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Environmental Influences on Neural Plasticity, the Limbic System, Emotional Development and Attachment: A Review

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Abstract

The effects of early environmental influences on neural plasticity, the limbic system, and social and emotional development are reviewed and an illustrative case study is briefly discussed. Deprived or abnormal rearing conditions induce severe disturbance in all aspects of social and emotional functioning, and effect the growth and survival of dendrites, axons, synapses, interneurons, neurons, and glia. The amygdala, cingulate, and septal nuclei develop at different rates which correlate with the emergence of wariness, fear, selective attachments, play behavior, and the oral and phallic stages of development. These immature limbic nuclei are “experience-expectant,” and may be differentially injured depending on the age at which they suffer deprivation. The medial amygdala and later the cingulate and septal nuclei are the most vulnerable during the first three years of life. If denied sufficient stimulation these nuclei may atrophy, develop seizure-like activity or maintain or form abnormal synaptic interconnections, resulting in social withdrawal, pathological shyness, explosive and inappropriate emotionality, and an inability to form normal emotional attachments.

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References

  1. Benes FM: Development of the corticolimbic system. In Human Behavior and the Developing Brain. eds. Dawson G, K. W. Fischer KW. New York: Guilford Press, 1994.

    Google Scholar 

  2. Yakovlev PI, Lecours A-R: The myelogenetic cycles of regional maturation of the brain. In Regional Development of the Brain in Early Life. ed. Minkowski A. Davis: Philadelphia, 1967.

    Google Scholar 

  3. Huttenlocher PR: Morphometric study of human cerebral cortex development. Neuropsychologia 5:517–527, 1990.

    Google Scholar 

  4. Rakic P, Bourgeois J.-P, Echenhoff MF, Zaecevic N, Goldman-Rakic P: Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232: 232–235, 1986.

    Google Scholar 

  5. Finlay B, Slattery M: Local differences in the amount of early cell death in neocortex predict local specialization. Science 219:1349–1351, 1983

    Google Scholar 

  6. Joseph R: The Neuropsychology of Development: Hemispheric Laterality, Limbic Language, and the Origin of Thought. J Clin Psychol 44:3–34, 1982.

    Google Scholar 

  7. Joseph R: The Limbic System: Emotion, Laterality, and Unconscious Mind. Psychoanalytic Rev 79:405–456, 1992.

    Google Scholar 

  8. Joseph R: Limbic language, social-emotional intelligence, development and attachment. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience. Baltimore: Williams & Wilkins, 1996.

    Google Scholar 

  9. Joseph R: Fetal brain-behavior and cognitive development. Dev Rev, in press.

  10. Diamond MC: Rat forebrain morphology: Right-left; male-female; young-old, enriched-impoverished. In Cerebral Lateralization in Nonhuman Primates. ed. Glick SD. Orlando, Academic Press, 1985.

    Google Scholar 

  11. Diamond MC: Environmental influences on the young brain. In Brain Maturation and Cognitive Development. eds. Gibson KR. Petersen, AC New York: Aldine De Gruyter, 1991.

    Google Scholar 

  12. Greenough WT, Black JE: Inducation of brain structure by experience: Substrates for cognitive development. In Minnesota Symposia in Child Development. Hillsdale, NJ: Erlbaum, 1992.

    Google Scholar 

  13. Walsh RN, Budtz-Olsen OE, Penny J, Cummins RA: The effects of environmental complexity on the histology of the rat hippocampus. J Comp Neurol 137:261–266, 1969.

    Google Scholar 

  14. Bremner JD, Randall PK, Southwick SM, Krystal JH, Innis RB, Charney DS: Stress-induced changes in memory and development. Am Psychiat Ass Sylab Proc Sum 148:112, 1995.

    Google Scholar 

  15. Stein MB, Hannah C. Koverloa, C, McClarty B: Neuroanatomic and cognitive correlates of early abuse. Am Psychiat Ass Sylab Proceed Sum 148:113, 1995.

    Google Scholar 

  16. Gahwiler BH: The action of neuropeptides on the bioelectric activity of hippocampal neurons. In Neurobiology of the Hippocampus. ed. Seifert W. San Diego, Academic Press, 1983.

    Google Scholar 

  17. Henriksen SJ, Bloom FE, McCoy F: B-endrophin induces nonconvulsive limbic seizures. Proc Nat Acad Sciences 75:5221–5225, 1978.

    Google Scholar 

  18. Heath R: Studies in schizophrenia. Cambridge. Harvard University Press, 1954.

    Google Scholar 

  19. Kraemer GW: A psychobiological theory of attachment. Beh Brain Sciences 15:493–541, 1992.

    Google Scholar 

  20. Greenough W, Chang F-LF: Plasticity of synapse structure and pattern in the cerebral cortex. In Cerbral Cortex. Vol. 7. Peters A, Jones E. eds. New York: Plenum, 1988.

    Google Scholar 

  21. Casagrande VA, Joseph R: Effects of monocular deprivation on geniculostriate connections in prosimian primates. Anatomical Rec 190:359, 1978.

    Google Scholar 

  22. Casagrande VA, Joseph R: Morphological effects of monocular deprivation and recovery on the dorsal lateral geniculate nucleus in galago. J Comp Neurology, 194:413–426, 1980.

    Google Scholar 

  23. Gyllenstein L, Malmfors T, Norrlin ML: Growth alteration in the auditory cortex of visually deprived mice. J Comp Neurology, 126:463–470, 1966.

    Google Scholar 

  24. Hubel DH, Wiesel TN: Receptive fields and functional architecture of monkey striate cortex. J Physiol, 195:215–243, 1968.

    Google Scholar 

  25. Hyvarinen J: The Parietal Cortex of Monkey and Man. Berlin: Springer Verlag, 1982.

    Google Scholar 

  26. Joseph R, Casagrande VA: Visual field defects and morphological changes resulting from monocular deprivation in primates. Proceed Soc Neuroscience, 4:2021, 1978.

    Google Scholar 

  27. Joseph R, Casagrande, VA: Visual deficits and recovery following monocular lid closure in a prosimian primate. Behav Brain Res 1:165–186, 1980.

    Google Scholar 

  28. Joseph R, Gallagher RE: Gender and early environmental influences on activity, overresponsiveness, and exploration. Developm Psychobiology 13:527–544, 1980.

    Google Scholar 

  29. Joseph R: The neuroanatomy and neurophysiology of repression, dissociation, and traumatic stress. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience. Baltimore: Williams & Wilkins, 1996.

    Google Scholar 

  30. Bowlby J: Separation anxiety. International J Psychoanalysis 412:1–25, 1960.

    Google Scholar 

  31. Bowlby J: Attachment and Loss. New York: Basic Books, 1982.

    Google Scholar 

  32. Geyer MA, Wilkinson LS, Humby T, Robbins TW: Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol Psychiatry 34:361–372, 1993.

    Google Scholar 

  33. Harlow H, Harlow MK: Effects of various mother-infant relationships on rhesus monkey behaviors. In Determinants of Infant Behavior. ed. B. M. Foss BM. New York: Methuen, 1965.

    Google Scholar 

  34. Spitz RA: Hospitalism: an inquiry into the genesis of psychiatric conditions in early childhood. Psychoanalytical Study Child. 1:53–74, 1945.

    Google Scholar 

  35. Spitz RA: Hospitalism: A follow up report. Psychoanalytic Study Child 1:53–74, 1946.

    Google Scholar 

  36. Joseph R: Traumatic amnesia, repression, and hippocampal injury due to corticosteroid and enkephalin secretion. Child Psychiat Hum Developm In press

  37. Joseph R: Effects of rearing and sex on learning and competitive exploration. J Psychol 101:37–43, 1979.

    Google Scholar 

  38. Camras LA, Ribrody S, HIlls J, Martino S, Sachs V, Spaccarellis S, Stefani R: Maternal facial behavior and the recognition and production of emotional expression by maltreated and nonmaltreated children. Developm Psychol 26: 304–312, 1990.

    Google Scholar 

  39. Cicchetti D. Tucker D: Development and self-regulatory structures of the mind. Developm Psychopathology 6:533–549, 1994.

    Google Scholar 

  40. Dennis W: Causes of retardation Among Institutionalized Children. J Gen Psychol 96:47–59, 1975.

    Google Scholar 

  41. Goldfarb W: Effects of early institutional care on adolescent personality. J Exp Ed 12, 106–1129, 1943.

    Google Scholar 

  42. Goldfarb W: Psychological privation in infancy and subsequent adjustment. Am J Orthopsychiat 15:247–255, 1945.

    Google Scholar 

  43. Goldfarb W: Variations in adolescent adjustment of institutionally-reared children. Am J Orthopsychiat 17:449–457, 1946.

    Google Scholar 

  44. Izard CE, Harris P: Emotional development and developmental psychopathology. In Developmental Psychopathology: Vol. 1. Theory and Methods. eds. Cicchetti D, Cohen C. New York: Wiley, 1995.

    Google Scholar 

  45. Joseph R: Reversal of cerebral dominance for language and emotion in a corpus callosotomy patient. J Neurol Neurosurg Psychiat 49:628–634, 1986.

    Google Scholar 

  46. Raisman G: Neural plasticity in the septal nuclei of the rat. Brain Res 14: 25–48, 1969.

    Google Scholar 

  47. Sroufe LA: Emotional Development. New York: Cambridge U. Press. 1996.

    Google Scholar 

  48. Sroufe LA: Psychopathology as an outcome of development. Developm Psychopathology 9:251–268, 1997.

    Google Scholar 

  49. De Wolff MS, Ijzendoorn H van: Sensitivity and attachment: A meta-analysis on parental antecedents of infant attachment. Child Developm 68:571–591, 1997.

    Google Scholar 

  50. Isabella RA:. Origins of attachment: Maternal interactive behavior across the first year. Child Developm 64:605–621, 1993

    Google Scholar 

  51. Charlesworth WR, Kreutzer MA: Facial expressions of infants and children. In Darwin and Facial Expression. ed. Ekman P. New York: Academic Press, 1973.

    Google Scholar 

  52. Spitz RA, Wolf KM: The smiling response: A contribution to the ontogenesis of social relations. Gen Psychol Monographs. 34, 57–125, 1946.

    Google Scholar 

  53. Cairns RB: The attachment behavior of mammals. Psychol Rev, 73:409–426, 1967.

    Google Scholar 

  54. Fisher AE: The effects of differential early treatment in on the social and exploratory behavior of puppies. Doctoral Disseration. Pennsylvania State University, 1955.

  55. Hoffman HS, DePaulo P: Behavioral control by an imprinting stimulus. Am Scientist 65:58–66, 1977.

    Google Scholar 

  56. Melzack R, Scott TH: The effects of early experience on the response to pain. J Comp Physiol Psychol 50:155–161, 1957.

    Google Scholar 

  57. Gloor P: Role of the amygdala in temporal lobe epilepsy. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  58. Halgren E: Emotional neurophysiology of the amygdala within the context of human cognition. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  59. Kling A: Effects of amygdalectomy on social-affective behavior in non-human primates. In The Neurobiology of the Amygdala. ed. Eleftherious BE. New York: Plenum, 1972.

    Google Scholar 

  60. Kling AS, Brothers LA: The amygdala and social behavior. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  61. LeDoux JE: Emotion and the amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  62. MacLean P: The Evolution of the Triune Brain. New York: Plenum, 1990.

    Google Scholar 

  63. Devinksy O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306, 1995.

    Google Scholar 

  64. Jurgens U: Vocal communication in primates. In Neurobiology of Comparative Cognition. eds. Kesner RP, Olton DS. New Jersey: Erlbaum, 1990.

    Google Scholar 

  65. Lilly R, Cummings JL, Benson F, Frankel M: The human Kluver-Bucy syndrome. Neurology 3:1141–1145, 1983.

    Google Scholar 

  66. Marlowe WB, Mancall EL, Thomas JJ: Complete Kluver-Bucy syndrome in man. Cortex 11:53–59, 1975.

    Google Scholar 

  67. Ramamurthi B: Stereotactic operation in behavior disorders. Amygdalotomy and hypothalamotomy. Acta Neurochir 44:152–157, 1988.

    Google Scholar 

  68. Terzian H, Ore GD: Syndrome of Kluver and Bucy in man by bilateral removal of temporal lobes. Neurology 5:373–380, 1955.

    Google Scholar 

  69. Kling A, Steklis HD: A neural substrate for affiliative behavior in nonhuman primates. Brain, Beh Evol 13:216–238, 1976.

    Google Scholar 

  70. Schore AN: Affect Regulation and the Origin of Self. New Jersey: Erlbaum, 1994.

    Google Scholar 

  71. Bronson GW: Infants reactions to unfamiliar persons and novel objects. Mon Soc Res Child Developm 37:3. Serial No. 148, 1972.

    Google Scholar 

  72. Schaffer HR: The onset of fear of strangers and the incongruity hypothesis. J Child Psychol Psychiat 7:95–106, 1966.

    Google Scholar 

  73. Waters E, Matas L, Stroufe LA: Infant's reactions to an approaching stranger: description, validation and functional significance of wariness. Child Developm 46:348–356, 1975.

    Google Scholar 

  74. Rolls ET: Neurophysiology and functions of the primate amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  75. Stevens JR: Psychosis and the temporal lobe. In Neurobehavioral Problems in Epilepsy. ed. Smith DB. New York: Raven, 1991.

    Google Scholar 

  76. Perez NM: Trimble MR, Murray NMF, Reider I: Epileptic psychosis. British J Psychiat 146:155–163, 1985.

    Google Scholar 

  77. Flor-Henry P: Cerebral basis of psychopathology. Boston: John Wright, 1983.

    Google Scholar 

  78. Cain DP: Kindling and the amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.

    Google Scholar 

  79. Heath RG: Physiological basis of emotional expression. Biol Psychiat 5: 172–184, 1972.

    Google Scholar 

  80. Jonason KR, Enloe LJ: Alterations in social behavior following septal and amygdaloid lesions in the rat. J Comp Phys Psychol 75: 280–301, 1972.

    Google Scholar 

  81. McClary RA: Response-modulating functions of the limbic system. In Progress in Physiological Psychology. eds. Stellar E., Sprague JM. New York: Academic Press, 1966.

    Google Scholar 

  82. Meyer DR, Ruth RA, Lavond DG: The septal social cohesiveness effect. Physiol Beh 21:1027–1029, 1978.

    Google Scholar 

  83. Kluver H, Bucy PC: Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiat 542:979–1000, 1939.

    Google Scholar 

  84. Panksepp J, Normansell, L, Herman, B: Neural and neurochemical control of the separation distress call. In The Physiological Control of Mammalian Behavior. Ed. Newman JD. New York: Plenum, 1988.

    Google Scholar 

  85. Rosenblum LA, Coplan JD, Friedman T: Adverse early experiences affect noradrenergic and serotonergic functioning in adult primates. Biol Psychiat 35:221–227, 1994.

    Google Scholar 

  86. Bear MF, Singer W: Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172–176, 1986.

    Google Scholar 

  87. Higley JD, Suomi SJ, Linnoila M: A longitudinal assessment of CSF monoamine metabolite and plasma concentrations in young rhesus monkeys. Bio Psychiat 32:127–145, 1992.

    Google Scholar 

  88. Parnavelas JG, Papadopoulos GC, Cavanagh ME: Changes in neurotransmitters during development. In Cerebral Cortex. vol. 7. eds. Peters A, Jones EG. New York: Plenum, 1988.

    Google Scholar 

  89. Pettigrew JD, Kasamatsu T: Local perfusion of noradrenaline maitnains visual plasticity. Nature 271: 761–763, 1978.

    Google Scholar 

  90. Sapolsky RM: Why stress is bad for your brain. Science 273:749–750, 1996.

    Google Scholar 

  91. Lupien SJ, McEwen BS: The acute effects of corticosteroids on cognition: integration of animal and human model studies. Brain Res Rev 24:1–27, 1997

    Google Scholar 

  92. Milner B: Memory and the medial temporal regions of the brain. In Biology of Memory. eds. Pribram K, Broadbent D. New York: Academic Press, 1970.

    Google Scholar 

  93. Nadel L: The hippocampus and space revisited. Hippocampus 1:221–229, 1991.

    Google Scholar 

  94. O'keefe J: Place units in the hippocampus of the freely moving rat. Exp Neurology 51:78–109, 1976.

    Google Scholar 

  95. Squire LR: Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231, 1992.

    Google Scholar 

  96. Rolls ET: Functions of neural networks in the hippocampus and neocortex in memory. In Neural Models of Plasticity: Theoretical and Empirical Approaches. ed. Byrne JH, Berry WO. New York: Acaemic Press, 1988.

    Google Scholar 

  97. Douglas J: The Unabomber. New York: Pocket Books, 1996.

    Google Scholar 

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Joseph, R. Environmental Influences on Neural Plasticity, the Limbic System, Emotional Development and Attachment: A Review. Child Psychiatry Hum Dev 29, 189–208 (1999). https://doi.org/10.1023/A:1022660923605

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