Memory functions of children born with asymmetric intrauterine growth restriction

OBJECTIVE Learning difficulties are frequently diagnosed in children born with intrauterine growth restriction (IUGR). Models of various animal species with IUGR were studied and demonstrated specific susceptibility and alterations of the hippocampal formation and its related neural structures. The main purpose was to study memory functions of children born with asymmetric IUGR in a large-scale cohort using a long-term prospective paradigm. METHODS One hundred and ten infants diagnosed with IUGR were followed-up from birth to 9 years of age. Their performance was compared with a group of 63 children with comparable gestational age and multiple socioeconomic factors. Memory functions (short-term, super- and long-term spans) for different stimuli types (verbal and visual) were evaluated using Visual Auditory Digit Span tasks (VADS), Rey Auditory Verbal Learning Test (Rey-AVLT), and Rey Osterrieth Complex Figure Test (ROCF). RESULTS Children with IUGR had short-term memory difficulties that hindered both serial verbal processing system and simultaneous processing of high-load visuo-spatial stimuli. The difficulties were not related to prematurity, neonatal complications or growth catch-up, but were augmented by lower maternal education. Recognition skills and benefits from reiteration, typically affected by hippocampal dysfunction, were preserved in both groups. CONCLUSIONS Memory profile of children born with IUGR is characterized primarily by a short-term memory deficit that does not necessarily comply with a typical hippocampal deficit, but rather may reflect an executive short-term memory deficit characteristic of anterior hippocampal-prefrontal network. Implications for cognitive intervention are discussed.

[1]  D. Andrewes,et al.  Degree of left hippocampal atrophy correlates with severity of neuropsychological deficits , 1997, Seizure.

[2]  J. Low,et al.  Association of intrauterine fetal growth retardation and learning deficits at age 9 to 11 years. , 1992, American journal of obstetrics and gynecology.

[3]  H. Whyte,et al.  The Importance of Head Growth Patterns in Predicting the Cognitive Abilities and Literacy Skills of Small-for-Gestational-Age Children , 2002, Developmental neuropsychology.

[4]  R. Geva,et al.  Neuropsychological Outcome of Children With Intrauterine Growth Restriction: A 9-Year Prospective Study , 2006, Pediatrics.

[5]  Prenatal diagnosis and management of intrauterine growth restriction: A long-term prospective study on outcome and maternal stress. , 2005, Infant mental health journal.

[6]  E. Hey,et al.  BORN TOO SMALL—IS OUTCOME STILL AFFECTED? , 1990, Developmental medicine and child neurology.

[7]  S. Rees,et al.  Dendritic morphology is altered in hippocampal neurons following prenatal compromise. , 2003, Journal of neurobiology.

[8]  A. Fattal-Valevski,et al.  Neurodevelopmental Outcome in Children With Intrauterine Growth Retardation: A 3-Year Follow-Up , 1999, Journal of child neurology.

[9]  F. Biasini,et al.  Visual recognition memory in IUGR and normal birth-weight infants , 1988 .

[10]  N. Cowan,et al.  The role of attention in the development of short-term memory: age differences in the verbal span of apprehension. , 1999, Child development.

[11]  L. Mrzljak,et al.  Early onset of synapse formation in the human hippocampus: A correlation with Nissl-Golgi architectonics in 15- and 16.5-week-old fetuses , 1989, Neuroscience.

[12]  S. Hinshaw,et al.  Performance of Girls With ADHD and Comparison Girls On the Rey-Osterrieth Complex Figure: Evidence for Executive Processing Deficits , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.

[13]  S. Rees,et al.  Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction , 2000, Neuroscience.

[14]  T. Kemper,et al.  Effects of prenatal protein malnutrition on hippocampal CA1 pyramidal cells in rats of four age groups , 1997, Hippocampus.

[15]  A. van Wassenaer Neurodevelopmental consequences of being born SGA. , 2005, Pediatric endocrinology reviews : PER.

[16]  P. Goldman-Rakic,et al.  Neurochemical development of the hippocampal region in the fetal rhesus monkey. I. Early appearance of peptides, calcium‐binding proteins, DARPP‐32, and monoamine innervation in the entorhinal cortex during the first half of gestation (E47 to E90) , 1993, Hippocampus.

[17]  P. Osterrieth Le test de copie d'une figure complexe , 1944 .

[18]  Simon K Warfield,et al.  Early Alteration of Structural and Functional Brain Development in Premature Infants Born with Intrauterine Growth Restriction , 2004, Pediatric Research.

[19]  P. Rautava,et al.  Academic achievement of small-for-gestational-age children at age 10 years. , 2002, Archives of pediatrics & adolescent medicine.

[20]  A. Tamir,et al.  Sonographic Biometry of the Frontal Lobe in Normal and Growth-Restricted Neonates , 2004, Pediatric Research.

[21]  S. Harel,et al.  The cephalization index: A screening device for brain maturity and vulnerability in normal and intrauterine growth retarded newborns , 1985, Brain and Development.

[22]  A. Ornoy,et al.  Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? , 2005, Reproductive toxicology.

[23]  D G Gadian,et al.  Developmental amnesia and its relationship to degree of hippocampal atrophy , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  O Josephs,et al.  Dissociable Human Perirhinal, Hippocampal, and Parahippocampal Roles during Verbal Encoding , 2002, The Journal of Neuroscience.

[25]  J. Bachevalier,et al.  Volume of focal brain lesions and hippocampal formation in relation to memory function after closed head injury in children , 2000, Journal of neurology, neurosurgery, and psychiatry.

[26]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

[27]  P. Szatmari,et al.  PSYCHIATRIC DISORDERS AT FIVE YEARS AMONG CHILDREN WITH BIRTHWEIGHTS < 1OOOg: A REGIONAL PERSPECTIVE , 1990 .

[28]  Perinatal Iron Deficiency Decreases Cytochrome c Oxidase (CytOx) Activity in Selected Regions of Neonatal Rat Brain , 2001 .

[29]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

[30]  H. Hoffman,et al.  Neurodevelopmental outcome of small-for-gestational-age infants. , 1998, European journal of clinical nutrition.

[31]  Theo G. M. van Erp,et al.  Hippocampal activations during encoding and retrieval in a verbal working memory paradigm , 2005, NeuroImage.

[32]  Michael K. Georgieff,et al.  Electrographic imaging of recognition memory in 34–38 week gestation intrauterine growth restricted newborns , 2004, Experimental Neurology.

[33]  T. Kemper,et al.  Effects of prtein undernutrition on the dentate gyrus in rats of three] age groups , 1990, Brain Research.

[34]  Joseph R. Manns,et al.  Recognition Memory and the Human Hippocampus , 2003, Neuron.

[35]  H. Eichenbaum,et al.  Memory, amnesia, and the hippocampal system , 1993 .

[36]  R. Hampson,et al.  Sequence-related changes in sensory-evoked potentials in the dentate gyrus: a mechanism for item-specific short-term information storage in the hippocampus. , 1985, Behavioral and neural biology.

[37]  D L Schacter,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Medial Blockintemporal Blockinlobe Blockinactivation Blockinduring Blockinepisodic Encoding Blockinand Blockinretrieval: Blockina Blockinpet Blockinstudy , 2022 .

[38]  E. Koppitz The Visual Aural Digit Span Test for Seventh Graders , 1981, Journal of learning disabilities.

[39]  R. Geva,et al.  Six-Year Follow-Up of Children With Intrauterine Growth Retardation: Long-Term, Prospective Study , 2000, Journal of child neurology.

[40]  Klaus F. Riegel,et al.  Effects of gestation and birth weight on the growth and development of very low birthweight small for gestational age infants: a matched group comparison , 2000, Archives of disease in childhood. Fetal and neonatal edition.

[41]  C. B. Cave,et al.  Intact verbal and nonverbal short‐term memory following damage to the human hippocampus , 1992, Hippocampus.

[42]  A. Baschat Pathophysiology of Fetal Growth Restriction: Implications for Diagnosis and Surveillance , 2004, Obstetrical & gynecological survey.

[43]  L. Squire,et al.  Neuroanatomy of memory. , 1993, Annual review of neuroscience.

[44]  Gail M Williams,et al.  Learning, cognitive, and attentional problems in adolescents born small for gestational age. , 2003, Pediatrics.

[45]  A. vanWassenaer Neurodevelopmental consequences of being born SGA. , 2005 .

[46]  S. Harel,et al.  Brain: Body ratio and conceptional age in vascular-induced intrauterine growth retarded rabbits , 1985, Brain and Development.

[47]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[48]  J. Bachevalier,et al.  The primate hippocampus: ontogeny, early insult and memory , 2005, Current Opinion in Neurobiology.

[49]  M. Posner,et al.  Hebb's Neural Networks Support the Integration of Psychological Science. , 2004 .

[50]  P. Szatmari,et al.  Psychiatric disorders at five years among children with birthweights less than 1000g: a regional perspective. , 1990, Developmental medicine and child neurology.

[51]  J. L. Talley,et al.  Memory in learning disabled children: digit span and the Rey Auditory Verbal Learning Test. , 1986, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[52]  S. Black,et al.  Memory impairments associated with hippocampal versus parahippocampal-gyrus atrophy: an MR volumetry study in Alzheimer’s disease , 1998, Neuropsychologia.

[53]  Alan Lucas,et al.  Hippocampal Volume and Everyday Memory in Children of Very Low Birth Weight , 2000, Pediatric Research.

[54]  H. Kinney,et al.  Reciprocal entorhinal‐hippocampal connections established by human fetal midgestation , 1996, The Journal of comparative neurology.

[55]  J. Kok,et al.  The discrepancy between maturation of visual-evoked potentials and cognitive outcome at five years in very preterm infants with and without hemodynamic signs of fetal brain-sparing. , 2000, Pediatrics.

[56]  Moshe Y. Vardi,et al.  Characterization of Memory Impairment Following Closed-Head Injury in Children Using the Rey Auditory Verbal Learning Test (AVLT) , 2004, Child neuropsychology : a journal on normal and abnormal development in childhood and adolescence.