Premature birth affects visual body representation and body schema in preterm children
Introduction
The representation of one’s own and others’ body is a crucial step in developing an emergent sense of self (Morin, 2006, Porciello et al., 2018), as well as in perceiving others’ actions and emotions (de Gelder, 2009). In adults, body representation is based on both visual (Corradi-Dell’Acqua & Tessari, 2010) and sensorimotor information (Medina & Coslett, 2010). Notably, recent studies have documented that infants show early sensitivity to body visual features (Gliga and Dehaene-Lambertz, 2005, Hock et al., 2016) and rely on sensorimotor and proprioceptive inputs in forming representations of their own bodies (DiMercurio et al., 2018, Marshall and Meltzoff, 2015). On the one hand, vision is the main sense through which we can perceive the shape of others’ body, thus playing a critical role in the development of expert body processing (Striem-Amit & Amedi, 2014). On the other, research has documented that newborns integrate visual information with tactile, auditory and proprioceptive information (Filippetti et al., 2013, Filippetti et al., 2015), sustaining that diverse sensorial and sensorimotor stimulations contribute to forming a primitive sense of the body (Montirosso & McGlone, 2020). This suggests that early adverse experiences such as premature birth, which are associated with atypical exposure to visual, sensorimotor, vestibular, and proprioceptive stimulation (Peng et al., 2009), may disrupt the efficacy of processing body-related information. Thus, premature birth is appropriate in examining how alterations of early sensorial and sensorimotor stimulation, strictly connected with this condition, could impact on body representation, with likely long-term effects on body processing. Moreover, even in absence of clinical complications and documented brain damage, preterm children present negative long-term sequelae on a wide range of neuropsychological domains, such as language (van Noort-van der Spek, Franken, & Weisglas-Kuperus, 2012), executive functions (Ritter, Perrig, Steinlin, & Everts, 2014), and social perception (Williamson & Jakobson, 2014). In our study, we examined whether school-aged children born preterm show alterations at multiple levels of body processing (Berlucchi & Aglioti, 2010; Corradi-Dell’Acqua et al., 2009, Schwoebel and Coslett, 2005; Sirigu, Grafman, Bressler, & Sunderland, 1991), namely visual body perception and body schema.
In the case of visual body perception, a category-specific representation, also known as body structural description (Fontes, Moura, & Haase, 2014), allows for the detection and recognition of visual body stimuli, as well as positions and boundaries of single parts of the body. In line with literature on face stimuli perception (Tanaka & Gordon, 2012), previous studies have reported that body stimuli are more likely to be perceived through specific visual perceptual strategies that allow for the detection of first-order and second-order relations among different parts of the stimulus (configural processing; (Maurer et al., 2002, Reed et al., 2006)) and their perception as a whole (holistic processing; (Tanaka & Gordon, 2012)). These processing strategies are more efficient than detail-based processing (Minnebusch & Daum, 2009) and assist the recognition of the identity, actions, and emotions of social stimuli, such as faces and bodies (Aviezer et al., 2012, Palermo et al., 2011). The presence of these two refined perceptual processing strategies is also revealed by category-specific areas in the occipito-temporal cortex that respond selectively to the visual presentation of body stimuli (Downing and Peelen, 2011, Urgesi et al., 2007) and represent the body as a whole (Brandman & Yovel, 2016) by coding the static structure of human forms (Peelen & Downing, 2007).
Body structural description is considered to derive primarily from visual experience (Corradi-Dell’Acqua & Tessari, 2010), as repeated exposure to body stimuli results in the development of configural and holistic body processing (Bosbach et al., 2006, Slaughter et al., 2011). Although previous research has suggested that body visual representations develop slowly in comparison to the rapid specialization in the case of face stimuli (Slaughter and Brownell, 2011, Slaughter et al., 2002, Zieber et al., 2010), recent studies have demonstrated that infants are sensitive to body structure as early as in the first six months of life. In particular, they are sensitive to first-order relations detected by means of configural processing (Gliga and Dehaene-Lambertz, 2005, Heck et al., 2018, Zieber et al., 2015) and to body stimuli represented as a whole through holistic processing (Hock et al., 2016). These findings point to an early development of expertise in body perception in the first six months of life leading to both configural and holistic processing of bodies. Noteworthy, the first six months of life represent a critical period for the development of visual functions in preterm infants (Atkinson & Braddick, 2012), which are often exposed to unusual visual stimulation in the neonatal intensive care unit (Peng et al., 2009). Indeed, preterm infants were reported to be particularly vulnerable to specific alterations in the processing of visual information (Atkinson et al., 2007, Jakobson and Taylor, 2009), with long-term consequences reliable even after age 6 (Butcher et al., 2012, MacKay et al., 2005, Santos et al., 2009, Taylor et al., 2009). This evidence suggests that preterm school-aged children could present specific alterations in the development of expert visual body processing (Jakobson & Taylor, 2009). In particular, since a previous study has documented normal sensitivity to first order relationships among the parts of non-bodily stimuli in preterm infants (Santos, Duret, Mancini, Busuttil, & Deruelle, 2010), we expected a greater effect on the higher-level holistic processing which is considered to be a more refined perceptual strategy than configural processing (Tanaka & Gordon, 2012), and thus more susceptible to alterations of sensorial experiences.
Preterm birth may impact on other levels of body representation, and particularly on body schema, which refers to a dynamic internal representation of one’s own body that guides action and movement, even when simulated internally (Lallee and Dominey, 2013, Schwoebel and Coslett, 2005). Although the body structural description and the body schema are inherently linked by partially sharing common mechanisms of body perception (Peelen and Downing, 2007, Perruchoud et al., 2016), they could be dissociated (Sirigu et al., 1991) and sub-serve diverse cognitive processes. Indeed, the former is more implicated in recognizing body identity and the latter is more involved in action processing and motor imagery (Blanke et al., 2010, Urgesi et al., 2007). Accordingly, while the body structural description is mainly concerned with visual information, the body schema primarily relies on proprioceptive information and multimodal sensorimotor integration (Berlucchi & Aglioti, 2010). As a result, many studies have shown that the body schema is directly influenced by sensorimotor experiences and is altered by damage to cortical areas involved in motor control and simulation (Corti et al., 2018, Mutsaarts et al., 2007). Alongside unusual early visual stimulations, preterm infants are exposed to atypical handling routines and physical contact (Peng et al., 2009), which provide them altered experiences of the environment and their own bodies. Recent studies indicate that premature birth affects the typical early experience of self-touch (Durier et al., 2015) and the motor foundation of embodied agency (Delafield-Butt et al., 2018), which are crucial to the emergence of a basic sense of body in the post-natal period (DiMercurio et al., 2018). Furthermore, evidence of impairments in motor skills and sensorimotor functioning in preterm sample from birth to adolescence (De Kieviet et al., 2009, Di Rosa et al., 2016, Marlow et al., 2007) suggests that premature birth may impact on the later development of the body schema and that alterations of this representation should be reliable in school-aged preterm children.
In our study, we compared the performance of preterm children aged 8–14 years with that of an age-matched full-term sample with typical development. The children carried out two tasks that have been widely used to assess, respectively, visual body processing and body schema. The visual body recognition task requires the visual discrimination of bodies in a delayed same-different-matching task and provides a measure of configural and holistic processing. Configural processing is indexed by the drop in performance when bodily stimuli are presented inverted to upright, since inversion is held to disrupt configural processing (Butti et al., 2018, Minnebusch et al., 2010). The presence of holistic processing is demonstrated by the composite illusion effect; when two identical top halves of bodies or faces are displayed aligned with two different bottom halves (with respect to the vertical axis), they are perceived as being different. On the contrary, misalignment disrupts the composite illusion, facilitating the same-different judgment on the two top halves of the stimuli (Rossion, 2013; Soria Bauser, Schriewer, & Suchan, 2015; Willems, Vrancken, Germeys, & Verfaillie, 2014). However, inversion of stimuli interferes not only with configural processing, but also with higher-level holistic strategy. This is expected to lead to an interaction between alignment and orientation of body stimuli, which reflects the presence of both holistic processing and configural processing, respectively.
The visuo-spatial imagery task allowed us to evaluate body schema by measuring the ability to carry out mental rotations of whole-body and non-bodily stimuli (i.e., letters) (Butti et al., 2019, Corti et al., 2018, Crescentini et al., 2014). Indeed, the mental rotation of body stimuli requires first-person mental transformations, while the same operation for non-bodily stimuli activates object-based mental transformations. First-person and object-based mental transformations correspond to the use of motor and visual imagery, respectively, and rely on partially distinct neural substrates (Sirigu and Duhamel, 2001, Zacks et al., 2002). Notably, only first-person mental transformations critically involve one’s own body schema (Kessler & Thomson, 2010) and, thus, is directly influenced by motor and embodied experiences (Kaltner et al., 2014, Steggemann et al., 2011). It is noteworthy that the emergence of first-person and object-based mental transformations follows different developmental trajectories (Crescentini et al., 2014). However, both are expected to operate at 8 years of age (Crescentini et al., 2014), despite the fact that these processes are hardly dissociable until 12 years of age (Vander Heyden, Huizinga, Kan, & Jolles, 2016). Consequently, the period between 8 and 12–14 years of age could be considered appropriate to study how premature birth influences body representation at the level of body schema.
In relation to the impact of prematurity on early visual and sensorimotor experiences, we expected that preterm children might show alterations at diverse levels of body representation. In the former task, the preterm sample was expected to show an impaired use of configural and/or holistic body processing as revealed by the absence of a body inversion/composite illusion effect. In the latter task, we hypothesized that preterm group performance would be worse than full-term performance when operating both first-person and object-based mental transformations, even though a more evident deficit was expected for first-person transformations triggered by body stimuli.
Section snippets
Participants
Preterm participants were recruited among children who referred to the A. Manzoni Hospital in Lecco, Italy. Eligible participants were identified by the attending physician and reported to the researchers. Inclusion criteria were: age ≥ 8 years and < 15 years; gestational age < 37 weeks. Exclusion criteria were: major brain lesions as documented by cerebral ultrasound (intraventricular hemorrhage ≤ grade 2 according to Papile (Papile, Burstein, Burstein, & Koffler, 1978)), periventricular
Visual body recognition task
Raw data for Accuracy and RTs for the visual body recognition task are reported in Table 2.
The 2 Alignment × 2 Orientation × 2 Groups ANOVA highlighted significant effects of Alignment (F1, 46 = 7.653, p = 0.008, η2p = 0.143) and Orientation (F1,46 = 13.015, p = 0.001, η2p = 0.221), in line with the presence of both composite illusion and inversion effects across the groups. These findings were better qualified by significant three-way interaction Alignment × Orientation × Group (F1,46 = 6.155,
Discussion
In our study, we compared the performance of preterm children with that of an age-matched full-term group when they performed two task types: a perceptual task assessing configural and holistic body processing and a visuo-spatial imagery task that required participants to carry out first-person or object-based mental transformations. We found that preterm children showed similar body inversion effect but altered composite illusion effect compared to full-term controls. Hence, there was evidence
Conclusions
The findings of the present study indicated that preterm children could present alterations in body representation at the levels of body visual perceptual processing and of body schema. For the former aspect, we found that preterm children presented spared configural processing but impaired holistic processing for body stimuli. As regards body schema, preterm children showed a general difficulty in expressing a visuospatial judgement on body stimuli, which was associated with a more specific
Funding
This work was supported by Italian Ministry of Health [Ricerca Corrente “2015–2017”, to C.U.]. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
CRediT authorship contribution statement
Niccolò Butti: Formal analysis, Investigation, Data curation, Writing - original draft. Rosario Montirosso: Conceptualization, Methodology, Writing - original draft, Project administration. Lorenzo Giusti: Investigation, Data curation, Writing - review & editing. Renato Borgatti: Writing - review & editing, Supervision. Cosimo Urgesi: Conceptualization, Methodology, Software, Formal analysis, Data curation, Writing - review & editing, Supervision, Project administration, Funding acquisition.
Declaration of Competing Interest
None.
Acknowledgements
Thanks to Dr. Lionello Fabris for proof-reading the manuscript draft. The authors are also grateful to Dr. Alberto Del Prete and Dr. Roberto Bellù for their help in recruiting the preterm sample. Finally, the authors would thank all children and their parents for taking part into the study.
References (119)
- et al.
Differences between perception of human faces and body shapes: Evidence from the composite illusion
Vision Research
(2011) - et al.
Body inversion effect without body sense: Insights from deafferentation
Neuropsychologia
(2006) - et al.
Holistic face processing is mature at 4 years of age: Evidence from the composite face effect
Journal of Experimental Child Psychology
(2007) - et al.
Predictive role of early milestones-related psychomotor profiles and long-term neurodevelopmental pitfalls in preterm infants
Early Human Development
(2016) - et al.
Development of body emotion perception in infancy: From discrimination to recognition
Infant Behavior and Development
(2018) - et al.
The embodied nature of spatial perspective taking: Embodied transformation versus sensorimotor interference
Cognition
(2010) - et al.
Gradual inversion affects the processing of human body shapes
NeuroImage
(2010) Levels of consciousness and self-awareness: A comparison and integration of various neurocognitive views
Consciousness and Cognition
(2006)- et al.
Impaired motor imagery in right hemiparetic cerebral palsy
Neuropsychologia
(2007) - et al.
Impaired holistic coding of facial expression and facial identity in congenital prosopagnosia
Neuropsychologia
(2011)
Faces are represented holistically in the human occipito-temporal cortex
NeuroImage
Face and body perception in schizophrenia: A configural processing deficit?
Psychiatry Research
Visual and visuocognitive development of children born very prematurely
Handbook of Growth and Growth Monitoring in Health and Disease
Holistic person processing: Faces with bodies tell the whole story
Journal of Personality and Social Psychology
Grounded cognition
Annual Review of Psychology
Executive functions in school-age children born very prematurely
Early Human Development
The body in the brain revisited
Experimental Brain Research
Mental imagery for full and upper human bodies: Common right hemisphere activations and distinct extrastriate activations
Brain Topography
Bodies are represented as wholes rather than their sum of parts in the occipital-temporal cortex
Cerebral Cortex
Extending mind, visuospatial integration, and the evolution of the parietal lobes in the human genus
Quaternary International
Body-specific representations of spatial location
Cognition
Visuospatial perception in children born preterm with no major neurological disorders
Neuropsychology
Maternal sensitivity is associated with configural processing of infant’s cues in preterm and full-term mothers
Early Human Development
Change in cognitive abilities over time during preschool age in low risk preterm children
Early Human Development
Embodiment of abstract concepts: Good and bad in right- and left-handers
Journal of Experimental Psychology: General.
Holistic processing for faces and cars in preschool-aged children and adults: Evidence from the composite effect
Developmental Science
Distinct contributions of extrastriate body area and temporoparietal junction in perceiving one’s own and others’ body
Cognitive, Affective and Behavioral Neuroscience
Is the body in the eye of the beholder?. Visual processing of bodies in individuals with anomalous anatomical sensory and motor features
Neuropsychologia.
What is the position of an arm relative to the body? Neural correlates of body schema and body structural description
Journal of Neuroscience.
Visual perception and spatial transformation of the body in children and adolescents with brain tumor
Neuropsychologia
Mental spatial transformations of objects and bodies: Different developmental trajectories in children from 7 to 11 years of age
Developmental Psychology
Why bodies? Twelve reasons for including bodily expressions in affective neuroscience
Philosophical Transactions of the Royal Society B: Biological Sciences
Motor development in very preterm and very low-birth-weight children from birth to adolescence: A meta-analysis
JAMA - Journal of the American Medical Association
Prospective organization of neonatal arm movements: A motor foundation of embodied agency, disrupted in premature birth
Developmental Science
A naturalistic observation of spontaneous touches to the body and environment in the first 2 months of life
Frontiers in Psychology
The role of occipitotemporal body-selective regions in person perception
Cognitive Neuroscience
Unexpected behavioural consequences of preterm newborns’ clothing
Scientific Reports
Body perception in newborns
Current Biology
Neural mechanisms of body awareness in infants
Cerebral Cortex
Evaluation of body representation in children with hemiplegic cerebral palsy: Toward the development of a neuropsychological test battery
Psychology and Neuroscience
Strategy modulates spatial perspective-taking: Evidence for dissociable disembodied and embodied routes
Frontiers in Human Neuroscience
Body-centered representations for visually-guided action emerge during early infancy
Cognition
Structural encoding of body and face in human infants and adults
Journal of Cognitive Neuroscience
Face inversion disproportionately impairs the perception of vertical but not horizontal relations between features
Journal of Experimental Psychology: Human Perception and Performance.
The whole picture: Holistic body posture recognition in infancy
Psychonomic Bulletin and Review
Human cerebellar activity reflecting an acquired internal model of a new tool
Nature
Differential vulnerability of cerebral visual functions in children born very prematurely
Acta Paediatrica, International Journal of Paediatrics.
Cited by (7)
Adult outcome of preterm birth: Implications for neurodevelopmental theories of psychosis
2022, Schizophrenia ResearchCitation Excerpt :Early motor difficulties could lead to impaired self-other distinction and development of the embodied self, which are implicated in the genesis of psychotic symptoms by virtue of a failure to distinguish between internally and externally generated sensation (Poletti et al., 2019). Recent evidence of impaired body representation and deficits in sensorimotor representation of self and other generated action in preterm children (Butti et al., 2020; Montirosso et al., 2019) provides a possible mechanistic link between abnormal motor development following preterm birth and vulnerability to psychosis. This is further underlined by evidence that neuromotor abnormalities are significantly associated with obstetric complications in high risk (Marcus et al., 1993) and psychotic (Peralta and Cuesta, 2011) individuals.
A conceptual framework on body representations and their relevance for mental disorders
2023, Frontiers in PsychologyHolistic Processing of Body Stimuli: Evidence of Body Composite Illusion in Adults and Children
2022, Developmental Psychology