Neonatal isolation alters LTP in freely moving juvenile rats: Sex differences

Brain Research Bulletin

Volumn 41, Issue 3, 1996, Pages 175-183

  Bronzino, J D ^a   Kehoe, P ^a   Austin LaFrance, R J ^a   Rushmore, R J ^a   Kurdian, J ^a  

^a TRINITY COLLEGE   (United States)

Author keywords

Dentate Gyrus; Hippocampus; Neonatal Stress; Neuroplasticity

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; STRESS;

EID: 0029814979     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(96)00166-9     Document Type: Article

References (64)

1. 1. Abercrombie, E. D.; Keefe, K. A.; DiFrischia, D. S.; Zigmond, M. J. (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J. Neurochem. 52:1655-1658.
2. 2. Adell, A.; Garcia-Marquez, C.; Armario, A.; Gelpi, E. (1988) Chronic stress increases serotonin and noradrenaline in rat brain and sensitizes their responses to a further acute stress. J. Neurochem. 50:1678-1681.
3. 3. Altaian, J.; Das, G. D.; Anderson, W. J. (1968) Effects of infantile handling on morphological development of the rat brain: An exploratory study. Dev. Psychobiol. 1:10-20.
4. 4. Anisman, H.; Zacharko, R. M. (1990) Multiple neurochemical and behavioral consequences of Stressors: Implications for depression. Pharmacol. Ther. 46:119-136.
5. 5. Arons, C.; Shoemaker, W.; Kehoe, P. (1993) Effects of early stress on the behavioral response of adult rats to an amphetamine challenge. Soc. Neurosci. Abstr. 19:1261.
6. 6. Austin, K. B.; Bronzino, J. D.; Morgane, P. J. (1985) Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Dev. Brain Res. 29:267-273.
7. 7. Bayer, S. A.; Yackel, J. W.; Puri, P. S. (1982) Neurons in the rat dentate gyrus layer substantially increase during juvenile and adult life. Science. 216:890-892.
8. 8. Bliss, T. V. P.; Gardner-Medwin, A. R. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path. J. Physiol. 232:357-374.
9. 9. Bliss, T. V. P.; Lømo, T. (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond), 232:331-356.
10. 10. Bronzino, J. D.; Abu-Hasaballah, K.; Austin-LaFrance, R. J.; Morgane, P. J. ( 1994) Maturation of long-term potentiation in the hippocampal dentate gyrus of the freely-moving rat. Hippocampus, 4:439-446.
11. 11. Camp, D. M.; Robinson, T. E. (1988) Susceptibility to sensitization. II. The influence of gonadal hormones on enduring changes in brain monoamines and behavior produced by repeated administration of D-amphetamine or restraint stress. Behav. Brain Res. 30:69-88.
12. 12. Ceccatelli, S.; Villar, M. J.; Goldstein, M.; Hokfelt, T. (1989) Expression of C-fos immunoreactivity in transmitter-characterized neurons after stress. Proc. Natl. Acad. Sci. 23:9569-9573.
13. 13. Coe, C. L.; Wiener, S. G.; Rosenberg, L. T.; Levine, S. (1985) Physiological consequences of maternal separation in the squirrel monkey. In: Handbook of Squirrel Monkey Research. New York. Plenum Press, L. A. Rosenberg and C. L. Coe, Eds. 127-148.
14. 14. Denenberg, V. H. (1975) Effects of exposure to Stressors in early life upon later behavioral and biological processes. In: (L. Levin, Ed.) Society, Stress and Disease, pp. 268-281. New York: Oxford University Press.
15. 15. Douglass, R. M.; Goddard, G. V. (1975) Long-term potentiation of the perforant path-granule cell synapse in the rat hippocampus. Brain Res. 240:259-272.
16. 16. Duncan, G. E.; Johnson, K. B.; Breese, G. R. (1993) Topographic patterns of brain activity in response to swim stress: Assessment by 2-deoxyglucose uptake and expression of fos-like immunoreactivity. J. Neurosci. 13:3932-3943.
17. 17. Foy, M. R.; Stanton, M. E.; Levine, S.; Thompson, R. F. (1987) Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav. and Neural Biol. 48:138-149.
18. 18. Harvey, A. T.; Moore, H.; Lucot, J. B.; Hennessey, M. B. (1994) Monoamine activity in anterior hypothalamus of guinea pig pups separated from their mothers. Behav. Neurosci. 108:171-176.
19. 19. Hennessey, M. B.; Moorman, L. (1989) Factors influencing cortisol and behavioral responses to maternal separation in guinea pigs. Physiol. Behav. 36:245-250.
20. 20. Hennessey, M. B.; Tamborski, A.; Schiml, P.; Lucot, J. B. (1989) The influence of maternal separation on plasma cortisol concentrations of ACTH, epinephrine, and norepinephrine in guinea pig pups. Pharmacol. Biochem. Behav. 45:1147-1152.
21. 21. Hill, S. D.; McCormack, S. A.; Mason, W. A. (1973) Effects of artificial mothers and visual experience on adrenal responsiveness of infant monkeys. Dev. Psychobiol. 30:421-429.
22. 22. Hofer, M. A.; Brunelli, S. A.; Shair, H. N. (1993) The effects of 24-Hr. maternal separation and of litter size reduction on the isolation-distress response of 12-day-old rat pups. Dev. Psychobiol. 26:483-497.
23. 23. Imperato, A.; Angelucci, L.; Casolini, P.; Zocchi, A.; Puglisi-Allegra, S. (1992) Repeated stressful experiences differentially effect limbic dopamine release during and following stress. Brain Res. 577:194-199.
24. 24. Insel, T. R. (1989) Decreased in vivo binding to brain benzodiazepine receptors during social isolation. Psychopharmacol. 97:142-144.
25. 25. Kalen, P.; Rosegren, E.; Lindvall, O.; Bjorklund, A. (1989) Hippocampal noradrenaline and serotonin release over 24 hours as measured by the dialysis technique in freely moving rats: Correlation to behavioral activity state, effect of handling and tail-pinch. Eur. J. Neurosci. 1:181-188.
26. 26. Kalivas, P. W.; Stewart, J. (1991) Dopamine transmission in the initiation and expression of drug-and stress-induced sensitization of motor activity. Brain Res. Revs. 16:223-244.
27. 27. Kehoe, P.; Blass, E. M. (1986) Opioid-mediation of separation distress in 10-day-old rats: Reversal of stress and maternal stimuli. Psychobiol. 19:385-398.
28. 28. Kehoe, P.; Shoemaker, W. (1991) Opioid-dependent behaviors in infant rats: Effects of prenatal exposure to ethanol. Pharmacol. Biochem. Behav. 39:389-394.
29. 29. Kehoe, P.; Boylan, C. B. (1994) Behavioral effects of kappa opioid receptor stimulation on neonatal rats. Behav. Neurosci. 108:418-423.
30. 30. Kehoe, P.; Hoffman, J. H.; Austin-LaFrance, R. J.; Bronzino, J. D. (1995) Neonatal isolation enhances hippocampal dentate response to tetanization in freely moving juvenile male rats. Exp. Neurol. 136:89-97.
31. 2 binding and dopamine turnover. Pharmacol. Biochem. Behav. 53:41-49.
32. 32. Keller, R. W.; Maisonneuve, I. M.; Nuccio, D. M.; Carlson, J. N.; Glick, S. D. (1994) Effects of prenatal cocaine exposure on the nigrostriatal dopamine system: An in vivo microdialysis study in the rat. Brain Res. 634:266-274.
33. 33. Kolta, M. G.; Scalzo, F. M.; Ali, S. F.; Holson, R. R. (1990) Ontogeny of the enhanced response to amphetamine in amphetamine-pretreated rats. Psychopharmacol. 100:377-382.
34. 34. Levine, S.; Lewis, G. W. (1959) Critical periods for the effects of infantile experience on maturation of the stress response. Science 129:42-43.
35. 35. Lipska, B. K.; Jaskiw, G. E.; Weinberger, D. R. (1993) Postpubertal emergence of hyperresponsiveness to stress and to amphetamine after neonatal excitotoxic hippocampal damage: A potential animal model of schizophrenia. Neurpsychopharmacol. 9:67-75.
36. 36. Lømo, T. (1967) Patterns of activation in a monosynaptic cortical path-dentate granule cell synapse. Exp. Brain Res. 12:46-63.
37. 37. Lømo, T. (1967) Patterns of activation in a monosynaptic cortical pathway: The perforant path input to the dentate area of the hippocampal formation. Exp. Brain Res. 12:18-45.
38. 38. MacLennan, A. J.; Maier, S. F. (1983) Coping and the stress-induced potentiation of stimulant stereotypy in the rat. Science 219:1091-1093.
39. 39. McNaughton, B. L. (1983) Activity dependent modulation of hippocampal synaptic efficacy: Some implications for memory processes. In: (Seifert, W. Ed. Neurobiology of the Hippocampus. New York: Academic Press, 233-252).
40. 40. Maren, S.; De Oca, B.; Fenslow, M. S. (1994) Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: Positive correlation between LTP and contextual learning. Brain Res. 661:25-34.
41. 41. Meany, M. J.; Aitken, D. H.; Bodnoff, S. R.; Iny, L. J.; Tatarewicz, J. E.; Sapolsky, R. M. (1985) Early postnatal handling alters glucocorticoid receptor concentration in selected brain regions. Behav. Neurosci. 99:765-770.
42. 42. Michelson, H. B.; Lothman, E. W. (1989) An in vivo electrophysiological study of the ontogeny of excitatory and inhibitory processes in the rat hippocampus. Dev. Brain Res. 47:113-122.
43. 43. Nisenbaum, L. K.; Zigmond, M. J.; Sved, A. F.; Abercrombie, E. D. (1991) Prior exposure to chronic stress results in enhanced synthesis and release of hippocampal norepinephrine in response to a novel Stressor. J. Neurosci. 11:1478-1484.
44. 44. Robinson, T. E.; Becker, J. B. (1986) Enduring changes in brain and behavior produced by chronic amphetamine administration: A review and evaluation of animal models of amphetamine psychosis. Brain Res. 11:157-198.
45. 45. Robinson, T. E.; Jursons, P. A.; Bennett, J. A.; Bengten, K. A. (1988) Persistent sensitization of dopamine neurotransmission in ventral striatum (nucleus accumbens) produced by prior experience with amphetamine: A microdialysis study in freely moving rats. Brain Res. 194-198.
46. 46. Sapolsky, R. M.; Krey, L. C.; McEwen, B. S. (1985) Prolonged glucocorticoid exposure reduces hippocampal neuron number: Implications for aging. J. Neurosci. 5:1222-1227.
47. 47. Sapolsky, R. M. (1990) Glucocorticoid hippocampal damage and the glutamatergic synapse. In: (Coleman, P. D. et al., Eds), Progress in Brain Research, Vol. 86. (pp. 13-23). Amsterdam Elsevier.
48. 48. Segal, D. S.; Kuczenski, R. (1992) In vivo microdialysis reveals a diminished amphetamine-induced DA response corresponding to behavioral sensitization produced by repeated amphetamine pretreatment. Brain Res. 571:330-377.
49. 49. Shoemaker, W. J.; Kehoe, P. (1994) Effect of isolation conditions on brain regional enkephalin and β-endorphin levels and vocalizations in 10-day-old rat pups. Behav. Neurosci. 109:117-122.
50. 50. Shors, T. J.; Thompson, R. F. (1992) Acute stress impairs (or induces) synaptic long-term potentiation but does not affect paired-pulse facilitation in the stratum radiatum of rat hippocampus. Synapse 11:262-265.
51. 51. Shors, T. J.; Seib, T. B.; Levine, S.; Thompson, R. F. (1989) Inescapable versus escapable shock modulates long-term potentiation (LTP) in rat hippocampus. Science 244:224-226.
52. 52. Shors, T. J.; Foy, M.; Levine, S.; Thompson, R. F. (1990) Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res. Bull. 24:663-667.
53. 53. Simson, P. E.; Weiss, J. M. (1992) Altered electrophysiology of the locus coeruleus following uncontrollable stress: Relationship to anxiety and anxiolytic action. In: (Murburg, M. Ed) Catecholamine Function in Post-Traumatic Stress Disorder, Emerging Concepts. Washington, D.C.; American Psychiatric Press.
54. 54. Spear, L. P.; Enters, E. K.; Aswad, M. A.; Louzan, M. (1985) Drug and environmentally-induced manipulations of the opiate and serotonergic systems alter nociception in neonatal rat pups. Beahv. Neuralbio. 44:1-20.
55. 55. Stanton, M. E.; Gutierrez, Y. R.; Levine, S. (1988) Maternal deprivation potentiates pituitary-adrenal stress responses of infant rats. Behav. Neurosci. 102:692-700.
56. 56. Swanson, L. W.; Sawchenko, P. E.; Lind, R. W. (1986) Regulation of multiple peptides in CRF parvocellular neurosecretory neurons: Implications for the stress response. Prog. Brain Res. 68:169-190.
57. 57. Tamborski, A.; Lucot, J. B.; Hennessey, M. B. (1990) Central dopamine turnover in guinea pigs during separation from their mothers in a novel environment. Behav. Neurosci. 4:607-611.
58. 58. Teyler, T. J.; DiScenna, P. (1984) Long-term potentiation as a candidate mnemonic device. Brain Res. 319:15-28.
59. 59. Teyler, T. J.: DiScenna, P. (1987) Long-term potentiation. Ann Rev. Neurosci. 10:131-161.
60. 60. Watanabe, Y.; Gould, E.; Daniels, D.; Cameron, H.; McEwen, B. S. (1992 ) Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur. J. Pharmacol. 222:157-162.
61. 61. Watanabe, Y.; Gould, E.; McEwen, B. S. (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 588:341-345.
62. 62. Wilson, D. A.; Willner, J.; Kurz, E. M.; Nadel, L. (1986) Early handling increases hippocampal long-term potentiation in young rats. Behav. Brain Res. 21:223-227.
63. 63. Woolley, C. A.; Gould, E.; McEwen, B. S. (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 531:225-231.
64. 64. Zimmerberg, B.; Shartrand, A. M. (1992) Temperature-dependent effects of maternal separation on growth, activity, and amphetamine sensitivity in the rat. Dev. Psychobiol. 25:213-226.