Brain, Vol. 122, No. 9, 1721-1729,
September 1999
© 1999 Oxford University Press
Interhemispheric asymmetries in the perception of unimanual and bimanual cutaneous stimuli
A study using transcranial magnetic stimulation
1 IRCCS `S. Lucia', 2 AFAR CRCCS Ospedale Fatebenefratelli, Isola Tiberina, 3 Clinica Neurologica, Università di Roma Tor Vergata, Rome and 4 IRCCS `S. Giovanni di Dio', Istituto Sacro Cuore, Brescia, Italy
Correspondence to:
Raimondo Traversa, MD, IRCCS `S. Lucia', Via Ardeatina, 306, 00194 Rome, Italy
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Abstract |
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Previous studies have shown that transcranial magnetic stimulation (TMS) of the sensorimotor cortex can induce a suppression of cutaneous perception from the fingers of the contralateral hand. In this work, 17 normal subjects were submitted to focal TMS of frontal and parietal scalp sites of each hemisphere. TMS was delivered at two interstimulus intervals (20 and 40 ms) following a cutaneous electrical stimulation of the first, third and fifth digits of either hand or both hands near the subjective threshold of perception. The aim of our study was to investigate whether TMS could detect an asymmetrical hemispheric specialization in the sensory perception of unimanual and bimanual, ipsilateral and contralateral sensory stimuli. At each interpulse interval, the right parietal cortex was significantly more sensitive to TMS interference with stimulus detection for both contralateral and ipsilateral stimuli compared with the left parietal cortex. These effects were mainly evident during bimanual discrimination tasks. Our results are indicative of an interhemispheric difference in the detection of cutaneous sensation, showing right hemispheric prevalence in the perception of contralateral as well as of ipsilateral stimuli. They provide neurophysiological support in normal humans to the clinical evidence which indicates that right hemisphere lesions can indeed produce deficits in the perception of ipsilateral sensory stimuli.
transcranial magnetic stimulation; somatosensory stimulation; hemispheric asymmetry; right hemisphere; ipsilateral space
F = frontal; P = parietal; TMS = transcranial magnetic stimulation
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Introduction |
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In addition to its traditional use as a technique for studying the excitability and viability of the corticospinal pathways, transcranial magnetic stimulation (TMS) can transiently interfere with the normal activity that occurs during the performance of a task, thus allowing the investigation of certain specific cognitive areas (Walsh and Cowey, 1998
). In this field, TMS has been used to block the perception of visual stimuli (Amassian et al., 1989, 1993a, Amassian et al., b), determine transient speech arrest (Pascual-Leone et al., 1991), induce contralateral visual extinctions (Pascual-Leone et al., 1994), delay the onset of a voluntary movement (Day et al., 1989) and interfere with the organization of future elements in complex motor sequences (Gerloff et al., 1997, 1998). In addition, it has been demonstrated previously (Cohen et al., 1991; Seyal et al., 1992, 1997) that TMS of the sensorimotor cortex produces suppression of perception of a threshold cutaneous stimulus from the fingers of the contralateral hand. The roles of different cortical regions in perceiving somatosensory stimuli are still poorly defined, and the effects of TMS disruption of the two hemispheres on bimanual discrimination and ipsilateral sensory perception in normal subjects have not been addressed previously.
The aim of this study was therefore to investigate whether interference by TMS with the function of critical areas of the two hemispheres can identify an asymmetrical hemispheric specialization in sensory perception of unimanual versus bimanual and of ipsilateral versus contralateral sensory stimuli. In particular, the power of TMS as a `virtual lesion' technique can be used to verify in normal humans, in the context of bulk of clinical and neuropsychological studies (Critchley, 1953; Weintraub and Mesulam, 1987; De Renzi et al., 1989; Feinberg et al., 1990), the dominant role of the right hemisphere in the distribution of attention to the ipsilateral space, as suggested by the fact that right hemisphere lesions can produce deficits in sensory perception not only from the affected side of the body but also from the normal side.
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Subjects and methods |
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We studied the effects of TMS on the detection of somatosensory stimuli in 17 normal volunteers (11 men and six women) aged 27–40 years (mean 34.57 ± 14 years). All subjects were right-handed according to the Edinburgh inventory (Oldfield, 1971
). They gave informed consent to participation in the study, which was approved by the ethical committee of IRCCS, S. Lucia.
Transcranial magnetic stimulation
TMS was carried out with a Novametrix MagStim 200 magnetic stimulator connected to a focal figure 8-shaped coil (each wing 70 mm in diameter). The excitability threshold was determined separately for the two hemispheres. TMS intensity was progressively increased, starting from 30% of maximum output, in 2% steps until it reached a level capable of inducing motor evoked potentials of >50 µV peak-to-peak amplitude in the contralateral abductor pollicis brevis muscle in at least five of 10 trials with the coil centred over the optimal scalp position (= hot spot) (Rossini et al., 1994).
Then, two scalp sites located 4 cm frontal (frontal site) and 4 cm posterior (parietal site) to the `hot spot' were identified and stimulated at threshold intensity during finger stimulation. Therefore, the stimulus had an intensity sufficient to reach the brain surface but was distant enough from the primary motor cortex not to elicit an arm/hand movement. Surface electrodes were placed over the thenar eminence bilaterally and EMG activity was monitored during the experiment. The coil was held parallel to the subject's scalp and oriented at ~45° with respect to the line connecting the opposite frontal or parietal scalp sites. The direction of current flow in the coil was such that current flow in the underlying cortex was posterior to anterior, as indicated in Fig. 1.
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Somatosensory stimulation
For cutaneous stimulation, pairs of surface electrodes were applied around the first, third and fifth fingers of each hand (cathode on the second phalanx, anode on the third phalanx) (Fig. 1
). Current pulses, with duration of 0.3 ms, were delivered using a dedicated electronic device that was able to trigger the magnetic stimulator. Starting with subthreshold stimuli, the intensity of stimulation was gradually increased until it was set slightly above the subjective threshold for perception. Stimulus current was then maintained at this intensity for the duration of the experiment. Finger stimuli were given in sets of 45 trials (15 each to the left hand alone, right hand alone or both hands simultaneously).
Task
Finger stimuli were delivered in a random sequence either on one side (unimanual discrimination tasks) or bilaterally (in this case to homologous digits; bimanual discrimination tasks). TMS followed cutaneous stimulation at two intervals: 40 ms in all subjects and 20 ms in six of the subjects.
Paired stimuli (finger stimulus followed by magnetic pulse) were delivered in four blocks of 45 stimulus pairs for each scalp site. Following the presentation of individual stimulus pairs, the subject had to indicate whether he or she perceived any finger stimulation and to localize it. The order of the trials, and thus of the stimulated scalp positions, was randomized and counterbalanced across subjects.
The number of 90 replications to be performed for each hemisphere was determined in advance in order to be sensitive to a difference of >15% between baseline (without TMS) and the scalp site at which the largest percentage of total errors might occur. Such a difference was arbitrarily considered as a relevant sign of TMS interference. The level of significance, 
, was set at 0.05 and the power 1 – ß at 0.80.
Control trials
Baseline trials (finger stimuli without TMS interference), randomly intermingled with test conditions, were also gathered in four blocks (a control trial for each of the two scalp positions in each hemisphere) with the magnetic coil still held over each scalp position, to control for non-specific effects of the experimental procedure (i.e. learning, spatial attention).
Trials in which TMS was applied without cutaneous stimulation were used as a measure of the subject's state of alertness.
To test for any possible non-specific effects of sound associated with the magnetic pulse, trigeminal activation and head muscle contraction on the perception of cutaneous stimuli, focal TMS was also applied in five subjects to scalp positions centred on the left/right prefrontal and occipital areas (positions Fp1, Fp2, O1, O2 of the 10–20 EEG system).
Data analysis
The mean percentages of errors in the different experimental conditions that were referred to both incorrect responses (stimulus dislocated to a different digit or contralateral hand) and omitted responses (stimulus suppression), were analysed by means of repeated measures analysis of variance, evaluating the effect of side (contralateral versus ipsilateral), stimulus (unimanual versus bimanual stimulation) and scalp position (right frontal and parietal, left frontal and parietal) as within-subject factors. The significance of the effects was assessed using a multivariate approach for repeated measures, specifically by means of Pillai's trace, the most robust and sensitive multivariate test (Olsen, 1976). Post hoc Tukey's comparison was used to test differences between the different levels of factors.
Paired t tests were used to compare motor threshold intensities of the two hemispheres, and ANOVA (analysis of variance) for repeated measures to compare the mean percentages of errors in control trials (baseline versus prefrontal versus occipital TMS).
For all statistical analyses the level of significance was set at P < 0.05.
MRI scan
In a single subject, the frontal (F) and parietal (P) sites were marked on the skull using capsules containing soya oil. A T1-weighted image was produced with a Siemens 1.5 T Vision Magnetom MR system (Erlangen, Germany; MPRAGE sequence, 1 mm isotropic voxels). As can be seen in Fig. 2A and B, a line parallel to the capsule and tangential to the surface of the skull and a perpendicular line originating in the centre of the capsule were drawn. These lines indicate, respectively, the coil orientation and the centre of the area where the induced field was at its maximum.
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The external landmark sites were labelled and the underlying brain cortex was identified with DISPLAY (Brain Imaging Center, Montreal Neurological Institute, McGill University), a program that permits labelling of a region of interest on each slice of the MRI volume and allows the three-dimensional reconstruction of the brain surface (Fig 2C
). The three-dimensional surface of the brain was created by using a three-dimensional model-based surface deformation algorithm (MacDonald, 1998). Pertinent sulcal landmarks were identified on the hemisphere to assist the definition of sites; the F site was over the portion of the inferior frontal sulcus located superior to the diagonal sulcus, while the P site was over the intraparietal sulcus at the level of the sulcus intermedius primus.
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Results |
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Control conditions
The mean percentages of errors in the recognition of uni- and bimanual stimuli in baseline trials (without TMS) and during prefrontal and occipital TMS are summarized in Table 1
. There were no significant differences in the recognition of uni- versus bimanual stimuli (P > 0.05). The percentage of errors during prefrontal and occipital TMS was not significantly different from that of trials without TMS (P > 0.05).
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In addition, the error rate was not significantly different between the four blocks of baseline trials, thus excluding the presence of any within-session learning effects.
Right and left hemisphere TMS
None of the subjects reported tingling sensations or paraesthesias in the arm and hand following the magnetic stimulus.
Excitability thresholds, and hence the TMS intensity used, for right and left hemispheres were 47.8 ± 8.2 and 47.2 ± 7.8%, respectively, without a significant interhemispheric threshold difference.
For each experimental condition, no significant differences were detected between the two tested interstimulus intervals (20 and 40 ms), either alone or in combination with the other factors. For this reason we did not consider the interstimulus interval as an additional factor in the ANOVA. In all trials the incorrect responses were virtually absent and therefore only the omitted responses were analysed.
Three out of 17 subjects were excluded from the analysis because of an elevated number of stimulus omissions during baseline; this was probably due to the fact that in these cases the intensity of sensory stimulation was adjusted to a value too low for appropriate stimulus detection, thus precluding any comparative analysis of the interfering effects of TMS.
Figure 3 shows the mean percentages of errors during uni- and bimanual stimulation as a function of the stimulated scalp sites, and Table 2 reports the results of the three-way analysis of variance.
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The significant main effect of scalp position suggests that right hemisphere TMS is more effective than TMS of corresponding sites on the left hemisphere in inducing suppression of cutaneous stimuli. In particular, post hoc tests revealed that the right parietal cortex is significantly more sensitive to TMS interference with stimulus detection compared with the contralateral parietal cortex (P < 0.001).
In addition, the presence of a significant main effect of type of stimulation suggests that bilateral cutaneous stimuli are more susceptible to errors than are unilateral stimuli (P = 0.002).
This finding is better explained by the significant interaction stimulation x scalp position, indicating that the differences among TMS sites vary according to the type of peripheral stimulation task (uni- or bimanual); post hoc tests showed that peripheral sensory stimuli, regardless of whether they were applied to contralateral or ipsilateral hemispace, were more readily disrupted by right parietal TMS, and this effect was significantly more evident during bimanual discrimination tasks. On the other hand, the difference between single and double stimulation tasks was significant only during right parietal TMS (Fig. 3).
The significant interaction TMS sites x side x type of stimulation is represented in Fig. 4, in which the effects of TMS are shown according to the peripheral stimulation task and the stimulus side. Right parietal TMS produced significantly greater attenuation of perception of both contralateral and ipsilateral stimuli than left parietal TMS. In addition, TMS over the different (frontal and parietal) sites had distinct effects depending on the peripheral stimulation task: post hoc tests showed that after parietal TMS the interhemispheric difference in perception of contralateral and ipsilateral stimuli was significant only in the bilateral modality (P = 0.0004 and P = 0.003, respectively). No significant interhemispheric differences for perception of contralateral and ipsilateral stimuli were found after frontal TMS, during either unimanual or bimanual discrimination tasks.
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Discussion |
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The main result of the present study is that the right parietal cortex is more sensitive to TMS interference with tactile stimulus detection, not only for contralateral but also for ipsilateral stimuli, compared with the left parietal cortex. In addition, a bimanual discrimination task seems to be more readily disrupted than a unimanual task, and this effect is evident only during right parietal TMS.
Previous studies have shown that the cortical processing required for the perception of cutaneous sensation from one hand can be transiently disrupted by TMS of the contralateral sensorimotor cortex (Cohen et al., 1991; Seyal et al., 1992, 1997). These studies, however, addressed only the effects of TMS applied over the hemisphere contralateral to the investigated hand. Interhemispheric differences in the perception of uni- or bimanual, ipsi- and contralateral finger stimuli have not been investigated previously.
A novel aspect of our study is the presence of hemispheric asymmetry in sensory perception, as evidenced by the greater susceptibility of the right hemisphere to TMS interference in the processing of both contralateral and ipsilateral stimuli. This suggests that the representation of not only contralateral but also ipsilateral tactile space is greater in the right hemisphere, which therefore would provide the major contribution to the overall neural representation of egocentric space.
Since we did not find any significant interhemispheric asymmetry in motor thresholds, our findings cannot be accounted for by the different TMS intensities used for the two hemispheres. This result is in accord with the majority of data reported in the literature (Mortifee et al., 1994; Cicinelli et al., 1997; Traversa et al., 1997; Rossini and Rossi, 1998), even if some authors have described a slightly higher excitability threshold for the right hemisphere (Cantello et al., 1991; Macdonnell et al., 1991; Triggs et al., 1997).
On the other hand, non-specific TMS effects such as the effect on global attention due to scalp muscle contraction or TMS-associated sound and blinking cannot explain our results, since TMS of other control positions (prefrontal and occipital), whose stimulation produces even more discomfort due to trigeminal and facial muscle activation, did not result in a significant increment in error induction.
A proposed interpretation of the interference by TMS with cutaneous sensory perception refers to a gating effect due to a TMS-induced finger movement (Starr and Cohen, 1985; Tapia et al., 1987). However, this does not seem to apply to our protocol, considering that we stimulated frontal and parietal sites other than the hot spot and that we did not record any muscle activity on EMG monitoring. These findings are in accord with those reported in other studies (Cohen et al., 1991).
In the present study, sensory perception was attenuated by single-pulse TMS applied even at an interstimulus interval of 40 ms, a period longer than the minimum afferent conduction time from the digits to the sensory cortex, as known from the somatosensory evoked potential latency (Rossini et al., 1987). Thus, if we assume that late cortical events are necessary for the conscious detection of somatosensory stimuli, it is plausible that interference by TMS in sensory perception occurred at a cortical level. This hypothesis is supported by the use of threshold-intensity TMS. It is, in fact, well accepted that, at threshold intensities, focal magnetic stimulation activates neurons trans-synaptically through cortico-cortical connections, and that this effect is limited to neurons within the grey matter (Day et al., 1988; Zarola et al., 1989).
In apparent contrast with our findings, Seyal and colleagues found increased sensitivity (instead of reduced perception) to ipsilateral peripheral stimuli following TMS of the right parietal lobe (Seyal et al., 1995). On the other hand, the approach used in the two studies is different. In Seyal's protocol, interfering TMS of only one hemisphere preceded cutaneous stimulation, no comparison was made of bimanual versus unimanual stimuli detection, the intensities of stimulation were higher, and performance was measured using a continuous dependent variable (changes in sensory threshold) rather than as correct responses (stimulus detected versus stimulus not detected). Comparing the results of the two studies, one can hypothesize that a magnetic stimulus delivered to the right parietal cortex can increase or decrease the discrimination of cutaneous ipsilateral stimuli depending on the time it is applied with reference to the electrical stimulus, and hence to the beginning of the crucial neural operations involved in the contralateral or ipsilateral sensory processing. It has been reported that the effects of TMS in anatomically connected regions can last even longer than at the site of stimulation (Ilmoniemi et al., 1997). With respect to this, it is worth noting that the phenomenon of enhancement of ipsilateral sensory perception after right parietal lobe disruption probably involves the disinhibition of contralateral, symmetrical, cortical structures via transcallosal connections (Seyal et al., 1995). Therefore, one can speculate that the perception of ipsilateral cutaneous stimuli can be suppressed provided that the magnetic pulse is timed to coincide with the arrival of the afferent volley at the primary sensory or association cortex (i.e. if cutaneous stimuli are delivered prior to TMS, as in our protocol); in this case, the contralateral parietal cortex disinhibition would appear too late to produce its effects on the already disrupted ipsilateral stimuli. On the other hand, when cutaneous stimuli are delivered after the magnetic pulse (Seyal et al., 1995), recovery from the colliding effects of TMS on ipsilateral sensory volleys probably takes <50 ms because of the co-ordinated activity in the other contralateral regions involved in the task. As a consequence, after right parietal TMS, left parietal cortex disinhibition outlasts and overwhelms right parietal disruption.
Another possibility is that an intensity of TMS higher than that used in our study is necessary for the producion of contralateral parietal cortex disinhibition.
The analysis of the interference effects showed that hemispheric asymmetry in sensory perception was evident only after parietal TMS, whereas stimulation of frontal scalp sites, though also interfering with the perception of contralateral and ipsilateral stimuli, did not reveal any hemispheric asymmetry in the representation of personal space. A major question is, therefore, which anatomical structures are stimulated when TMS is applied to frontal and parietal scalp sites measured relative to the hot spot, as in our protocol. This was estimated by coregistration of TMS scalp sites with MRI scans, and provided evidence that the parietal scalp site was situated in a region overlying the intraparietal sulcus in the posterior parietal lobe and the frontal site lay over the inferior frontal sulcus. These regions constitute one of the major cortical components of the anatomical–functional networks subserving spatial distribution of attention, and lesion of them can cause neglect or extinction of stimuli delivered in the contralateral space (Mesulam, 1981; Heilman, 1993).
Our findings confirm the general hypothesis that, in man, lesions on the lateral surface of the frontal lobe may be associated with deficits in the exploration of contralateral space (Husain and Kennard, 1996; Damasio et al., 1980). In these cases, the lesion site does not show a constant pattern of hemispheric localization, and some investigators have even found an unexpected predominance of left-sided lesions in frontal neglect (Damasio et al., 1980). The lack of hemispheric differences in contralateral extinctions observed after frontal TMS is therefore consistent with these suggestions. On the other hand, neglect and extinctions following lesions of the parietal lobes are more closely associated with disruption of the functioning of the right hemisphere. In normal individuals, conscious perception of somatosensory stimuli seems to be organized in an asymmetrical pattern (with right hemisphere dominance) in the posterior parietal lobe, which is involved in the representation of personal and extrapersonal space (Bisiach and Vallar, 1988; Vallar et al., 1994). As a result of perceptual processing, somatotopically coded information is mapped onto an egocentric body representation, a process that requires the activity of bilaterally located neural structures that process sensory information from the two sides of space and body (Bisiach and Vallar, 1988; Vallar et al., 1993).
In accordance with this background, we can hypothesize that the deficits in contralateral and ipsilateral space perception observed after right parietal TMS do not have a sensory component but rather reflect disturbances at a perceptual–attentional level. This is confirmed by the significant hemispheric asymmetry observed in TMS disruption of bimanual discrimination tasks.
The bimanual discrimination task represents a condition demanding more attention than the unimanual task and it allows the demonstration of perceptual deficits not evidenced by single stimulation. Its disruption by temporary TMS interference of one hemisphere determines a condition similar to extinction, the phenomenon whereby patients with damage to the CNS fail to report one of two stimuli in conditions of simultaneous stimulation while the perception of single stimuli is preserved (Gainotti et al., 1989; Vallar et al., 1994). Extinction, like neglect, is closely associated with dysfunction of the right hemisphere, and it has been interpreted as an attentional deficit occurring with reference to spatial (e.g. egocentric) frames of reference rather than to the anatomical organization of the sensory afferent pathways (Vallar et al., 1993). Contralateral extinction is a common and expected finding after a right hemisphere lesion. Extinction on the side of the body ipsilateral to the affected hemisphere is much less common and implies an attentional disturbance with respect to ipsilateral hemispace. Our findings suggest that it is also closely associated with right parietal disruption. These results are in line with some clinical reports describing the occurrence of ipsilateral extinctions following right brain damage. Critchley and colleagues first noted that unilaterally brain-damaged patients, in conditions of double simultaneous stimulation, may show inattention to the normal side of the body (Critchley et al., 1953). Weintraub and Mesulam reported the presence of signs of inattention for the right space, in addition to the classical left neglect syndrome, in right brain-damaged patients investigated with a visual cancellation test (Weintraub and Mesulam, 1987). Similar findings were reported by Feinberg and colleagues and De Renzi and colleagues in patients showing damage to the right side of the brain and contralateral neglect, but not in subjects with right brain damage without neglect or in patients with left hemisphere lesions (De Renzi et al., 1989; Feinberg et al., 1990). Other studies, including investigations of acute hemispheric incapacitation through the intracarotid sodium amytal procedure (Meador et al., 1988) and PET (Pardo et al., 1991), have confirmed that the right hemisphere can be activated regardless of the side of stimulation, reflecting its unique ability also to exert attentional control on the ipsilateral space.
Our results provide a clear neurophysiological demonstration of these observations in normal humans, in whom factors that are usually encountered in brain-damaged patients, such as a generalized cognitive impairment, unco-operativeness and the presence of multiple lesions, cannot account for specific disturbances of attention.
In conclusion, our study shows a right hemispheric prevalence in the processing of bimanual and ipsilateral somatosensory stimuli and emphasizes the role of TMS as a promising technique for the study of the lateralization and locations of brain functions.
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Received October 21, 1998. Revised March 10, 1999. Accepted March 10, 1999.
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Y. Oshiro, A. S. Quevedo, J. G. McHaffie, R. A. Kraft, and R. C. Coghill Brain Mechanisms Supporting Spatial Discrimination of Pain J. Neurosci., March 28, 2007; 27(13): 3388 - 3394. [Abstract] [Full Text] [PDF]
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M. Oliveri, P. Turriziani, G.A. Carlesimo, G. Koch, F. Tomaiuolo, M. Panella, and C. Caltagirone Parieto-frontal Interactions in Visual-object and Visual-spatial Working Memory: Evidence from Transcranial Magnetic Stimulation Cereb Cortex, July 1, 2001; 11(7): 606 - 618. [Abstract] [Full Text] [PDF]
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