Longitudinal magnetic resonance imaging study of rhesus monkey brain development

To examine early brain development, T1‐weighted structural MRI scans of seven rhesus monkeys (Macaca mulatta) were obtained longitudinally between the ages of 1 week and 4 years at 12 age points. Total brain volume, calculated at each age point, increased significantly, by 56%, between 1 week and 4 years. The greatest increase of 22% occurred between 1 week and 1 month, followed by further significant increases between 1 and 2 months, and 3 and 4 months. Gradually smaller increases continued up to 3 years with no further significant changes thereafter. A robust maturation of white matter occurred between 1 week, at which the only easily identifiable fibre tracts were internal capsule and optic radiations, and 3 months, at which most large fibre tracts were visible; only at this age reproducible measurements were possible for all cases. White matter volume increased by 126% between 3 months and 4 years, with the biggest increase between 3 and 4 months (32%) followed by smaller but significant increases up to 4 years. The macaque brain development parallels that of humans by reaching the maximum in total brain volume around the age of sexual maturity (in macaques 3–4 years) and by the increases in white matter continuing beyond this age. The most rapid growth in both total brain volume and white matter from birth to approximately 4 months is consistent with the emergence of various cognitive abilities in macaques at that age.

[1]  R. Passingham,et al.  Anatomical differences between the neocortex of man and other primates. , 1973, Brain, behavior and evolution.

[2]  R. Holloway, The evolution of the primate brain: some aspects of quantitative relations. , 1968, Brain research.

[3]  J. Townsend,et al.  Normal brain development and aging: quantitative analysis at in vivo MR imaging in healthy volunteers. , 2000, Radiology.

[4]  P S Goldman-Rakic,et al.  Development of cortical circuitry and cognitive function. , 1987, Child development.

[5]  T M Mayhew,et al.  A review of recent advances in stereology for quantifying neural structure , 1992, Journal of neurocytology.

[6]  E. Terasawa,et al.  HYPOTHALAMIC CONTROL OF PUBERTY IN THE FEMALE RHESUS MACAQUE1234 , 1983 .

[7]  G. Sackett,et al.  Rearing infant monkeys (Macaca nemestrina) in pairs produces deficient social development compared with rearing in single cages , 1991, American journal of primatology.

[8]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[9]  D. Kennedy,et al.  Magnetic resonance imaging–based brain morphometry: Development and application to normal subjects , 1989, Annals of neurology.

[10]  T. Insel,et al.  Rearing Effects on Cerebrospinal Fluid Oxytocin Concentration and Social Buffering in Rhesus Monkeys , 2003, Neuropsychopharmacology.

[11]  M. Keshavan,et al.  Sex differences in brain maturation during childhood and adolescence. , 2001, Cerebral cortex.

[12]  M. Linnoila,et al.  A nonhuman primate model of type II alcoholism? Part 2. Diminished social competence and excessive aggression correlates with low cerebrospinal fluid 5-hydroxyindoleacetic acid concentrations. , 1996, Alcoholism, clinical and experimental research.

[13]  J. Frank,et al.  Magnetic resonance imaging of the rhesus monkey brain: use for stereotactic neurosurgery , 2004, Experimental Brain Research.

[14]  J. Bachevalier,et al.  Limbic-dependent recognition memory in monkeys develops early in infancy. , 1993, Neuroreport.

[15]  T. Paus Mapping brain maturation and cognitive development during adolescence , 2005, Trends in Cognitive Sciences.

[16]  T. Insel,et al.  The primate neocortex in comparative perspective using magnetic resonance imaging. , 1999, Journal of human evolution.

[17]  J. Bachevalier,et al.  Object recognition versus object discrimination: comparison between human infants and infant monkeys. , 1992, Behavioral neuroscience.

[18]  Alan C. Evans,et al.  Maturation of white matter in the human brain: a review of magnetic resonance studies , 2001, Brain Research Bulletin.

[19]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

[20]  D. Kennedy,et al.  The human brain age 7-11 years: a volumetric analysis based on magnetic resonance images. , 1996, Cerebral cortex.

[21]  J. Giedd Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[22]  M. Mishkin,et al.  Effects of Neonatal Inferior Prefrontal and Medial Temporal Lesions on Learning the Rule for Delayed Nonmatching-to-Sample , 2000, Developmental neuropsychology.

[23]  T. Takeya,et al.  Volumetric quantification of brain development using MRI , 1997, Neuroradiology.

[24]  G. Sacher,et al.  Relation of Gestation Time to Brain Weight for Placental Mammals: Implications for the Theory of Vertebrate Growth , 1974, The American Naturalist.

[25]  Alan C. Evans,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2000, Nature.

[26]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[27]  J. Rilling,et al.  Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys , 1998, Brain Research.

[28]  M. Mishkin,et al.  Early brain pathology and its relation to cognitive impairment: the role of quantitative magnetic resonance techniques. , 1999, Advances in neurology.

[29]  J. Bachevalier,et al.  Revisiting the maturation of medial temporal lobe memory functions in primates. , 2000, Learning & memory.

[30]  Adele Diamond,et al.  Frontal lobe involvement in cognitive changes during the first year of life. , 1991 .

[31]  J. Valk,et al.  MR imaging of the various stages of normal myelination during the first year of life , 2004, Neuroradiology.

[32]  M. Mishkin,et al.  An early and a late developing system for learning and retention in infant monkeys. , 1984, Behavioral neuroscience.

[33]  S. Suomi,et al.  Social interaction in nonhuman primates: an underlying theme for primate research. , 1991, Laboratory animal science.

[34]  A. Reiss,et al.  Brain development, gender and IQ in children. A volumetric imaging study. , 1996, Brain : a journal of neurology.

[35]  M Ashtari,et al.  Computerized volume measurement of brain structure. , 1990, Investigative radiology.

[36]  S. Baron-Cohen,et al.  Autism: a window onto the development of the social and the analytic brain. , 2005, Annual review of neuroscience.

[37]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[38]  H. Gundersen Stereology of arbitrary particles * , 1986, Journal of microscopy.

[39]  Jocelyne Bachevalier,et al.  Non-human primate models of childhood psychopathology: the promise and the limitations. , 2003, Journal of child psychology and psychiatry, and allied disciplines.

[40]  J. Thornton,et al.  Quantitative MRI: a reliable protocol for measurement of cerebral gyrification using stereology. , 2006, Magnetic resonance imaging.

[41]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[42]  O. Pascalis,et al.  Recognition memory in 3- to 4-day-old human neonates. , 1994, Neuroreport.

[43]  Robert B. Innis,et al.  Effects of Early Life Stress on [11C]DASB Positron Emission Tomography Imaging of Serotonin Transporters in Adolescent Peer- and Mother-Reared Rhesus Monkeys , 2006, The Journal of Neuroscience.

[44]  Kathleen R. Gibson,et al.  Myelination and behavioral development: A comparative perspective on questions of neoteny, altriciality and intelligence. , 1991 .

[45]  Gwenn S. Smith,et al.  Alzheimer disease: measuring loss of cerebral gray matter with MR imaging. , 1991, Radiology.

[46]  G. Sackett,et al.  Survival, growth, health, and reproduction following nursery rearing compared with mother rearing in pigtailed monkeys (Macaca nemestrina) , 2002, American journal of primatology.

[47]  G. Press,et al.  Methods for measuring brain morphologic features on magnetic resonance images. Validation and normal aging. , 1990, Archives of neurology.

[48]  P. Goldman-Rakic,et al.  Comparison of human infants and rhesus monkeys on Piaget's AB task: evidence for dependence on dorsolateral prefrontal cortex , 2004, Experimental Brain Research.

[49]  N. Ma,et al.  Social interaction in nonhuman primates: an underlying theme for primate research. , 1991 .

[50]  K. Swartz,et al.  Visual recognition in infant pigtailed macaques after a 24‐hour delay , 1985, American journal of primatology.

[51]  S. Suomi,et al.  Early stress and adult emotional reactivity in rhesus monkeys. , 1991, Ciba Foundation symposium.

[52]  J. Bachevalier Medial temporal lobe structures and autism: A review of clinical and experimental findings , 1994, Neuropsychologia.

[53]  Age and sex differences in the effects of selective temporal lobe lesion on the formation of visual discrimination habits in rhesus monkeys (Macaca mulatta). , 1990, Behavioral neuroscience.

[54]  M. Linnoila,et al.  CSF monoamine metabolite concentrations vary according to age, rearing, and sex, and are influenced by the stressor of social separation in rhesus monkeys , 2005, Psychopharmacology.

[55]  A. Diamond,et al.  Rate of Maturation of the Hippocampus and the Developmental Progression of Children's Performance on the Delayed Non‐Matching to Sample and Visual Paired Comparison Tasks a , 1990, Annals of the New York Academy of Sciences.

[56]  H. Nagaraja,et al.  Timing of Prenatal Stressors and Autism , 2005, Journal of autism and developmental disorders.

[57]  K. Wallen,et al.  Sexual maturation in male rhesus monkeys: importance of neonatal testosterone exposure and social rank. , 1998, The Journal of endocrinology.

[58]  H. Harlow The Nature of Love , 1958 .

[59]  R. Gur,et al.  Age-related volumetric changes of brain gray and white matter in healthy infants and children. , 2001, Cerebral cortex.

[60]  M. Novak,et al.  Pair‐rearing infant monkeys (Macaca nemestrina) using a “rotating‐peer” strategy , 1997, American journal of primatology.

[61]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[62]  J. Bachevalier,et al.  Ontogenetic Development of Habit and Memory Formation in Primates , 1990, Annals of the New York Academy of Sciences.

[63]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[64]  H. Harlow,et al.  Nature of love--simplified. , 1970, The American psychologist.

[65]  G. Sackett,et al.  Social development in nursery‐reared pigtailed macaques (Macaca nemestrina) , 1997, American journal of primatology.

[66]  A. Neuhold,et al.  Down syndrome: MR quantification of brain structures and comparison with normal control subjects. , 1991, AJNR. American journal of neuroradiology.

[67]  M. Bastian,et al.  Long-term effects of infant rearing condition on the acquisition of dominance rank in juvenile and adult rhesus macaques (Macaca mulatta). , 2003, Developmental psychobiology.

[68]  P. Schoenemann,et al.  Prefrontal white matter volume is disproportionately larger in humans than in other primates , 2005, Nature Neuroscience.