Enhanced brain activity preceding voluntary movement in early blind humans

Neuroscience Letters 253 (1998) 155–158

Enhanced brain activity preceding voluntary movement in early blind humans Anne Lehtokoski*, Teija Kujala, Risto Na¨a¨ta¨nen, Kimmo Alho Cognitive Brain Research Unit, Department of Psychology, P.O. Box 13 (Meritullinkatu 1), FIN-00014, University of Helsinki, Helsinki, Finland Received 1 July 1998; received in revised form 27 July 1998; accepted 27 July 1998

Abstract Effects of blindness on movement-related brain activity were investigated by measuring from the scalp movement-related potentials (MRPs) associated with self-paced button presses in blind and sighted young adults. The blind subjects had lost their vision at an early age due to a deficit in the peripheral visual system. The negative slope (NS′) of MRP at about 400 ms prior to movement and the preceding readiness potential (RP) were larger in the blind than in the sighted subjects, but were similarly distributed on the scalp in these groups. The results suggest functional changes in the blind subjects’ brain activity, presumably, in the cortical areas involved in preparation and initiation of voluntary movement.  1998 Elsevier Science Ireland Ltd. All rights reserved

Keywords: Blindness; Movement-related potentials; Self-paced movement; Brain plasticity; Brain responses; Humans

Blindness caused by a peripheral deficit leads to functional changes in brain areas representing the intact sensory modalities. For instance, as a result of bilateral eye enucleation performed one day after birth, spine density increases in rat auditory cortices [17]. Furthermore, in blind humans’ somatosensory cortex, the representation of the reading finger is expanded compared with the non-reading fingers. In addition, the representation area of the first dorsal interosseous muscle of the reading hand in the blind is significantly larger than that of the same muscle of the non-reading hand or that of either hand of the sighted control subjects [15]. In addition to changes in intact modalities, blindness causes plastic changes in the occipital and parietal cortical areas that normally process visual information [5,6]. It has been suggested that the visual cortex of the blind participates in detection of a change in auditory [10,12] and somatosensory [20] stimuli, and in auditory selective attention [1]. For instance, deviant target sounds, but not occasional deviant sounds occurring in an ignored sound sequence activate the occipital cortex in the blind [9,12]. * Corresponding author. Tel.: +358 9 19123406; fax: +358 9 19122924; e-mail: [email protected]

More posterior scalp distributions of DC potentials in the blind than in the sighted indicate occipital-cortex involvement in the blind during Braille reading and tactile mental imagery. Furthermore, DC-potential recordings have suggested that in the blind, occipital areas are involved in encoding and transformation of haptic images [16]. Visual cortex involvement was recently shown in Braille reading and tactile recognition of patterns in the blind [2,18]. This far the studies concerning the blind humans’ crossmodal plasticity have concentrated either in sensory functions or have included overlapping sensory and motor tasks. In the present study, motor functions of the blind were addressed by comparing movement-related brain potentials (MRPs) elicited by self-paced movements in blind and sighted subjects. MRP consists of a readiness potential (RP) starting at 1000–1200 ms prior to movement onset, a negative slope (NS′) peaking at 200–400 ms, and a motor potential (MP) usually peaking at 100–200 ms prior to the movement [19]. RP is probably generated in the supplementary motor area (SMA) [11], NS′ in the SMA and in the motor cortex [4], and MP mainly in the motor cortex [19]. RP, reflecting the initiation of a self-paced movement controlled by prefrontal cortex [8] and NS′ and MP reflect-

0304-3940/98/$19.00  1998 Elsevier Science Ireland Ltd. All rights reserved PII S0304- 3940(98) 00626- 0

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ing the cortical activity associated with the execution of a self-paced movement [19] were measured from 14 righthanded young adults. Seven subjects were sighted (mean age 25.7 years, three males) and seven subjects were blind (mean age 26.9 years, three males; see Table 1). Subjects were seated in an electrically and acoustically shielded room. Their task was to press a button with the index finger (two 5-min blocks for each index finger) in a self-paced manner approximately once in every 4 s. In order to mask the weak sounds coming from the button press, Gaussian white noise was binaurally presented through headphones at an intensity of 75 dB (SPL). Half of the subjects started with the right hand and the other half with the left hand. The same procedure was administered twice with the sighted subjects, four blocks in a dark room (‘dark’) to minimize the effects of visual input on brain responses, and four blocks in a normally lit room (‘light’) with the subject’s gaze fixed on a fixation point. Half of the sighted subjects were studied first in light, and then in dark, while for the other half, the order of conditions was reversed. Because the sighted subjects participated in two conditions instead of one, possible effects of learning or fatigue were studied by comparing amplitudes of different MRP components in the first and second condition with each other. The EEG (0.1–100 Hz, −3 dB points, sampling rate 250 Hz) was recorded with nose-referenced Ag/AgCl scalp electrodes, placed at the midline and over the left and right scalp areas (Fig. 1). The button press initiated a trigger pulse for MRP analysis when the button was in a half way to down position. The MRPs were off-line averaged beginning 1500 ms before and continuing 1500 ms after each button press. Epochs with EEG change exceeding 150 mV at any channel were omitted from averaging. Data were digitally filtered (lowpass 30 Hz) by an FFT-filter. The MRP amplitudes were measured as the mean amplitudes over 200-ms time periods (see Fig. 1). The MP amplitude was not measured Table 1 Blind subjects’ background Subject Onset

Cause of blindness

Clinical condition

VEP

S1

Congenital

Totally blind

–

S2 S3

Congenital 6 months

,1 year ,2 years ,2 years

S7

,5 years

RoP

Totally blind Totally blind, LP until 1 year Some LP Totally blind In one eye some LP Totally blind, LP until 5 years

– No resp.

S4 S5 S6

Mothers’ rubella during pregnancy (MRdP) MRdP Retinopathy of Prematurity (RoP) RoP RoP MRdP

No resp. – No resp. No resp.

Visual evoked potentials (VEPs) were previously [9] recorded from subjects who had some diffuse light perception (LP) (however they did not have contour or pattern vision).

because of difficulties in identifying this component in single-subject data. In order to compare the hemispheric (left hemisphere: electrodes, F3, C3, P3, and O1′; right hemisphere: F4, C4, P4, and O2′) and anterior-posterior (all, except EOG and Fpz electrodes; see Fig. 1) scalp distributions of the MRP components between the groups, the measured MRP amplitudes were normalized. This was done separately for each subject and each measurement period by dividing the amplitude at each electrode by the square root of the sum of the squared amplitudes at the electrodes included in the analysis [1,9]. Three- and two-way ANOVAs for repeated measures were used in the statistical analyses. In the results, the reported significance levels for the F values from ANOVAs with BMDP 2V statistical software are Greenhouse-Geisser corrected where appropriate. In the blind and in the sighted in light and in dark, the RP was maximal at Fz while the NS′ was largest at the frontocentral scalp areas over the hemisphere contralateral to the hand used for the button press (Fig. 1). NS′ amplitudes (all electrodes except the Fpz and EOG included in the ANOVA) were significantly larger in the blind than in the sighted subjects (in light, F(1,12) = 7.65, P , 0.05; in dark F(1,12) = 9.40, P , 0.01; see Figs. 1 and 2), and the RP was larger in the blind than in the sighted subjects in dark (F(1,12) = 8.88, P , 0.05; Figs. 1 and 2). In the sighted subjects, there were no significant differences between the MRP amplitudes elicited in light and dark. In addition, the comparison of the first and second condition of the sighted (independent of being measured in light or dark) revealed no significant differences between these conditions. The postmovement positive wave (measured over 200–400 ms after button press) showed no differences between the blind and sighted or conditions. ANOVAs for normalized amplitudes of the different MRP components revealed no differences between the two groups either in anterior-posterior or leftright scalp distributions. The larger RP and NS′ potentials in the blind than in the sighted suggest that brain activity associated with preparation and initiation of self-paced movements is increased in the blind compared with the sighted. The difference between the blind and the sighted was not reduced when the MRPs of the sighted subjects were recorded in a lit room. This indicates that the difference in MRPs between the blind and sighted subjects was not caused by an MRP decrement in the sighted because of an inhibitory effect of the light or some other visual input on MRPs. The enhanced MRPs in the blind found in the present study might reflect the blind individuals’ increased motortactile rehearsal. This rehearsal might have altered the hand representation area in the motor cortex. Previous studies have shown that with practice, the representation of fingers that have been used in training of tapping sequences expands in the primary motor cortex [7]. Thus, the enhanced NS′ amplitudes elicited by the button-press task in the blind might reflect a similar expansion of finger representations in

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Fig. 1. MRPs associated with self-paced button presses with the left and right index finger in the blind (thick solid line), in the sighted in dark (thin solid line), and in the sighted in light (thin dotted line). O1′ electrode is located halfway between Oz and O1 and O2′ halfway between Oz and O2. The other EEG electrodes were placed according to the International 10–20 System. The button press occurred at the vertical mV calibration bar. All amplitudes were measured in reference to the mean amplitude over a period of 1200–1500 ms prior to the button press (a). The RP was measured as the mean amplitude over 600–800 ms (b) and the NS′ as the mean amplitude over 200–400 ms (c) before the button press. Also the amplitude 200–400 ms (d) after the button press, and its difference from NS′ was measured.

motor cortex. Accordingly, Pascual-Leone et al. [14] suggested that in proficient blind Braille readers, the cortical representation area of the first dorsal interosseous muscle of the reading hand was significantly larger than that of the same muscle of the non-reading hand or that of either hand of the sighted control subjects. Behavioral studies, which have shown that the blind subjects are superior to the sighted subjects in tactile-motor tasks (see, however, [13] for contradictory results; for a review, see [15]) support the findings obtained by brain activity measurements. For example, when exploring object shapes, blind adults use more effective scanning techniques than sighted adults,

and the blind individuals′ judgments of the curvature shape were more accurate than those of the sighted [3]. Unlike in the auditory and somatosensory tasks of the previous studies [1,9,10,20], no scalp-distribution differences were found between the blind and sighted in the responses elicited in the present motor task. This suggests that the occipital areas of the blind do not participate in the movement control. In summary, the present results show that the RP and NS′ amplitudes preceding a self-paced movement are enhanced in blind humans. However, no MRP distribution differences were found between the blind and sighted subjects. Thus, the cortical control of motor functions may be altered within the blind subjects′ motor system but motor functions do not spread in the blind into the cortical areas normally serving the visual modality. This study was supported by the University of Helsinki and the Academy of Finland. We thank Dr. Heikki Ha¨ma¨la¨inen for his comments on the previous version of the manuscript, and Kalevi Reinikainen and Teemu Rinne for their technical assistance.

Fig. 2. Mean amplitudes (and standard errors) of different MRP components at the C3 electrode over the left-hemisphere motor areas contralateral to the right index finger used for button presses.

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