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Research Articles, Development/Plasticity/Repair

The Extent of Task Specificity for Visual and Tactile Sequences in the Auditory Cortex of the Deaf and Hard of Hearing

M. Zimmermann, P. Mostowski, P. Rutkowski, P. Tomaszewski, P. Krzysztofiak, K. Jednoróg, A. Marchewka and M. Szwed
Journal of Neuroscience 24 November 2021, 41 (47) 9720-9731; https://doi.org/10.1523/JNEUROSCI.2527-20.2021
M. Zimmermann
1Institute of Psychology, Jagiellonian University, 30-060 Krakow, Poland
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P. Mostowski
6Section for Sign Linguistics, University of Warsaw, 00-927 Warsaw, Poland
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P. Rutkowski
6Section for Sign Linguistics, University of Warsaw, 00-927 Warsaw, Poland
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P. Tomaszewski
4Polish Sign Language and Deaf Communication Research Laboratory, Faculty of Psychology, University of Warsaw, 00-183 Warsaw, Poland
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P. Krzysztofiak
5Faculty of Psychology, University of Social Sciences and Humanities, 03-815 Warsaw, Poland
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K. Jednoróg
3Laboratory of Language Neurobiology, Nencki Institute for Experimental Biology, 02-093 Warsaw, Poland
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A. Marchewka
2Laboratory of Brain Imaging, Nencki Institute for Experimental Biology, 02-093 Warsaw, Poland
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M. Szwed
1Institute of Psychology, Jagiellonian University, 30-060 Krakow, Poland
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  • Figure 1.
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    Figure 1.

    Experimental design. The experimental design involved eight conditions: two sensory modalities, tactile and visual; two types of stimuli (dimensions), temporal and spatial; and two levels of task versus no-task (i.e., doing a task vs passive observation).

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    Figure 2.

    Experimental design and behavioral results. A, Experimental tasks. Temporal sequences: series of six flashes (white circles) presented on the screen, or a series of six tactile stimuli presented on four fingers of both hands for longer or shorter periods of time (50 or 200 ms with 100-ms blank interval between). The temporal sequences control condition involved presentation of a temporally regular series of stimuli (visual or tactile). Each stimulus was presented for the same duration (125 ms with a 100-ms blank interval between). B, Behavioral results. Performance in the fMRI (the accuracy of the same/different decision in the experimental task). Behavioral results were all significantly above chance level. There were significant differences between groups (F = 12.57, p < 0.001), but there were no significant differences between modalities or between types of task (p > 0.05). We found a significant effect of interaction of dimension and modality (F(1,142) = 10.02, p < 0.01), and a significant effect of interaction between group and dimension (F(1,142) = 11.53, p < 0.01); *p < 0.05, **p < 0.01, ***p < 0.001. Error bars represent SEM.

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    Figure 3.

    A, Visual and tactile processing lead to auditory cortex recruitment in the deaf and hard of hearing but not in the hearing. The effect of group (deaf/hard of hearing ≥ hearing) peaks in the right auditory cortex MNI = 60, −20, 1, t = 6.11. B, Interaction group × dimension in the right superior and middle temporal gyrus (MNI = 66, −32, −12, t = 6.32).

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    Figure 4.

    A, Task-specific effect for temporal stimuli (temporal sequences task > temporal sequences no-task) for both modalities is reflected in an activation within the right auditory cortex MNI = 58, −22, −4, t = 5.43). B, Visual and tactile task activation peaks in a very similar region within the right auditory cortex. The overlap (yellow) between visual (red) and tactile (green) temporal sequences (for task–no-task condition) contains 87% of the tactile activation cluster. Temporal sequences and tactile temporal sequences (relative to no-task condition, conjunction) peaking in the superior temporal gyrus (MNI = 52, −18, −6, t = 3.85). Visually induced activation is more spread out across the auditory cortex than tactile activation. C, Comparison between temporal and spatial sequences discrimination task (relative to no-task) in both modalities revealed an activation cluster within right auditory cortex in deaf and hard of hearing subjects (temporal sequences > spatial sequences × task > no task) peak MNI = 60, −22, 4, t = 4.18. SVC analysis, threshold: p < 0.05, voxel-wise, FWE. All effects (A–C) were also equally significant as corrected within an alternative, anatomically defined ROI: the right superior temporal gyrus mask (neuromorphometrics); p < 0.005 voxel-wise, p < 0.05 cluster-wise, FWE corrected.

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    Figure 5.

    Results of the functional ROI analyses. The ROI was defined around the peak of activation (as revealed in the previous study) for the contrast: the visual rhythms condition versus the visual control condition. A, ROI analysis revealed a significant task-specific activation for temporal sequences versus temporal control condition in both the visual and tactile modalities. This effect is specific for the temporal task but not for the spatial task. The analysis revealed a significant effect of interaction: temporal sequences relative to spatial sequences (task vs no-task). B, No significant activation within the ROI in the hearing subjects. Significance: *p < 0.05, **p < 0.01, ***p < 0.001. Error bars represent SEM.

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    Figure 6.

    Results of the ROI analysis in which activations in the auditory cortex induced by visual temporal sequences (visual rhythms) and tactile temporal sequences were used as independent localizers for each other. A, ROIs for comparison between visual conditions were defined based on tactile temporal sequences versus regular visual stimulation (no-task) contrast. ROI analysis revealed a significant difference between the temporal visual sequence discrimination task and the temporal visual control condition. B, ROIs for comparison between tactile tasks were defined based on visual temporal sequences versus regular visual stimulation (no-task) contrast. ROI analysis revealed a significant difference between the temporal tactile sequence discrimination task and the temporal tactile control condition: *p < 0.05, **p < 0.01, ***p < 0.001. Error bars represent SEM.

Tables

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    Table 1.

    Deaf and hard of hearing participants

    GeneralDeafnessHearing aids / cochlear implants
    1234567891011
    AgeSexLevel of deafnessDiagnosisCause of deafnessDid you ever use hearing aids in the past?Are you using hearing aids use now?How well do you understand speech when using hearing aids?How well are you able to understand speech without seeing the person talking?Cochlear implant
    137F90 dBProfound deafnessMedical mistakeYesYesWellPoorNo
    230F90–119 dBProfound deafnessUnknownYesYesModerateNoNo
    319F90–119 dBProfound deafnessGenetic defectYesNoModerateNoNo
    426F90–119 dBProfound deafnessUnknownYesYesModerateNoNo
    541M> 120 dBAbsolute deafnessUnknownNoNo–NoNo
    626M90–119 dBProfound deafnessGenetic defectYesNoPoorNoNo
    742F90–119 dBProfound deafnessUnknownYesYesPoorNoNo
    825F90–119 dBProfound deafnessUnknownYesNoWellPoorNo
    924M> 120 dBAbsolute deafnessGenetic defectNoNo–NoNo
    1035F115 dBProfound deafnessGenetic defectYesYesPoorNoNo
    1130M90–119 dBProfound deafnessUnknownYesYesPoorModerateNo
    1221M90–119 dBProfound deafnessUnknownYesYesWellModerateNo
    1323M90–119 dBProfound deafnessUnknownYesNoWellNoNo
    1421F100 dBProfound deafnessUnknownYesYesWellPoorNo
    1534M> 120 dBAbsolute deafnessGenetic defectNoNo–NoNo
    1623M85–90 dBProfound deafnessGenetic defectYesNoWellWellNo
    1723F90–119 dBProfound deafnessGenetic defectYesNoModerateNoNo
    1831F90–119 dBProfound deafnessGenetic defectYesNoWellPoorNo
    1940F90–119 dBProfound deafnessUnknownYesYesPoorNoNo
    2034F90–119 dBProfound deafnessGenetic defectNoNo–NoNo
    2129M90–119 dBProfound deafnessGenetic defectYesYesPoorNoNo
    • Options for question 9: poor, moderate, good, very good. For question 10: not at all, poor, moderate, good, very good. scale of possible answers for question 12: none, poor, moderate, good, fluent. For questions 13 and 15: never, rarely, sometimes, often, all the time.

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    Table 2.

    Deaf and hard of hearing participants

    Language
    121314151617181920
    lp.How well do you know PJM?How often did you use PJM in your childhood?In your childhood, did you speak in PJM with deaf adults?How often do you use PJM now?What is your main way of communicating now?Is your mother deaf?Is your father deaf?From whom did you learn PJM?Since when have you used PJM?
    1FluentAll the timeYesAll the timePJMNoNoTeachersSince primary school
    2FluentAll the timeYesAll the timePJMNoNoTeachersSince elementary school
    3FluentAll the timeYesAll the timePJMYesYesParentsAlways
    4FluentAll the timeYesAll the timePJMNoNoTeachersSince primary school
    5FluentOftenYesOftenPJMYesYesParentsAlways
    6FluentAll the timeYesAll the timePJMNoNoTeachersSince school
    7WellAll the timeYesAll the timePJMNoNoTeachersSince primary school
    8FluentAll the timeYesAll the timePJMNoNoTeachersSince primary school
    9FluentAll the timeYesAll the timePJMYesYesParentsAlways
    10FluentAll the timeYesAll the timePJMYesYesParentsAlways
    11FluentAll the timeYesAll the timePJMNoNoTeachersSince primary school
    12FluentAll the timeYesAll the timePJMYesYesParentsAlways
    13FluentAll the timeYesAll the timePJMYesYesParentsAlways
    14FluentAll the timeYesAll the timePJMNoNoTeachersSince school
    15FluentAll the timeYesAll the timePJMYesYesParentsAlways
    16FluentAll the timeYesAll the timePJMNoNoTeachersSince primary school
    17WellAll the timeYesAll the timePJMNoNoTeachersSince primary school
    18ModerateOftenYesOftenPJMYesYesTeachersSince primary school
    19ModerateAll the timeYesAll the timePJMNoNoTeachersSince primary school
    20FluentAll the timeYesAll the timePJMYesYesParentsAlways
    21FluentAll the timeYesAll the timePJMNoNoParentsAlways
    • Scale of possible answers for question 12: none, poor, moderate, good, fluent. For questions 13 and 15: never, rarely, sometimes, often, all the time.

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    Table 3.

    Whole-brain ANOVA main effects

    ContrastRegionHemisphereCluster sizeF valueMNI coordinates
    Main effect of modality (visual vs tactile)
    Inferior occipital gyrusRight5653408.8630−868
    18−84−10
    20−944
    Inferior occipital gyrusLeft4864326.81−16−942
    −24−886
    −18−84−12
    Central operculumRight37156.6048−1618
    52−2420
    Central operculumRight46353.6444830
    Central operculumLeft33049.17−56−2014
    −48−2420
    Main effect of task vs no task
    Superior frontal gyrusLeft72276.97−22−460
    −24−652
    −36058
    Middle frontal gyrusRight64164.0228260
    26−652
    Superior parietal lobuleRight32962.2414−6858
    Superior parietal lobuleRight36654.9338−4044
    Superior parietal lobuleLeft43841.58−32−5856
    −14−7052
    −30−5042
    Main effect of type of stimuli (temporal vs spatial)
    Supplementary motor areaLeft/right28083.37−4062
    61648
    Middle frontal gyrusLeft258371.93−282454
    −185632
    −362050
    Precentral gyrusLeft21265.29−46−454
    Middle occipital gyrus28054.4650−6824
    38−8026
    Angular gyrusLeft102050.82−48−6826
    −42−6832
    −34−7446
    Posterior cingulate gyrusLeft217150.40−8−4636
    0−4436
    Middle frontal gyrusRight35845.9732054
    52646
    38.2244254
    Supramarginal gyrusRight29042.7346−3448
    481024
    Fusiform gyrusLeft20037.62−28−42−12
    Superior frontal gyrus23734.14263450
    184644
    262438
    Main effect of group (deaf and hard of hearing vs hearing)
    Superior temporal gyrusRight9837.3060−200
    66−3010
    Supplementary motor areaLeft627.86−6−268
    • View popup
    Table 4.

    Small volume analysis

    ContrastRegionHemispheret statCluster sizeMNI coordinates
    Whole-brain effects (between group) Effect of group: deaf (hard of hearing) > hearingSuperior temporal gyrusRight6.1114560−202
    66−3010
    Interaction: dimension × group Spatial > temporal × deaf > hearingSuperior temporal gyrusRight6.3223666−3112
    Middle temporal gyrus56−3810
    Effects in the auditory cortex of the deaf and hard of hearing: temporal sequences (task > no-task, control)Superior temporal gyrusRight5.4345658−22−4
    48201
    64−304
    Interaction effect of dimension (temporal > spatial) × (task > no-task)Superior temporal gyrusRight4.1821060−22−4
    66−16−8
    54−126
    Effect of task > no-taskSuperior temporal gyrusRight3.5212956−20−4
    Whole-brain effects in the deaf and hard of hearing: effect of dimension (spatial > temporal sequences)Superior frontal gyrusLeft6.8193−22−660
    −24−652
    −36−648
    Superior frontal gyrusRight6.7849126−652
    32250
    32−248
    Middle temporal gyrusRight6.7718352−546
    Superior parietal lobuleRight6.2128534−3838
    Superior temporal gyrusRight5.5117163−3814
    Middle temporal gyrusLeft5.4214554−3812
    • View popup
    Table 5.

    Leave-one-out analysis, t values, and peak of activation for each of 21 GLM

    Temporal task > no task (Fig. 4A)Conjunction: visual and tactile temporal task > no task (Fig. 4B)Interaction: temporal > spatia × task > no task (Fig. 4C)
    Peak MNI coordinatesPeak MNI coordinatesPeak MNI coordinates
    Participant excluded from the analysist valuexyzt valuexyzt valuexyz
    15.3356−20−63.7652−18−64.3260−22−4
    25.4358−22−43.9352−18−63.8960−22−4
    35.5558−22−43.6652−18−64.1360−22−4
    45.2258−22−43.6752−18−64.3558−22−6
    55.1456−20−63.7152−18−64.2360−22−4
    65.3456−20−63.852−18−63.8860−22−4
    75.7258−22−43.952−18−63.8860−22−4
    85.4756−20−64.1552−18−64.0560−22−4
    95.3256−20−63.7952−18−63.9560−22−4
    105.2958−22−43.5752−18−64.3760−22−4
    115.0556−20−63.4852−18−64.360−22−4
    125.3756−20−64.0954−16−44.0460−22−4
    135.0756−20−63.6552−18−64.3958−22−6
    145.1856−20−63.7654−16−44.2860−22−4
    155.1958−22−43.7452−18−64.260−22−4
    165.4258−22−43.8452−18−64.1558−22−6
    175.2158−22−43.5252−18−64.1858−22−6
    185.4858−22−43.9254−16−44.0760−22−4
    195.4458−22−43.8352−18−63.660−22−4
    205.7556−20−63.7152−18−64.1960−22−4
    215.6456−20−64.0952−18−64.160−22−4
    Whole group analysis5.4358−22−43.8552−18−64.1860−22−4
    • From each of the linear models, one participant (from the group of deaf and hard of hearing individuals) has been left out.

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The Journal of Neuroscience: 41 (47)
Journal of Neuroscience
Vol. 41, Issue 47
24 Nov 2021
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The Extent of Task Specificity for Visual and Tactile Sequences in the Auditory Cortex of the Deaf and Hard of Hearing
M. Zimmermann, P. Mostowski, P. Rutkowski, P. Tomaszewski, P. Krzysztofiak, K. Jednoróg, A. Marchewka, M. Szwed
Journal of Neuroscience 24 November 2021, 41 (47) 9720-9731; DOI: 10.1523/JNEUROSCI.2527-20.2021

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The Extent of Task Specificity for Visual and Tactile Sequences in the Auditory Cortex of the Deaf and Hard of Hearing
M. Zimmermann, P. Mostowski, P. Rutkowski, P. Tomaszewski, P. Krzysztofiak, K. Jednoróg, A. Marchewka, M. Szwed
Journal of Neuroscience 24 November 2021, 41 (47) 9720-9731; DOI: 10.1523/JNEUROSCI.2527-20.2021
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Keywords

  • auditory cortex
  • cross-modal perception
  • deaf
  • fMRI
  • plasticity

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  • RE: Campbell, 2022
    Maria Zimmermann and Marcin Szwed
    Published on: 28 March 2022
  • RE: Zimmermann et al (2021)
    Ruth Campbell
    Published on: 01 February 2022
  • Published on: (28 March 2022)
    Page navigation anchor for RE: Campbell, 2022
    RE: Campbell, 2022
    • Maria Zimmermann, PhD candidate in cognitive neuroscience, Jagiellonian University
    • Other Contributors:
      • Marcin Szwed

    Campbell (2022) implies that the Auditory Cortex (AC) recruitment for visual and tactile rhythm perception in the deaf (Zimmermann et al., 2021) is not due to sensory deprivation, as we proposed, but rather to sign-language acquisition. While the issue can be decisively resolved only by new experiments that would include a control group of hearing sign-language users, we nonetheless would like to point out arguments in favour of our position. Certainly, the sign-language acquisition is an important driver of brain plasticity. We argue however that is does not explain well our findings.
    First, the effects revealed in our study are strongly right-lateralised, while language-related effects, including sign-language effects, are left-lateralised (e.g. Cardin, et al. 2020).
    Second, deaf individuals perceive different aspects of music (Good, et al. 2014, Russo, et al. 2012) through vibrotactile stimulation. Such non-linguistic experience might drive the right AC recruitment for rhythm perception.
    Third, while we agree that in sign-language body parts are touched when producing signs, one could argue that this aspect is important only for sign-language production, not perception. This issue could be framed as whether one needs perception for action. The reverse question, i.e. whether one needs action for perception is the topic of long-going debate. However, the weight of evidence in the last decade has shifted against the idea of a tight coupling between the tw...

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    Campbell (2022) implies that the Auditory Cortex (AC) recruitment for visual and tactile rhythm perception in the deaf (Zimmermann et al., 2021) is not due to sensory deprivation, as we proposed, but rather to sign-language acquisition. While the issue can be decisively resolved only by new experiments that would include a control group of hearing sign-language users, we nonetheless would like to point out arguments in favour of our position. Certainly, the sign-language acquisition is an important driver of brain plasticity. We argue however that is does not explain well our findings.
    First, the effects revealed in our study are strongly right-lateralised, while language-related effects, including sign-language effects, are left-lateralised (e.g. Cardin, et al. 2020).
    Second, deaf individuals perceive different aspects of music (Good, et al. 2014, Russo, et al. 2012) through vibrotactile stimulation. Such non-linguistic experience might drive the right AC recruitment for rhythm perception.
    Third, while we agree that in sign-language body parts are touched when producing signs, one could argue that this aspect is important only for sign-language production, not perception. This issue could be framed as whether one needs perception for action. The reverse question, i.e. whether one needs action for perception is the topic of long-going debate. However, the weight of evidence in the last decade has shifted against the idea of a tight coupling between the two (e.g. Hickok, 2014).
    As to studies on the tactile language deaf-blind population mentioned by Campbell (2022), they are a different case as their tactile modality supports both active language production and language perception. Nonetheless, such studies are definitely worthwhile and needed.

    Cardin, V., Grin, K., Vinogradova, V., & Manini, B. (2020). Crossmodal reorganisation in deafness: mechanisms for functional preservation and functional change. Neuroscience & Biobehavioral Reviews, 113, 227-237.
    Good, A., Reed, M. J., & Russo, F. A. (2014). Compensatory plasticity in the deaf brain: Effects on perception of music. Brain sciences, 4(4), 560-574.
    Hickok, G. (2014). The myth of mirror neurons: The real neuroscience of communication and cognition. W W Norton & Co.
    Russo, F. A., Ammirante, P., & Fels, D. I. (2012). Vibrotactile discrimination of musical timbre. Journal of Experimental Psychology: Human Perception and Performance, 38(4), 822.
    Zimmermann, M., Mostowski, P., Rutkowski, P., Tomaszewski, P., Krzysztofiak, P., Jednoróg, K., & Szwed, M. (2021). The extent of task specificity for visual and tactile sequences in the auditory cortex of the deaf and hard of hearing. Journal of Neuroscience, 41(47), 9720-9731.

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    Competing Interests: None declared.
  • Published on: (1 February 2022)
    Page navigation anchor for RE: Zimmermann et al (2021)
    RE: Zimmermann et al (2021)
    • Ruth Campbell, psychologist/neuropsychologist, University College London

    In discussing the similar recruitment of AC for tactile and for visual rhythmic trains in sign language users who are deaf, Zimmerman et al. (Zimmermann et al., 2021) suggest that “… tactile perception, unlike visual processing, does not seem to be directly connected with sign language acquisition…” (p 9729). Thus, they suggest their findings argue for a (general) sensory, not language-driven task-specific pattern of organization. This inference may be premature: while sign language is predominantly visual, it is also inherently tactile. Its tactility is evident in the pre-linguistic and linguistic interactions between a deaf child and Deaf caregiver (Koester et al., 2000) as well as ways in which in hands, face and body parts are touched in sign production. Tactile signing between communication partners is used – readily - by sighted Deaf people when vision is not available (ie in darkness). Tactile signing is, of course, paramount in Deaf-blind people including those whose early experience was visual (Reed et al., 1990; Willoughby et al., 2020). Its cortical correlates are still underinvestigated (Obretenova et al., 2010),.

    Koester, L. S., Brooks, L., & Traci, M. A. (2000). Tactile Contact by Deaf and Hearing Mothers During Face-to-Face Interactions With Their Infants. J Deaf Stud Deaf Educ, 5(2), 127-139. https://doi.org/10.1093/deafed/5.2.127
    Obretenova, S., Halko, M. A., Plow, E. B., Pascual-Leo...

    Show More

    In discussing the similar recruitment of AC for tactile and for visual rhythmic trains in sign language users who are deaf, Zimmerman et al. (Zimmermann et al., 2021) suggest that “… tactile perception, unlike visual processing, does not seem to be directly connected with sign language acquisition…” (p 9729). Thus, they suggest their findings argue for a (general) sensory, not language-driven task-specific pattern of organization. This inference may be premature: while sign language is predominantly visual, it is also inherently tactile. Its tactility is evident in the pre-linguistic and linguistic interactions between a deaf child and Deaf caregiver (Koester et al., 2000) as well as ways in which in hands, face and body parts are touched in sign production. Tactile signing between communication partners is used – readily - by sighted Deaf people when vision is not available (ie in darkness). Tactile signing is, of course, paramount in Deaf-blind people including those whose early experience was visual (Reed et al., 1990; Willoughby et al., 2020). Its cortical correlates are still underinvestigated (Obretenova et al., 2010),.

    Koester, L. S., Brooks, L., & Traci, M. A. (2000). Tactile Contact by Deaf and Hearing Mothers During Face-to-Face Interactions With Their Infants. J Deaf Stud Deaf Educ, 5(2), 127-139. https://doi.org/10.1093/deafed/5.2.127
    Obretenova, S., Halko, M. A., Plow, E. B., Pascual-Leone, A., & Merabet, L. B. (2010). Neuroplasticity associated with tactile language communication in a deaf-blind subject. Front Hum Neurosci, 3, 60. https://doi.org/10.3389/neuro.09.060.2009
    Reed, C. M., Delhorne, L. A., Durlach, N. I., & Fischer, S. D. (1990). A study of the tactual and visual reception of fingerspelling. J Speech Hear Res, 33(4), 786-797. https://doi.org/10.1044/jshr.3304.786
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    Competing Interests: None declared.

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