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The Somatosensory Mismatch Negativity As a Window Into Body Representations in Infancy T ⁎ Guannan Shena, , Staci M

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The Somatosensory Mismatch Negativity As a Window Into Body Representations in Infancy T ⁎ Guannan Shena, , Staci M International Journal of Psychophysiology 134 (2018) 144–150 Contents lists available at ScienceDirect International Journal of Psychophysiology journal homepage: www.elsevier.com/locate/ijpsycho The somatosensory mismatch negativity as a window into body representations in infancy T ⁎ Guannan Shena, , Staci M. Weissa, Andrew N. Meltzoffb, Peter J. Marshalla a Department of Psychology, Temple University, 1701 N. 13th Street, Philadelphia, PA 19122, USA b Institute for Learning & Brain Sciences, University of Washington, Seattle, WA, USA ABSTRACT How the body is represented in the developing brain is a topic of growing interest. The current study takes a novel approach to investigating neural body re- presentations in infants by recording somatosensory mismatch negativity (sMMN) responses elicited by tactile stimulation of different body locations. Recent research in adults has suggested that sMMN amplitude may be influenced by the relative distance between representations of the stimulated body parts in soma- tosensory cortex. The current study uses a similar paradigm to explore whether the sMMN can be elicited in infants, and to test whether the infant sMMN response is sensitive to the somatotopic organization of somatosensory cortex. Participants were healthy infants (n = 31) aged 6 and 7 months. The protocol leveraged a discontinuity in cortical somatotopic organization, whereby the representations of the neck and the face are separated by representations of the arms, the hands and the shoulder. In a double-deviant oddball protocol, stimulation of the hand (100 trials, 10% probability) and neck (100 trials, 10% probability) was interspersed among repeated stimulation of the face (800 trials, 80% probability). Waveforms showed evidence of an infant sMMN response that was significantly larger for the face/neck contrast than for the face/hand contrast. These results suggest that, for certain combinations of body parts, early pre-attentive tactile discrimination in infants may be influenced by distance between the corresponding cortical representations. The results provide the first evidence that the sMMN can be elicited in infants, and pave the way for further applications of the sMMN in studying body representations in preverbal infants. 1. Introduction 2010), vibrotactile frequency (Spackman et al., 2010), and spatial lo- cation (Shen et al., 2018b; Akatsuka et al., 2007; Naeije et al., 2016; The mismatch negativity (MMN), an event-related potential (ERP) Naeije et al., 2018; Restuccia et al., 2009). To our knowledge, there has component occurring between 100 and 200 ms after the onset of sen- been no prior published work on somatosensory mismatch responses in sory stimulus deviance, is an automatic change-detection response infants. In the current study, our initial aim was to test whether the commonly elicited using oddball paradigms in which infrequent de- sMMN could be elicited to the stimulation of different body parts in 6- viants are embedded in repeated frequent standard stimuli (see to 7-month-old infants. Since research on the developmental trajectory Näätänen et al., 2005, 2007 for review). Because the elicitation of the and maturation of mismatch responses in infancy has primarily in- MMN does not depend on explicit instructions to allocate attention or to volved auditory stimuli, the literature on the infant auditory MMN re- respond behaviorally, it has been particularly useful in developmental sponse provides the most relevant background for the current study. studies. In the auditory domain, the MMN has been widely employed in In the auditory modality, mismatch responses in infants show some the study of speech and language development in both typical (e.g., interesting differences from those of adults, with both negative mis- Conboy and Kuhl, 2011; Shafer et al., 2012) and atypical (e.g., Rinker match responses (nMMR) and positive mismatch responses (pMMR) et al., 2007; Friedrich et al., 2009) populations. It has also been used to being reported in infants (e.g., Conboy and Kuhl, 2011; Friedrich et al., examine sensitivities to different speech signals in monolingual and 2009; Kushnerenko et al., 2002; Partanen et al., 2013). Although the bilingual infants (Garcia-Sierra et al., 2011, 2016; Shafer et al., 2012). physiological mechanisms underlying the different polarities of these Although MMN responses have been observed in other sensory mod- infant responses are yet to be elucidated, it has been suggested that the alities in adults (visual: Mo et al., 2011; somatosensory: Shen et al., positive mismatch response, typically elicited between 200 and 400 ms, 2018a), much less is known about mismatch responses outside of the is a less mature response (Garcia-Sierra et al., 2016; Friedrich et al., auditory modality, and related developmental studies are very sparse. 2009), since the extent of this positivity diminishes with age (Cheng In the tactile domain, the somatosensory MMN (sMMN) can be et al., 2015; Morr et al., 2002). In general, mismatch responses are elicited in adults by deviance in various stimulus properties such as primarily positive in infants younger than 4 months of age; most infants duration (Akatsuka et al., 2005; Butler et al., 2011; Spackman et al., then begin to show negative MMN responses to salient stimulus ⁎ Corresponding author. E-mail address: [email protected] (G. Shen). https://doi.org/10.1016/j.ijpsycho.2018.10.013 Received 19 June 2018; Received in revised form 19 October 2018; Accepted 29 October 2018 Available online 30 October 2018 0167-8760/ © 2018 Elsevier B.V. All rights reserved. G. Shen et al. International Journal of Psychophysiology 134 (2018) 144–150 contrasts between 4 and 6 months of age (Cheng et al., 2015; Partanen responses are influenced by the ordering and separation of body part et al., 2013; Choudhury and Benasich, 2011; Näätänen et al., 2012). representations in SI, while later ERP responses to tactile novelty may Aside from age or neural maturity, another factor modulating the be more influenced by separation of the stimulated body parts on the 3- polarity of mismatch responses in infants is stimulus characteristics. D body surface itself. Contrasts that are more difficult to discriminate (e.g., non-native pho- In the current infant study, we employed a similar protocol to Shen netic units or contrasts with small deviance levels) tend to elicit a po- et al. (2018a) by employing the same two contrasts (face/neck and sitive response, while contrasts that were easier to discriminate elicited face/hand) used in that adult work. Our working assumption was that more adult-like negative responses in 5- to 6-month-old infants (Cheng the ordering of body parts on the tactile homunculus in SI would be et al., 2015; Friedrich et al., 2009). It has been suggested that a nega- similar in 6- and 7-month-olds as in adults. If the infant sMMN is indeed tive-going mismatch response reflects a more advanced mapping from sensitive to the distance between the representations of body parts in SI, acoustic input to phonetic representation, whereas a positive response we predicted that the sMMN elicited by the face/neck contrast would may indicate less efficient acoustic processing (Ferjan Ramírez et al., have greater amplitude than the sMMN response elicited by the face/ 2017; Garcia-Sierra et al., 2016; Shafer et al., 2011). From a clinical hand contrast. perspective, a developmentally delayed shift from a positive response to a negative adult-like mismatch response has been associated with a 2. Methods heightened risk of language impairment (Friedrich et al., 2009; Friedrich et al., 2004; Guttorm et al., 2005). 2.1. Participants In addition to the early mismatch responses, auditory oddball paradigms with infants often elicit a late discriminative negativity Thirty-three infants aged 6 or 7 months participated in the study (LDN) (Bishop et al., 2010, 2011; Cheour et al., 2001; Rinker et al., (range: 6 months and 0 days to 7 months and 31 days). Infants were 2007; Zachau et al., 2005), which is sometimes also referred to as a recruited using birth records and commercially available mailing lists. “late nMMR” (Conboy and Kuhl, 2011; Friedrich et al., 2009; Shafer All participating infants were born within three weeks of their due date et al., 2011; Garcia-Sierra et al., 2016). The LDN is commonly observed and had not experienced serious developmental delays or illness. between 250 and 450 ms, following the initial mismatch response. Al- Infants taking long-term medication or who had two left-handed par- though the amplitude of the LDN is largest in infants and children, in ents were excluded from study participation. Data from two infants adults it has been observed in response to changes in complex auditory were excluded from further analyses due to excessive movement stimuli (Cheour et al., 2001; Zachau et al., 2005). Less is understood (n = 1) or problems with EEG signal acquisition (n = 1), which pre- about the LDN than about infant mismatch responses. It has been cluded the recording of a minimum number of artifact-free trials for suggested that this late discriminative component reflects higher-order each deviant and control stimulus (40 trials). The final sample used in processing of novelty but without explicit, conscious processing of sti- the statistical analyses comprised 31 infants (mean age = 30 weeks, mulus change (Čeponienė et al., 2004; Friedirch et al., 2009). Other 6 days, SD = 2.72 weeks; 16 male; 16 African-American, 7 Caucasian, 2 studies have interpreted the LDN in infancy as the precursor of an adult- Hispanic, 6 other/multi-race). like MMN (Garcia-Sierra et al., 2016; Shafer et al., 2011). Inspired by the successful application of the auditory MMN in the 2.2. Stimuli study of speech and language development in infancy, combined with the lack of developmental research on the MMN in other sensory Tactile stimuli were delivered using an inflatable membrane modalities, the goal of the current study was to explore somatosensory mounted in a plastic casing (10 mm external diameter; MEG mismatch responses in infants aged 6 to 7 months.
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