Variation and Variability: Key Words in Human Motor Development

This article reviews developmental processes in the human brain and basic principles underlying typical and atypical motor development. The Neuronal Group Selection Theory is used as theoretical frame of reference. Evidence is accumulating that abundance in cerebral connectivity is the neural basis of human behavioral variability (ie, the ability to select, from a large repertoire of behavioral solutions, the one most appropriate for a specific situation). Indeed, typical human motor development is characterized by variation and the development of adaptive variability. Atypical motor development is characterized by a limited variation (a limited repertoire of motor strategies) and a limited ability to vary motor behavior according to the specifics of the situation (ie, limited variability). Limitations in variation are related to structural anomalies in which disturbances of cortical connectivity may play a prominent role, whereas limitations in variability are present in virtually all children with atypical motor development. The possible applications of variation and variability in diagnostics in children with or at risk for a developmental motor disorder are discussed.

[1]  Linda B. Smith,et al.  Development as a dynamic system , 1992, Trends in Cognitive Sciences.

[2]  Mijna Hadders-Algra,et al.  The assessment of minor neurological dysfunction in infancy using the Touwen Infant Neurological Examination: strengths and limitations , 2010, Developmental medicine and child neurology.

[3]  H. Supèr,et al.  The functions of the preplate in development and evolution of the neocortex and hippocampus , 1998, Brain Research Reviews.

[4]  S. Campbell,et al.  Construct validity of the test of infant motor performance. , 1995, Physical therapy.

[5]  K. Adolph,et al.  Learning in the development of infant locomotion. , 1997, Monographs of the Society for Research in Child Development.

[6]  B C Touwen,et al.  How normal is variable, or how variable is normal? , 1993, Early human development.

[7]  A N Bhat,et al.  Toy-oriented changes during early arm movements: hand kinematics. , 2006, Infant behavior & development.

[8]  B. Dan,et al.  A report: the definition and classification of cerebral palsy April 2006 , 2007, Developmental medicine and child neurology. Supplement.

[9]  R. Seitz,et al.  Congenitally altered motor experience alters somatotopic organization of human primary motor cortex , 2009, Proceedings of the National Academy of Sciences.

[10]  G. Edelman.  Neural Darwinism: The Theory Of Neuronal Group Selection , 1989 .

[11]  Jean Massion,et al.  Postural Control Systems in Developmental Perspective , 1998, Neuroscience & Biobehavioral Reviews.

[12]  C. Amiel‐Tison,et al.  Neurological Development from Birth to Six Years: Guide for Examination and Evaluation , 2001 .

[13]  J. Duysens,et al.  Muscle force generation and force control of finger movements in children with spastic hemiplegia during isometric tasks. , 2005, Developmental medicine and child neurology.

[14]  K. Himmelmann,et al.  Gross and fine motor function and accompanying impairments in cerebral palsy , 2006 .

[15]  K. Newell,et al.  Practice of a precision isometric grip‐force task by children with spastic cerebral palsy , 1998, Developmental medicine and child neurology.

[16]  V. Hömberg,et al.  Maturation of fastest afferent and efferent central and peripheral pathways: No evidence for a constancy of central conduction delays , 1994, Neuroscience Letters.

[17]  P. Gaspar,et al.  Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. , 1995, Science.

[18]  M. Hadders‐Algra,et al.  Postural adjustments and reaching in 4- and 6-month-old infants: an EMG and kinematical study , 2007, Experimental Brain Research.

[19]  Roslyn N Boyd,et al.  Quality of General Movements Is Related to White Matter Pathology in Very Preterm Infants , 2008, Pediatrics.

[20]  Katsumi Nakajima,et al.  Direct and indirect pathways for corticospinal control of upper limb motoneurons in the primate. , 2004, Progress in brain research.

[21]  Mijna Hadders-Algra,et al.  Ontogeny of the human central nervous system: what is happening when? , 2006, Early human development.

[22]  G Cioni,et al.  Differences and variations in the patterns of early independent walking. , 1993, Early human development.

[23]  M. Hadders‐Algra,et al.  Kinematic Characteristics of Postural Control during Reaching in Preterm Children with Cerebral Palsy , 2005, Pediatric Research.

[24]  H. Prechtl,et al.  General movement assessment as a method of developmental neurology: new paradigms and their consequences. The 1999 Ronnie MacKeith lecture. , 2001 .

[25]  E. Thelen.  Motor development: A new synthesis. , 1995 .

[26]  Mijna Hadders-Algra,et al.  The Neuronal Group Selection Theory : a framework to explain variation in normal motor development , 2000 .

[27]  Maarten Mennes,et al.  Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review , 2005, Neuroscience & Biobehavioral Reviews.

[28]  H. Prechtl,et al.  Continuity of neural functions from prenatal to postnatal life , 1984 .

[29]  Mijna Hadders-Algra,et al.  Evaluation of Neuromotor Function in Infancy–A Systematic Review of Available Methods , 2008, Journal of developmental and behavioral pediatrics : JDBP.

[30]  M. Hadders‐Algra,et al.  The Infant Motor Profile: a standardized and qualitative method to assess motor behaviour in infancy , 2008, Developmental medicine and child neurology.

[31]  Hans Forssberg,et al.  Postural adjustments due to external perturbations during sitting in 1-month-old infants: evidence for the innate origin of direction specificity , 2004, Experimental Brain Research.

[32]  Kristin M. Heineman,et al.  Development of adaptive motor behaviour in typically developing infants , 2010, Acta paediatrica.

[33]  J. Stephenson,et al.  Neurological Development in Infancy , 1977 .

[34]  M. Hadders‐Algra,et al.  Predictive value of definitely abnormal general movements in the general population , 2009, Developmental medicine and child neurology.

[35]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[36]  J. Volpe.  Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances , 2009, The Lancet Neurology.

[37]  G. Holstege.  Descending motor pathways and the spinal motor system: limbic and non-limbic components. , 1991, Progress in brain research.

[38]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[39]  U. Thyen,et al.  Predictive Value of Neurodevelopmental Assessment versus Evaluation of General Movements for Motor Outcome in Preterm Infants with Birth Weights <1500 g , 2007, Neuropediatrics.

[40]  S. Harris.  Congenital hypotonia: clinical and developmental assessment , 2008, Developmental medicine and child neurology.

[41]  M. Molinari,et al.  Neuronal plasticity of interrelated cerebellar and cortical networks , 2002, Neuroscience.

[42]  H. Prechtl,et al.  General movement assessment as a method of developmental neurology: new paradigms and their consequences , 2001, Developmental medicine and child neurology.

[43]  P G Nelson,et al.  Synapse elimination from the mouse neuromuscular junction in vitro: a non-Hebbian activity-dependent process. , 1993, Journal of neurobiology.

[44]  H Forssberg,et al.  Periventricular leucomalacia and preterm birth have different detrimental effects on postural adjustments. , 1999, Brain : a journal of neurology.

[45]  Giovanni Cioni,et al.  Prechtl's Method on the Qualitative Assessment of General Movements in Preterm, Term and Young Infants , 2004 .

[46]  Pasko Rakic,et al.  Modes and Mishaps of Neuronal Migration in the Mammalian Brain , 2008, The Journal of Neuroscience.

[47]  Neil Gordon,et al.  Neurophysiology and Neuropsychology of Motor Development. , 1998 .

[48]  P. Zelazo.  The development of walking: new findings and old assumptions. , 1983, Journal of motor behavior.

[49]  K. Himmelmann,et al.  Gross and fine motor function and accompanying impairments in cerebral palsy. , 2006, Developmental medicine and child neurology.

[50]  Ambikaipakan Senthilselvan,et al.  Trajectories of serial motor scores of typically developing children: Implications for clinical decision making. , 2009, Infant behavior & development.

[51]  G. Cioni,et al.  Visual disorders in children with brain lesions: 2. Visual impairment associated with cerebral palsy. , 2001, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[52]  M. Hadders‐Algra,et al.  Postural Control: A Key Issue in Developmental Disorders , 2008 .

[53]  P. Rakić,et al.  Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain , 1990, The Journal of comparative neurology.

[54]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[55]  Jaynie F. Yang,et al.  Spinal and Brain Control of Human Walking: Implications for Retraining of Walking , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[56]  Mijna Hadders-Algra,et al.  General movements: A window for early identification of children at high risk for developmental disorders. , 2004, The Journal of pediatrics.

[57]  H Forssberg,et al.  IMPAIRED ANTICIPATORY CONTROL OF ISOMETRIC FORCES DURING GRASPING BY CHILDREN WITH CEREBRAL PALSY , 1992, Developmental medicine and child neurology.

[58]  Klaas Postema,et al.  General movements in early infancy predict neuromotor development at 9 to 12 years of age , 2005, Developmental medicine and child neurology.

[59]  Bennett I. Bertenthal,et al.  An Epigenetic Perspective on the Development of Self-Produced Locomotion and Its Consequences , 1994 .

[60]  M. Hadders‐Algra,et al.  Development of postural control in typically developing children and children with cerebral palsy: Possibilities for intervention? , 2007, Neuroscience & Biobehavioral Reviews.

[61]  M. Hadders‐Algra,et al.  Fetal Onset of General Movements , 2008, Pediatric Research.

[62]  Changeux Jp,et al.  Variation and selection in neural function. , 1997 .

[63]  Carole Hurran,et al.  Motor Assessment of the Developing Infant , 1995 .

[64]  The Neuromuscular Maturation of the Human Infant , 1963 .

[65]  H. Forssberg,et al.  Postural adjustments during sitting at preschool age: presence of a transient toddling phase , 1998, Developmental medicine and child neurology.

[66]  H. Forssberg,et al.  Postural Control in Sitting Children with Cerebral Palsy , 1998, Neuroscience & Biobehavioral Reviews.

[67]  Bert C. L. Touwen,et al.  Neurological development in infancy , 1976 .

[68]  R. Bolt.  Developmental Diagnosis—Normal and Abnormal Child Development , 1942 .

[69]  L. Krubitzer,et al.  Nature versus nurture revisited: an old idea with a new twist , 2003, Progress in Neurobiology.

[70]  M. Hadders-Algra,et al.  Does early intervention in infants at high risk for a developmental motor disorder improve motor and cognitive development? , 2007, Neuroscience & Biobehavioral Reviews.

[71]  Ivica Kostović,et al.  Transient patterns of cortical lamination during prenatal life: Do they have implications for treatment? , 2007, Neuroscience & Biobehavioral Reviews.

[72]  P. Rakic.  Evolution of the neocortex: Perspective from developmental biology , 2010 .

[73]  M. Hadders‐Algra,et al.  The neuronal group selection theory: promising principles for understanding and treating developmental motor disorders , 2000, Developmental medicine and child neurology.

[74]  E. Flikweert,et al.  Development of postural adjustments during reaching in preterm infants. , 2000, Pediatric physical therapy : the official publication of the Section on Pediatrics of the American Physical Therapy Association.

[75]  A. Graybiel.  The basal ganglia: learning new tricks and loving it , 2005, Current Opinion in Neurobiology.

[76]  Mijna Hadders-Algra,et al.  Putative neural substrate of normal and abnormal general movements , 2007, Neuroscience & Biobehavioral Reviews.

[77]  H. Forssberg.  Ontogeny of human locomotor control I. Infant stepping, supported locomotion and transition to independent locomotion , 2004, Experimental Brain Research.

[78]  K. Bjornson,et al.  Lower extremity sensory function in children with cerebral palsy , 2005, Pediatric rehabilitation.

[79]  H. Forssberg,et al.  Postural adjustments in sitting humans following external perturbations: muscle activity and kinematics , 2004, Experimental Brain Research.

[80]  G. Cioni,et al.  Visual disorders in children with brain lesions: 1. Maturation of visual function in infants with neonatal brain lesions: correlation with neuroimaging. , 2001, European journal of paediatric neurology : EJPN : official journal of the European Paediatric Neurology Society.

[81]  M. Yekutiel,et al.  SENSORY DEFICIT IN THE HANDS OF CHILDREN WITH CEREBRAL PALSY: A NEW LOOK AT ASSESSMENT AND PREVALENCE , 1994, Developmental medicine and child neurology.

[82]  Hans Forssberg,et al.  Development of postural adjustments in sitting position during the first half year of life. , 2005, Developmental medicine and child neurology.

[83]  M. Latash,et al.  What are “normal movements” in atypical populations? , 1996, Behavioral and Brain Sciences.

[84]  J. Campos,et al.  Effect of self-produced locomotion on infant postural compensation to optic flow. , 1996 .

[85]  A. Diamond.  The Interplay of Biology and the Environment Broadly Defined It Is Not Simply That Genes and the Environment Interact Experience Affects Gene Expression , 2022 .

[86]  H. Frahm,et al.  Comparison of brain structure volumes in Insectivora and Primates. I. Neocortex. , 1982, Journal fur Hirnforschung.

[87]  Woong Sun,et al.  Adaptive roles of programmed cell death during nervous system development. , 2006, Annual review of neuroscience.

[88]  F. Polleux.  Genetic Mechanisms Specifying Cortical Connectivity Let’s MakeSome Projections Together , 2005, Neuron.

[89]  P. Gaspar,et al.  Plasma Membrane Transporters of Serotonin, Dopamine, and Norepinephrine Mediate Serotonin Accumulation in Atypical Locations in the Developing Brain of Monoamine Oxidase A Knock-Outs , 1998, The Journal of Neuroscience.

[90]  A Piepsz,et al.  Functional imaging of brain maturation in humans using iodine-123 iodoamphetamine and SPECT. , 1989, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[91]  T. Sejnowski,et al.  A universal scaling law between gray matter and white matter of cerebral cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[92]  S. Harris.  Postural Control: A Key Issue in Developmental Disorders , 2010 .

[93]  R. Palisano,et al.  Development and reliability of a system to classify gross motor function in children with cerebral palsy , 1997, Developmental medicine and child neurology.

[94]  J. Changeux,et al.  Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks , 1976, Nature.

[95]  J I P de Vries,et al.  Normal fetal motility: an overview , 2006, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[96]  J. Kaas,et al.  The evolution of the neocortex in mammals: how is phenotypic diversity generated? , 2005, Current Opinion in Neurobiology.

[97]  W. Greenough,et al.  Experience and brain development. , 1987, Child development.

[98]  B. Kolb,et al.  Age, Experience and the Changing Brain , 1998, Neuroscience & Biobehavioral Reviews.

[99]  L. de Groot.  Posture and motility in preterm infants. , 2000, Developmental medicine and child neurology.

[100]  W Singer,et al.  Involvement of Serotonin in Developmental Plasticity of Kitten Visual Cortex , 1995, The European journal of neuroscience.

[101]  H. Forssberg,et al.  Ontogeny of postural adjustments during sitting in infancy: variation, selection and modulation. , 1996, The Journal of physiology.

[102]  John H. Martin,et al.  Activity- and use-dependent plasticity of the developing corticospinal system , 2007, Neuroscience & Biobehavioral Reviews.

[103]  M. Hadders‐Algra,et al.  Quality of general movements and psychiatric morbidity at 9 to 12 years. , 2009, Early human development.

[104]  Tyrone D. Cannon,et al.  Infant motor development is associated with adult cognitive categorisation in a longitudinal birth cohort study. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[105]  Bryan Kolb,et al.  Brain plasticity and recovery from early cortical injury. , 2007, Developmental psychobiology.

[106]  L. Lossi,et al.  In vivo cellular and molecular mechanisms of neuronal apoptosis in the mammalian CNS , 2003, Progress in Neurobiology.

[107]  M. Hadders‐Algra.  Two distinct forms of minor neurological dysfunction: perspectives emerging from a review of data of the Groningen Perinatal Project , 2002, Developmental medicine and child neurology.

[108]  L. B. Ames,et al.  The Neuromuscular Maturation of the Human Infant , 1943, The Yale Journal of Biology and Medicine.

[109]  Lily Yeh Jan,et al.  The Control of Dendrite Development , 2003, Neuron.

[110]  Mijna Hadders-Algra,et al.  Reduced variability in motor behaviour: an indicator of impaired cerebral connectivity? , 2008, Early human development.

[111]  A. Gordon,et al.  Fingertip Force Planning During Grasp Is Disrupted by Impaired Sensorimotor Integration in Children With Hemiplegic Cerebral Palsy , 2006, Pediatric Research.

[112]  Colin Blakemore,et al.  Development of the human cerebral cortex: Boulder Committee revisited , 2008, Nature Reviews Neuroscience.

[113]  M. Weinstock.  Alterations induced by gestational stress in brain morphology and behaviour of the offspring , 2001, Progress in Neurobiology.

[114]  C. Hofsten.  Eye–hand coordination in the newborn. , 1982 .

[115]  J P Changeux,et al.  Variation and selection in neural function. , 1997, Trends in neurosciences.

[116]  T. Ingram.  The Neurology of Cerebral Palsy , 1966, Archives of disease in childhood.

[117]  H Forssberg,et al.  Training affects the development of postural adjustments in sitting infants. , 1996, The Journal of physiology.

[118]  A. Gordon,et al.  Efficacy of a hand–arm bimanual intensive therapy (HABIT) in children with hemiplegic cerebral palsy: a randomized control trial , 2007, Developmental medicine and child neurology.

[119]  Mijna Hadders-Algra,et al.  Construct validity of the Infant Motor Profile: relation with prenatal, perinatal, and neonatal risk factors , 2010, Developmental medicine and child neurology.

[120]  K. Eishima,et al.  The analysis of sucking behaviour in newborn infants. , 1991, Early human development.

[121]  G. Edelman.  Neural Darwinism: Selection and reentrant signaling in higher brain function , 1993, Neuron.

[122]  Hugh Jolly,et al.  Clinics in Developmental Medicine , 1965 .

[123]  Milos Judas,et al.  Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants , 2006, Developmental medicine and child neurology.

[124]  C. Hofsten,et al.  Development of visually guided hand orientation in reaching. , 1984, Journal of experimental child psychology.

[125]  Beth A. Smith,et al.  Lyapunov exponent and surrogation analysis of patterns of variability: profiles in new walkers with and without down syndrome. , 2010, Motor control.