis of auditory compensation after early visual deprivation, congenitally blind and sighted adults performed an auditory discrimination task. They had to detect a rare target tone among frequent standard tones. Stimuli were presented with different interstimulus intervals (ISIs) (200, 1000, 2000 ms) and the auditory-event related potentials to all tones and reaction times to targets were recorded. Increasing ISIs resulted in an increasing amplitude of the vertex response (N1-P2) in both groups, but this amplitude recovery was more pronounced in the blind. Furthermore, targets elicited larger and more posteriorly distributed N2 responses in the blind than in the sighted. Since target detection times were shorter in the blind as well, these findings imply compensatory adaptations within the auditory modality in humans blind from birth. 1999 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Auditory-evoked potentials; Neuronal plasticity; Blindness; Sensory deprivation; Humans; Auditory processing
The idea of auditory compensation in blind people has still not been unambiguously clarified [10]. However, because of the absence of absolute sensitivity differences between sighted and blind humans [15], but superior performance of the blind in some more complex auditory tasks [11], it was suggested that compensation due to blindness takes place at higher or more central levels of information processing [15]. Electrophysiological studies have revealed shorter latencies and/or larger amplitudes for some mid-and long-latency components of the auditory event-related potential (ERP) in blind compared to sighted humans [13,15,19]. Furthermore, neuroimaging studies have provided evidence for a greater activation of posterior, polymodal or normally primarily visual brain areas during non-visual tasks in blind compared to sighted people [1,9,18–20]. This was hypothesized to be related to compensatory behavior in the blind. The purpose of our research was to gain insight into the level(s) of CNS activity that possibly mediate enhanced * Corresponding author. Tel.: +49-6421-283723; fax: +49-6421288948; e-mail: [email protected]
0304-3940/99/$ - see front matter PII: S03 04-3940(99)001 82-2
auditory abilities in blind humans. Here, we used a simple auditory discrimination paradigm to compare refractory properties of auditory ERPs between sighted and blind adults: in normal adults stimulus repetition within one modality causes an amplitude reduction of some event-related potential components and is known as relative refractoriness or recovery cycle [12]. Since synapses recover faster, it is assumed that complex neural circuits (or generators) cause these ERP effects [12]. In general, the relative refractory period has been regarded as an index of excitability of cortical neurons [14] and has been linked to processing rate or efficiency. In the context of compensatory plasticity it has been shown that N150 and P230 of visual ERPs recover faster in deaf than hearing people [14]. In the present study, sighted and blind participants listened to a series of pure tones which were preceded by different interstimulus intervals. We hypothesized that changes in the efficiency of auditory processing due to blindness should lead to a decreased refractoriness of auditory ERPs. The group of the congenitally blind consisted of 11 participants (Ps) (five females) with an average age of 35 years
1999 Elsevier Science Ireland Ltd. All rights reserved.
54
B. Ro¨der et al. / Neuroscience Letters 264 (1999) 53–56
(range 25–48 years) of whom all but one were righthanded. Eight were totally blind and three had some rudimentary sensitivity for light (without pattern vision). Blindness was caused in all cases by peripheral defects: retrolental fibroplasia (RLF) (six Ps), congenital glaucoma (two Ps), exposure to toxic substances (one P), anophthalmos (one P), rubella (one P, who had no other neurological problems). Eleven persons with normal (three Ps) or corrected to normal vision served as sighted controls; they were matched in age, sex, handedness and approximate educational level (five female and six male Ps. Average age was 35 years (range 23–48 years), all but one were right-handed). All participants reported having normal hearing. They all received monetary compensation for their participation. A series of ‘standard’ sine tones of 1500 Hz (duration: 50 ms, 65 dB SPL) was presented with headphones (TDH-39P) to the right, left or both ears (probability of each location was 0.33). Tones were presented with an interstimulus interval of 200, 1000 or 2000 ms. ‘Target’ stimuli (P = 0.1, 1000 Hz) were pseudo randomly mixed with standard stimuli and were always followed by a 2000 ms ISI. Participants were instructed to press a button as quickly as possible to each target irrespective of its location (response hand was counterbalanced across participants). The EEG was recorded with 28 tin electrodes mounted into an elastic cap (Electrocap International) from frontal, central, temporal, parietal and occipital scalp positions against the right mastoid. Offline an average mastoid reference was calculated. Impedances were maintained at 2 kQ or below. The EEG was digitized at 250 Hz and amplified with Grass amplifiers (model 7P511) using a bandpass of 0.01– 100 Hz (resolution of the A/D converter was 12 bit). The horizontal EOG was monitored using a bipolar recording of two electrodes attached at the outer canthus of each eye and the vertical eye movements were recorded separately for the left and right eye using electrodes beneath the left and right eye (against mastoid reference). The light was turned off in the recording chamber so that any visual input was eliminated for sighted participants as well. Reaction times were measured for target responses (within 100–2000 ms poststimulus). Nine separate ERPs were computed for standard stimuli dependant on the preceding ISI (short, medium or long) and the location of the tone (left, right or in both ears). Peak amplitudes were measured relative to a 100 ms prestimulus baseline within time epoch 70–150 ms (N1) and 150–250 ms (P2). ERPs to correctly detected targets were evaluated using difference waveforms, i.e. Standard and Target ERPs were averaged across ISI and Ear conditions and the difference waveform ERP (Targets) minus ERP (Standards) was calculated. N2 peak amplitudes and latencies (200–300 ms poststimulus) and P3 peak latencies and average amplitudes (300–600 ms poststimulus) were determined. These dependant variables were separately submitted to
analyses of variance (ANOVA, using the SAS program) with Group (Sighted vs. Blind) as a between participant factor and ISI (200, 1000 and 2000 ms). Ear (left, right or in both) and Electrode (28) as repeated measurement factors. To compensate for non-sphericity of the data, Huynh/ Feld-corrected P-values are reported in the result section. Blind participants (M (Blind) = 416.89 ms SE = 9.47) responded to the targets faster than sighted controls (M (Sighted) = 558.13 ms SE = 14.02: main effect Group: F(1,20) = 9.29 P = 0.0063). No further effect was significant (P . 0.12). By contrast, sighted and blind participants were equally accurate in deciding whether a tone was or was not a target (t(20) = 1.39, P = 0.1805; error percentages; M (Sighted) = 6% SE = 2.3; M (Blind) = 2% SE = 1.71). The peak amplitude of N1 showed significantly larger and faster recovery in blind than in sighted participants at
Fig. 1. Top; grand average of the event-related activity elicited by standard tones in the ISI 2000 ms condition at the posterior temporal electrodes T5 (left) and T6 (right). Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid line) are superimposed. Bottom: mean peak amplitude of the N1 (in mVol, with standard error bars) to standard stimuli as a function of the interstimulus interval measured at T5 (left) and T6 (right) for the matched sighted (white bars) and the congenitally blind (black bars). Negativity in both panels is up.
B. Ro¨der et al. / Neuroscience Letters 264 (1999) 53–56
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temporal and parieto-occipital electrodes (ISI × Group P , 0.05 and P , 0.1, respectively) (Fig. 1). The N1 latencies of standard tones (evaluated at Fz) were longest in the ISI-200 condition (main effect ISI: F(2,40) = 23.00, P = 0.0001). The latencies did not differ between groups (P . 0.45). The P2 amplitude increased with increasing ISI as well (F(2.4) = 48.84, P , 0.0001). Both this ISI effect and the P2 in general had a fronto-central distribution (Electrode; (F(27,540) = 52.06, P = 0.0001. Electrode × ISI: F(54,1080) = 19.53, P = 0.0001. This held for both groups. However, the blind had a larger P2 amplitude than the sighted at fronto-central electrodes, particularly in the binaural conditions (Electrode × Ear × Group: F(54,1080) = 2.23, P = 0.0185: main effect Group at fronto-central electrodes: P , 0.05) (Fig. 2). In addition, the overall ANOVA revealed a significant four-way interaction ElecFig. 3. Grand average difference waves: ERPs (Targets) minus ERP (Standards) at fronto-central (FC5 and FC6), parietal (P3 and P4) and temporo-occipital (TO1 and TO2) electrodes of the left and right hemisphere, respectively. Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid lines) are superimposed. P300 is indicated by a pointer at electrode P3 and the N2 at electrodes P3 and FC6.
Fig. 2. Top: grand average of the event-related activity elicited by standard tones in the ISI 2000 ms binaural condition at fronto-central electrodes FC5 (left) and FC6 (right). Traces for the group of matched sighted (Match. Sigh.) (dashed line) and the group of congenitally blind participants (Cong. Blind) (solid line) are superimposed. Bottom: mean peak amplitude of the P2 (in mVol, with standard error bars) to standard stimuli as a function of the interstimulus interval measured at FC5 (left) and FC6 (right) for the sighted (stripped bars) and the congenitally blind (black bars). Negativity in both panels is up.
trode × Ear × ISI × Group (F(108,2160) = 1.70, P = 0.0450). A separate ANOVA for the three levels of factor Ear, revealed an Electrode × Group interaction (F(27,540) = 3.05, P = 0.0166) and marginal significant Electrode × ISI × Group interaction (F(54,1080) = 2.02, P = 0.0771) for the binaural presentation mode. Topographic group differences for the N1 and P2 were tested with normalized N1 and P2 peak amplitude scores (M = 100, SD = 15) (averaged across monaural and binaural conditions) as well as for the ISI effect proper, i.e. the standardized N1 and P2 difference wave ERP (3532000) − ERP (353200). None of these analyses revealed any significant effect involving the Group factor (N1: P . 0.68: P2: P . 0.37). Targets elicited in addition to the vertex potential (N1P2) a N2 and a posteriorly distributed P3 wave (Fig. 3). Due to the small number of trials, ISI effects were not analyzed for target ERPs. The N2 had a similar latency in the congenitally blind and the sighted but was more pronounced in the blind (F(1,20) = 4.39, P = 0.0491). In addition, the Electrode × Group interaction indicated a posteriorly shifted topography in the blind compared to the sighted (F(27,540) = 5.49, P = 0.0002) (Fig. 3), which was confirmed using standardized amplitude scores (F(27,540) = 3.26, P = 0.0082). Reliable amplitude differences between groups existed over the whole posterior brain (P , 0.05). There were no significant effects involving factor Group for any P300–600 parameter (latency, raw or standardized amplitude scores). Several studies have documented that multiple generators
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contribute to the N1 response. In the present study the ISI effects upon the N1 amplitude could be due to a faster recovery of the supratemporal and/or the unspecific components [12]. At long intervals the N1 distribution was found to be posteriorly shifted perhaps due to the contribution of an unspecific component [5]. Therefore, the posterior distributed ISI effect in the blind may indicate that it was mainly due to the unspecific component. The importance of posterior temporal and parietal association areas for the generation of the N1 is implied by both brain lesion data, showing that neither primary auditory nor frontal cortex lesions diminished the N1 response but lesions in the temporo-parietal cortex did [8] and anatomical data pointing towards a greater extension of auditory structures into parietal areas in humans than in monkeys [2]. ISI effects were more robust and pronounced for the P2 (as in [5]) in both groups but the recovery of the P2 was again faster in the blind. The lack of reliable topographic group differences for the N1 and P2 imply that the similar generator structures were activated in the blind and sighted participants. A greater use of and reliance on the auditory sensory system could have resulted in a grow (hypertrophy [3]), and greater excitability and therefore more efficient functioning of these neural units in the blind (intramodal plasticity). Intracranial recordings [4] and scalp recordings in brain damaged patients [7] have located the N2- generators in the temporal-parietal junction and in other parietal brain structures. Since these brain areas are known to be polymodal, it can be speculated that in the blind visual subdivisions are occupied by the intact modalities, as has been observed in visually deprived animals [6,16], leading to a stronger and more posteriorly orientated dipole [19]. Since the N2 is proposed to reflect early half-automatic classification mechanisms [17], a reorganization of the N2 generator structures could have contributed to the shorter reaction time in the blind as well (intermodal plasticity). Taken together, we found evidence that both intra- and intermodal changes follow visual deprivation in humans. Elementary auditory stimulus processing steps seem to be mediated by the same brain systems in sighted and blind individuals, but they seem to work more efficiently in the latter. Later processing steps, i.e. those associated with target classification proper, display intermodal reorganizations. The study was supported by Ro 1226/1–2 of the German Research Foundation (Deutsche Forschungsgemeinschaft) to B.R. and grants N.I.H. DC00128 to H.N. We thank the Oregon Commission for the Blind and the National Federation of the Blind in Eugene for their help in recruiting blind participants. [1] De Voder, A.G., Bol, A., Blin, J., Robert, A., Arno, P., Grandin, C., Michel, C. and Veraart, C., Brain energy metabolism in early blind subjects; neural activity in the visual cortex, Brain Res., 750 (1997) 235–244.
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