https://eutils.ncbi.nlm.nih.gov/entrez/eutils/efetch.fcgi?db=pubmed&id=38790453&retmode=xml&tool=Litmetric&email=readroberts32@gmail.com&api_key=61f08fa0b96a73de8c900d749fcb997acc09 3879045320240527
2076-34251452024May08Brain sciencesBrain SciGaze Orienting in the Social World: An Exploration of the Role Played by Caregiving Vocal and Tactile Behaviors in Infants with Visual Impairment and in Sighted Controls.47410.3390/brainsci14050474Infant attention is a cognitive function that underlines sensory-motor integration processes at the interface between the baby and the surrounding physical and socio-relational environment, mainly with the caregivers. The investigation of the role of non-visual inputs (i.e., vocal and tactile) provided by the caregivers in shaping infants' attention in the context of visual impairment is relevant from both a theoretical and clinical point of view. This study investigated the social attention (i.e., gaze orientation) skills in a group of visually impaired (VI) and age-matched sighted controls (SCs) between 9 and 12 months of age. Moreover, the role of VI severity and maternal vocalizations and touch in shaping the social attention were investigated. Overall, 45 infants and their mothers participated in a video-recorded 4 min interaction procedure, including a play and a still-face episode. The infants' gaze orientation (i.e., mother-directed, object-directed, or unfocused) and the types of maternal vocalizations and touch (i.e., socio-cognitive, affective) were micro-analytically coded. Maternal vocalizations and touch were found to influence gaze orientation differently in VI infants compared SCs. Moreover, the group comparisons during the play episode showed that controls were predominantly oriented to the mothers, while VI infants were less socially oriented. Visual impairment severity did not emerge as linked with social attention. These findings contribute to our understanding of socio-cognitive developmental trajectories in VI infants and highlight the need for tailored interventions to promote optimal outcomes for VI populations.GrumiSerenaS0000-0003-4353-3803Developmental Psychobiology Lab, IRCCS Mondino Foundation, 27100 Pavia, Italy.CapelliElenaEDepartment of Brain and Behavioral Sciences, University of Pavia, 27100 Pavia, Italy.MorelliFedericaF0000-0003-1239-9904Developmental Neuro-Ophthalmology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy.VercellinoLuisaL0000-0003-3599-874XDevelopmental Psychobiology Lab, IRCCS Mondino Foundation, 27100 Pavia, Italy.MascherpaEleonoraEDevelopmental Neuro-Ophthalmology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy.GhibertiChiaraCDepartment of Brain and Behavioral Sciences, University of Pavia, 27100 Pavia, Italy.Developmental Neuro-Ophthalmology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy.CarraroLauraL0009-0001-6221-4982Department of Brain and Behavioral Sciences, University of Pavia, 27100 Pavia, Italy.Developmental Neuro-Ophthalmology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy.SignoriniSabrinaSDevelopmental Neuro-Ophthalmology Unit, IRCCS Mondino Foundation, 27100 Pavia, Italy.ProvenziLivioL0000-0001-7424-8744Developmental Psychobiology Lab, IRCCS Mondino Foundation, 27100 Pavia, Italy.Department of Brain and Behavioral Sciences, University of Pavia, 27100 Pavia, Italy.engRicerca Corrente 2022-2024Ministero della SaluteJournal Article20240508
SwitzerlandBrain Sci1015986462076-3425attentioninfantsparentsensory processingstill facestressvisual impairmentThe authors declare no conflicts of interest.
2024432024522024532024525105420245251053202452513202458epublish38790453PMC1112018910.3390/brainsci14050474brainsci14050474Dionne-Dostie E., Paquette N., Lassonde M., Gallagher A. Multisensory integration and child neurodevelopment. Brain Sci. 2015;5:32–57. doi: 10.3390/BRAINSCI5010032.10.3390/BRAINSCI5010032PMC439079025679116Bruce M., Panneton R., Taylor C. Multisensory integration and maternal sensitivity are related to each other and predictive of expressive vocabulary in 24-month-olds. J. Exp. Child Psychol. 2022;214:105304. doi: 10.1016/J.JECP.2021.105304.10.1016/J.JECP.2021.105304PMC860872434624708Johnson M.H., Senju A., Tomalski P. The two-process theory of face processing: Modifications based on two decades of data from infants and adults. Neurosci. Biobehav. Rev. 2015;50:169–179. doi: 10.1016/J.NEUBIOREV.2014.10.009.10.1016/J.NEUBIOREV.2014.10.00925454353Shultz S., Klin A., Jones W. Neonatal Transitions in Social Behavior and Their Implications for Autism. Trends Cogn. Sci. 2018;22:452–469. doi: 10.1016/J.TICS.2018.02.012.10.1016/J.TICS.2018.02.012PMC655474029609895Bastianello T., Keren-Portnoy T., Majorano M., Vihman M. Infant looking preferences towards dynamic faces: A systematic review. Infant Behav. Dev. 2022;67:101709. doi: 10.1016/J.INFBEH.2022.101709.10.1016/J.INFBEH.2022.10170935338995Libertus K., Landa R.J., Haworth J.L. Development of Attention to Faces during the First 3 Years: Influences of Stimulus Type. Front. Psychol. 2017;8:293890. doi: 10.3389/FPSYG.2017.01976.10.3389/FPSYG.2017.01976PMC569827129204130Grossmann T. The development of emotion perception in face and voice during infancy. Restor. Neurol. Neurosci. 2010;28:219–236. doi: 10.3233/RNN-2010-0499.10.3233/RNN-2010-049920404410Schröer L., Çetin D., Vacaru S.V., Addabbo M., van Schaik J.E., Hunnius S. Infants’ sensitivity to emotional expressions in actions: The contributions of parental expressivity and motor experience. Infant Behav. Dev. 2022;68:101751. doi: 10.1016/J.INFBEH.2022.101751.10.1016/J.INFBEH.2022.10175135914367Gogate L., Maganti M. The Dynamics of Infant Attention: Implications for Crossmodal Perception and Word-Mapping Research. Child Dev. 2016;87:345–364. doi: 10.1111/CDEV.12509.10.1111/CDEV.1250927015082White-Traut R., Gillette P., Simpson P., Zhang L., Nazarloo H.P., Carter C.S. Early Postpartum Maternal and Newborn Responses to Auditory, Tactile, Visual, Vestibular, and Olfactory Stimuli. J. Obstet. Gynecol. Neonatal Nurs. JOGNN. 2022;51:402–417. doi: 10.1016/J.JOGN.2022.03.003.10.1016/J.JOGN.2022.03.00335469779Abrams D.A., Chen T., Odriozola P., Cheng K.M., Baker A.E., Padmanabhan A., Ryali S., Kochalka J., Feinstein C., Menon V. Neural circuits underlying mother’s voice perception predict social communication abilities in children. Proc. Natl. Acad. Sci. USA. 2016;113:6295–6300. doi: 10.1073/PNAS.1602948113.10.1073/PNAS.1602948113PMC489671927185915Williamson S., McGrath J.M. What Are the Effects of the Maternal Voice on Preterm Infants in the NICU? Adv. Neonatal Care. 2019;19:294–310. doi: 10.1097/ANC.0000000000000578.10.1097/ANC.000000000000057831335378Uchida M.O., Arimitsu T., Yatabe K., Ikeda K., Takahashi T., Minagawa Y. Effect of mother’s voice on neonatal respiratory activity and EEG delta amplitude. Dev. Psychobiol. 2018;60:140–149. doi: 10.1002/DEV.21596.10.1002/DEV.21596PMC583687729205320Porges S.W., Arnold W.R., Forbes E.J. Heart rate variability: An index of attentional responsivity in human newborns. Dev. Psychol. 1973;8:85–92. doi: 10.1037/h0033793.10.1037/h0033793Ferrari G.A., Nicolini Y., Demuru E., Tosato C., Hussain M., Scesa E., Romei L., Boerci M., Iappini E., Prati G.D.R., et al. Ultrasonographic investigation of human fetus responses to maternal communicative and non-communicative stimuli. Front. Psychol. 2016;7:137792. doi: 10.3389/FPSYG.2016.00354.10.3389/FPSYG.2016.00354PMC479288327014160Della Longa L., Gliga T., Farroni T. Tune to touch: Affective touch enhances learning of face identity in 4-month-old infants. Dev. Cogn. Neurosci. 2019;35:42–46. doi: 10.1016/j.dcn.2017.11.002.10.1016/j.dcn.2017.11.002PMC634757929153656Montirosso R., McGlone F. The body comes first. Embodied reparation and the co-creation of infant bodily-self. Neurosci. Biobehav. Rev. 2020;113:77–87. doi: 10.1016/J.NEUBIOREV.2020.03.003.10.1016/J.NEUBIOREV.2020.03.00332145222Croy I., Sehlstedt I., Wasling H.B., Ackerley R., Olausson H. Gentle touch perception: From early childhood to adolescence. Dev. Cogn. Neurosci. 2019;35:81–86. doi: 10.1016/J.DCN.2017.07.009.10.1016/J.DCN.2017.07.009PMC696895928927641Tuulari J.J., Scheinin N.M., Lehtola S., Merisaari H., Saunavaara J., Parkkola R., Sehlstedt I., Karlsson L., Karlsson H., Björnsdotter M. Neural correlates of gentle skin stroking in early infancy. Dev. Cogn. Neurosci. 2019;35:36–41. doi: 10.1016/J.DCN.2017.10.004.10.1016/J.DCN.2017.10.004PMC696895829241822Capelli E., Grumi S., Fullone E., Rinaldi E., Provenzi L. An Update on Social Touch: How Does Humans’ Social Nature Emerge at the Periphery of the Body? Rorschachiana. 2022;43:168–185. doi: 10.1027/1192-5604/a000153.10.1027/1192-5604/a000153Manzotti A., Cerritelli F., Esteves J.E., Lista G., Lombardi E., La Rocca S., Gallace A., McGlone F.P., Walker S.C. Dynamic touch reduces physiological arousal in preterm infants: A role for c-tactile afferents? Dev. Cogn. Neurosci. 2019;39:100703. doi: 10.1016/J.DCN.2019.100703.10.1016/J.DCN.2019.100703PMC696936631487608McGlone F., Wessberg J., Olausson H. Discriminative and Affective Touch: Sensing and Feeling. Neuron. 2014;82:737–755. doi: 10.1016/j.neuron.2014.05.001.10.1016/j.neuron.2014.05.00124853935Baker J.K., Messinger D.S., Lyons K.K., Grantz C.J. A pilot study of maternal sensitivity in the context of emergent autism. J. Autism Dev. Disord. 2010;40:988–999. doi: 10.1007/S10803-010-0948-4.10.1007/S10803-010-0948-4PMC290482120130975Shai D., Belsky J. Parental embodied mentalizing: Let’s be explicit about what we mean by implicit. Child Dev. Perspect. 2011;5:187–188. doi: 10.1111/j.1750-8606.2011.00195.x.10.1111/j.1750-8606.2011.00195.xProvenzi L., Fumagalli M., Bernasconi F., Sirgiovanni I., Morandi F., Borgatti R., Montirosso R. Very Preterm and Full-Term Infants’ Response to Socio-Emotional Stress: The Role of Postnatal Maternal Bonding. Infancy. 2017;22:695–712. doi: 10.1111/infa.12175.10.1111/infa.1217533158334Tröster H., Brambring M. Early social-emotional development in blind infants. Child. Care. Health Dev. 1992;18:207–227. doi: 10.1111/j.1365-2214.1992.tb00355.x.10.1111/j.1365-2214.1992.tb00355.x1386004Adamson L.B., Bakeman R., Suma K., Robins D.L. Sharing sounds: The development of auditory joint engagement during early parent-child interaction. Dev. Psychol. 2019;55:2491–2504. doi: 10.1037/DEV0000822.10.1037/DEV0000822PMC686163431524417Grumi S., Cappagli G., Aprile G., Mascherpa E., Gori M., Provenzi L., Signorini S. Togetherness, beyond the eyes: A systematic review on the interaction between visually impaired children and their parents. Infant Behav. Dev. 2021;64:101590. doi: 10.1016/J.INFBEH.2021.101590.10.1016/J.INFBEH.2021.10159034062369Campbell J., Johnston C. Emotional availability in parent-child dyads where children are blind. Parenting. 2009;9:216–227. doi: 10.1080/15295190902844456.10.1080/15295190902844456Baird S.M., Mayfield P., Baker P. Mothers’ interpretations of the behavior of their infants with visual and other impairments during interactions. J. Vis. Impair. Blind. 1997;91:467–483. doi: 10.1177/0145482x9709100507.10.1177/0145482x9709100507Nagayoshi M., Hirose T., Toju K., Suzuki S., Okamitsu M., Teramoto T., Omori T., Kawamura A., Takeo N. Related visual impairment to mother-infant interaction and development in infants with bilateral retinoblastoma. Eur. J. Oncol. Nurs. 2017;28:28–34. doi: 10.1016/j.ejon.2017.02.002.10.1016/j.ejon.2017.02.00228478852Rogers S.J., Puchalski C.B. Social characteristics of visually impaired infants’ play. Topics Early Child. Spec. Educ. 1984;3:52–56. doi: 10.1177/027112148400300409.10.1177/027112148400300409Rowland C. Preverbal communication of blind infants and their mothers. J. Vis. Impair. Blind. 1984;78:297–302. doi: 10.1177/0145482x8407800701.10.1177/0145482x8407800701Urqueta Alfaro A., Vacaru S., Wittich W., Sterkenburg P.S. Identifying when children with visual impairment share attention: A novel protocol and the impact of visual acuity. Infant Behav. Dev. 2021;64:101585. doi: 10.1016/J.INFBEH.2021.101585.10.1016/J.INFBEH.2021.10158534058632Bonomi A.E., Altenburger L.E., Walton N.L. “Double crap!” Abuse and harmed identity in Fifty Shades of Grey. J. Women’s Health. 2013;22:733–744. doi: 10.1089/jwh.2013.4344.10.1089/jwh.2013.434423931257Andersen E.S., Dunlea A., Kekelis L. The impact of input: Language acquisition in the visually impaired. First Lang. 1993;13:23–49. doi: 10.1177/014272379301303703.10.1177/014272379301303703Moore V., McConachie H. Communication between blind and severely visually impaired children and their parents. Br. J. Dev. Psychol. 1994;12:491–502. doi: 10.1111/j.2044-835x.1994.tb00650.x.10.1111/j.2044-835x.1994.tb00650.xSola-Carmona J.J., López-Liria R., Padilla-Góngora D., Daza M.T., Sánchez-Alcoba M.A. Anxiety, psychological well-being and self-esteem in Spanish families with blind children. A change in psychological adjustment? Res. Dev. Disabil. 2013;34:1886–1890. doi: 10.1016/j.ridd.2013.03.002.10.1016/j.ridd.2013.03.00223578904Gui A., Perelli D., Rizzo G., Ferruzza E., Mercuriali E. Children’s total blindness as a risk factor for early parent-child relationships: Preliminary findings from an Italian sample. Front. Psychol. 2023;14:1175675. doi: 10.3389/FPSYG.2023.1175675.10.3389/FPSYG.2023.1175675PMC1017248237179868Goodman S.H., Simon H.F.M., Shamblaw A.L., Kim C.Y. Parenting as a Mediator of Associations between Depression in Mothers and Children’s Functioning: A Systematic Review and Meta-Analysis. Clin. Child Fam. Psychol. Rev. 2020;23:427–460. doi: 10.1007/S10567-020-00322-4.10.1007/S10567-020-00322-432734498Teller D.Y., McDonald M.A., Preston K., Sebris S.L., Dobson V. Assessment of visual acuity in infants and children: The acuity card procedure. Dev. Med. Child Neurol. 1986;28:779–789. doi: 10.1111/J.1469-8749.1986.TB03932.X.10.1111/J.1469-8749.1986.TB03932.X3817317Mesman J., van IJzendoorn M.H., Bakermans-Kranenburg M.J. The many faces of the Still-Face Paradigm: A review and meta-analysis. Dev. Rev. 2009;29:120–162. doi: 10.1016/j.dr.2009.02.001.10.1016/j.dr.2009.02.001Provenzi L., Giusti L., Montirosso R. Do infants exhibit significant cortisol reactivity to the Face-to-Face Still-Face paradigm? A narrative review and meta-analysis. Dev. Rev. 2016;42:34–55. doi: 10.1016/j.dr.2016.07.001.10.1016/j.dr.2016.07.001Erickson S.J., Vaccaro S., Kubinec N., Moss N., Avila-Rieger R., Lowe J.R., Tofighi D. Preliminary longitudinal evidence for stability of maternal behavior and infant stress regulation among infants born preterm at 4 and 9 months during the Still Face paradigm. Infant Behav. Dev. 2022;68:101745. doi: 10.1016/J.INFBEH.2022.101745.10.1016/J.INFBEH.2022.10174535760033Beck A.T., Steer R.A., Carbin M.G. Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation. Clin. Psychol. Rev. 1988;8:77–100. doi: 10.1016/0272-7358(88)90050-5.10.1016/0272-7358(88)90050-5Spielberg C.D. State-Trait Anxiety Inventory: Bibliography. Consulting Psychologists Press; Palo Alto, CA, USA: 1989.Abidin R.R. Parenting Stress Index: Manual, administration booklet, and research update; Proceedings of the “Research Update” Presented at the Annual Meeting of the American Psychological Association 91st; Anaheim, CA, USA. 26–30 August 1983; Charlottesville, VA, USA: Pediatric Psychology Press, 2915 Idlewood Drive; 1983. p. 86.Sica C., Ghisi M. The Italian versions of the Beck Anxiety Inventory and the Beck Depression Inventory-II: Psychometric properties and discriminant power. In: Lange M.A., editor. Leading-Edge Psychological Tests and Testing Research. Nova Science Publishers; Hauppauge, NY, USA: 2007. pp. 27–50.Pedrabissi L., Santiello M. STAI State-Trait Anxiety Inventory Forma Y: Manuale. Organizzazioni Speciali; Firenze, Italy: 1996.Tadić V., Pring L., Dale N. Story discourse and use of mental state language between mothers and school-aged children with and without visual impairment. Int. J. Lang. Commun. Disord. 2013;48:679–688. doi: 10.1111/1460-6984.12040.10.1111/1460-6984.12040PMC422906424165364Dote-Kwan J. Impact of mothers’ interactions on the development of their young visually impaired children. J. Vis. Impair. Blind. 1995;89:46–58. doi: 10.1177/0145482X9508900109.10.1177/0145482X9508900109Yu C., Smith L.B. Joint attention without gaze following: Human infants and their parents coordinate visual attention to objects through eye-hand coordination. PLoS ONE. 2013;8:e79659. doi: 10.1371/JOURNAL.PONE.0079659.10.1371/JOURNAL.PONE.0079659PMC382743624236151Bigelow A.E. The development of joint attention in blind infants. Dev. Psychopathol. 2003;15:259–275. doi: 10.1017/S0954579403000142.10.1017/S095457940300014212931827Frischen A., Bayliss A.P., Tipper S.P. Gaze Cueing of Attention: Visual Attention, Social Cognition, and Individual Differences. Psychol. Bull. 2007;133:694–724. doi: 10.1037/0033-2909.133.4.694.10.1037/0033-2909.133.4.694PMC195044017592962Johnson S.C., Ok S.J., Luo Y. The attribution of attention: 9-month-olds’ interpretation of gaze as goal-directed action. Dev. Sci. 2007;10:530–537. doi: 10.1111/J.1467-7687.2007.00606.X.10.1111/J.1467-7687.2007.00606.X17683339Farroni T., Johnson M.H., Brockbank M., Simion F. Infants’ use of gaze direction to cue attention: The importance of perceived motion. Vis. Cogn. 2000;7:705–718. doi: 10.1080/13506280050144399.10.1080/13506280050144399Akhtar N., Gernsbacher M.A. On Privileging the Role of Gaze in Infant Social Cognition. Child Dev. Perspect. 2008;2:59–65. doi: 10.1111/J.1750-8606.2008.00044.X.10.1111/J.1750-8606.2008.00044.XPMC426654425520748