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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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.
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.
Huttenlocher PR: Morphometric study of human cerebral cortex development. Neuropsychologia 5:517–527, 1990.
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.
Finlay B, Slattery M: Local differences in the amount of early cell death in neocortex predict local specialization. Science 219:1349–1351, 1983
Joseph R: The Neuropsychology of Development: Hemispheric Laterality, Limbic Language, and the Origin of Thought. J Clin Psychol 44:3–34, 1982.
Joseph R: The Limbic System: Emotion, Laterality, and Unconscious Mind. Psychoanalytic Rev 79:405–456, 1992.
Joseph R: Limbic language, social-emotional intelligence, development and attachment. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience. Baltimore: Williams & Wilkins, 1996.
Joseph R: Fetal brain-behavior and cognitive development. Dev Rev, in press.
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.
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.
Greenough WT, Black JE: Inducation of brain structure by experience: Substrates for cognitive development. In Minnesota Symposia in Child Development. Hillsdale, NJ: Erlbaum, 1992.
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.
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.
Stein MB, Hannah C. Koverloa, C, McClarty B: Neuroanatomic and cognitive correlates of early abuse. Am Psychiat Ass Sylab Proceed Sum 148:113, 1995.
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.
Henriksen SJ, Bloom FE, McCoy F: B-endrophin induces nonconvulsive limbic seizures. Proc Nat Acad Sciences 75:5221–5225, 1978.
Heath R: Studies in schizophrenia. Cambridge. Harvard University Press, 1954.
Kraemer GW: A psychobiological theory of attachment. Beh Brain Sciences 15:493–541, 1992.
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.
Casagrande VA, Joseph R: Effects of monocular deprivation on geniculostriate connections in prosimian primates. Anatomical Rec 190:359, 1978.
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.
Gyllenstein L, Malmfors T, Norrlin ML: Growth alteration in the auditory cortex of visually deprived mice. J Comp Neurology, 126:463–470, 1966.
Hubel DH, Wiesel TN: Receptive fields and functional architecture of monkey striate cortex. J Physiol, 195:215–243, 1968.
Hyvarinen J: The Parietal Cortex of Monkey and Man. Berlin: Springer Verlag, 1982.
Joseph R, Casagrande VA: Visual field defects and morphological changes resulting from monocular deprivation in primates. Proceed Soc Neuroscience, 4:2021, 1978.
Joseph R, Casagrande, VA: Visual deficits and recovery following monocular lid closure in a prosimian primate. Behav Brain Res 1:165–186, 1980.
Joseph R, Gallagher RE: Gender and early environmental influences on activity, overresponsiveness, and exploration. Developm Psychobiology 13:527–544, 1980.
Joseph R: The neuroanatomy and neurophysiology of repression, dissociation, and traumatic stress. In Neuropsychiatry, Neuropsychology, Clinical Neuroscience. Baltimore: Williams & Wilkins, 1996.
Bowlby J: Separation anxiety. International J Psychoanalysis 412:1–25, 1960.
Bowlby J: Attachment and Loss. New York: Basic Books, 1982.
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.
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.
Spitz RA: Hospitalism: an inquiry into the genesis of psychiatric conditions in early childhood. Psychoanalytical Study Child. 1:53–74, 1945.
Spitz RA: Hospitalism: A follow up report. Psychoanalytic Study Child 1:53–74, 1946.
Joseph R: Traumatic amnesia, repression, and hippocampal injury due to corticosteroid and enkephalin secretion. Child Psychiat Hum Developm In press
Joseph R: Effects of rearing and sex on learning and competitive exploration. J Psychol 101:37–43, 1979.
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.
Cicchetti D. Tucker D: Development and self-regulatory structures of the mind. Developm Psychopathology 6:533–549, 1994.
Dennis W: Causes of retardation Among Institutionalized Children. J Gen Psychol 96:47–59, 1975.
Goldfarb W: Effects of early institutional care on adolescent personality. J Exp Ed 12, 106–1129, 1943.
Goldfarb W: Psychological privation in infancy and subsequent adjustment. Am J Orthopsychiat 15:247–255, 1945.
Goldfarb W: Variations in adolescent adjustment of institutionally-reared children. Am J Orthopsychiat 17:449–457, 1946.
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.
Joseph R: Reversal of cerebral dominance for language and emotion in a corpus callosotomy patient. J Neurol Neurosurg Psychiat 49:628–634, 1986.
Raisman G: Neural plasticity in the septal nuclei of the rat. Brain Res 14: 25–48, 1969.
Sroufe LA: Emotional Development. New York: Cambridge U. Press. 1996.
Sroufe LA: Psychopathology as an outcome of development. Developm Psychopathology 9:251–268, 1997.
De Wolff MS, Ijzendoorn H van: Sensitivity and attachment: A meta-analysis on parental antecedents of infant attachment. Child Developm 68:571–591, 1997.
Isabella RA:. Origins of attachment: Maternal interactive behavior across the first year. Child Developm 64:605–621, 1993
Charlesworth WR, Kreutzer MA: Facial expressions of infants and children. In Darwin and Facial Expression. ed. Ekman P. New York: Academic Press, 1973.
Spitz RA, Wolf KM: The smiling response: A contribution to the ontogenesis of social relations. Gen Psychol Monographs. 34, 57–125, 1946.
Cairns RB: The attachment behavior of mammals. Psychol Rev, 73:409–426, 1967.
Fisher AE: The effects of differential early treatment in on the social and exploratory behavior of puppies. Doctoral Disseration. Pennsylvania State University, 1955.
Hoffman HS, DePaulo P: Behavioral control by an imprinting stimulus. Am Scientist 65:58–66, 1977.
Melzack R, Scott TH: The effects of early experience on the response to pain. J Comp Physiol Psychol 50:155–161, 1957.
Gloor P: Role of the amygdala in temporal lobe epilepsy. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
Halgren E: Emotional neurophysiology of the amygdala within the context of human cognition. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
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.
Kling AS, Brothers LA: The amygdala and social behavior. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
LeDoux JE: Emotion and the amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
MacLean P: The Evolution of the Triune Brain. New York: Plenum, 1990.
Devinksy O, Morrell MJ, Vogt BA: Contributions of anterior cingulate cortex to behaviour. Brain 118:279–306, 1995.
Jurgens U: Vocal communication in primates. In Neurobiology of Comparative Cognition. eds. Kesner RP, Olton DS. New Jersey: Erlbaum, 1990.
Lilly R, Cummings JL, Benson F, Frankel M: The human Kluver-Bucy syndrome. Neurology 3:1141–1145, 1983.
Marlowe WB, Mancall EL, Thomas JJ: Complete Kluver-Bucy syndrome in man. Cortex 11:53–59, 1975.
Ramamurthi B: Stereotactic operation in behavior disorders. Amygdalotomy and hypothalamotomy. Acta Neurochir 44:152–157, 1988.
Terzian H, Ore GD: Syndrome of Kluver and Bucy in man by bilateral removal of temporal lobes. Neurology 5:373–380, 1955.
Kling A, Steklis HD: A neural substrate for affiliative behavior in nonhuman primates. Brain, Beh Evol 13:216–238, 1976.
Schore AN: Affect Regulation and the Origin of Self. New Jersey: Erlbaum, 1994.
Bronson GW: Infants reactions to unfamiliar persons and novel objects. Mon Soc Res Child Developm 37:3. Serial No. 148, 1972.
Schaffer HR: The onset of fear of strangers and the incongruity hypothesis. J Child Psychol Psychiat 7:95–106, 1966.
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.
Rolls ET: Neurophysiology and functions of the primate amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
Stevens JR: Psychosis and the temporal lobe. In Neurobehavioral Problems in Epilepsy. ed. Smith DB. New York: Raven, 1991.
Perez NM: Trimble MR, Murray NMF, Reider I: Epileptic psychosis. British J Psychiat 146:155–163, 1985.
Flor-Henry P: Cerebral basis of psychopathology. Boston: John Wright, 1983.
Cain DP: Kindling and the amygdala. In The Amygdala. ed. Aggleton JP. New York: Wiley, 1992.
Heath RG: Physiological basis of emotional expression. Biol Psychiat 5: 172–184, 1972.
Jonason KR, Enloe LJ: Alterations in social behavior following septal and amygdaloid lesions in the rat. J Comp Phys Psychol 75: 280–301, 1972.
McClary RA: Response-modulating functions of the limbic system. In Progress in Physiological Psychology. eds. Stellar E., Sprague JM. New York: Academic Press, 1966.
Meyer DR, Ruth RA, Lavond DG: The septal social cohesiveness effect. Physiol Beh 21:1027–1029, 1978.
Kluver H, Bucy PC: Preliminary analysis of functions of the temporal lobes in monkeys. Arch Neurol Psychiat 542:979–1000, 1939.
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.
Rosenblum LA, Coplan JD, Friedman T: Adverse early experiences affect noradrenergic and serotonergic functioning in adult primates. Biol Psychiat 35:221–227, 1994.
Bear MF, Singer W: Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320:172–176, 1986.
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.
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.
Pettigrew JD, Kasamatsu T: Local perfusion of noradrenaline maitnains visual plasticity. Nature 271: 761–763, 1978.
Sapolsky RM: Why stress is bad for your brain. Science 273:749–750, 1996.
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
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.
Nadel L: The hippocampus and space revisited. Hippocampus 1:221–229, 1991.
O'keefe J: Place units in the hippocampus of the freely moving rat. Exp Neurology 51:78–109, 1976.
Squire LR: Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231, 1992.
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.
Douglas J: The Unabomber. New York: Pocket Books, 1996.
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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
- Neural Plasticity
- Septal Nuclei
- Cingulate Gyrus
- the Unabomber