Acute stress and hippocampal output: Exploring dorsal CA1 and subicular synaptic plasticity simultaneously in anesthetized rats

Physiological Reports

Volumn 1, Issue 2, 2013, Pages

  Macdougall, Matthew J ^a   Howland, John G ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Hippocampus; In vivo electrophysiology; Late developing potentiation; Long term potentiation; Paired pulse facilitation

Indexed keywords

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIORAL STRESS; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTOLOGY; INFORMATION PROCESSING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; RAT;

EID: 85008969534     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.1002/phy2.35     Document Type: Article

References (53)

1. Amaral, D. G., and M. P. Witter. 1989. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31: 571–591.
2. Amaral, D. G., C. Dolorfo, and P. Alvarez-Royo. 1991. Organization of CA1 projections to the subiculum: a PHA-L analysis in the rat. Hippocampus 1: 415–435.
3. Andersen, P., R. Morris, T. Bliss, D. Amaral, and J. O’Keefe. 2006. The hippocampus book. Oxford Univ. Press, New York, NY.
4. Anderson, M., S. Commins, and S. M. O’Mara. 2000. The effects of low frequency and two-pulse stimulation protocols on synaptic transmission in the CA1-subiculum pathway in the anaesthetized rat. Neurosci. Lett. 279: 181–184.
5. Behr, J., C. Wozny, P. Fidzinski, and D. Schmitz. 2009. Synaptic plasticity in the subiculum. Prog. Neurobiol. 89: 334–342.
6. Buckmaster, P. S., B. W. Strowbridge, and P. A. Schwartzkroin. 1993. A comparison of rat hippocampal mossy cells and CA3c pyramidal cells. J. Neurophysiol. 70: 1281–1299.
7. Cazakoff, B. N., and J. G. Howland. 2010. Acute stress disrupts paired pulse facilitation and long-term potentiation in rat dorsal hippocampus through activation of glucocorticoid receptors. Hippocampus 20: 1327–1331.
8. Cazakoff, B. N., K. J. Johnson, and J. G. Howland. 2010. Converging effects of acute stress on spatial and recognition memory in rodents: a review of recent behavioural and pharmacological findings. Prog. Neuropsychopharmacol. Biol. Psychiatry 34: 733–741.
9. Collingridge, G. L., S. Peineau, J. G. Howland, and Y. T. Wang. 2010. Long-term depression in the CNS. Nat. Rev. Neurosci. 11: 459–473.
10. Commins, S., J. Gigg, M. Anderson, and S. M. O’Mara. 1998a. Interaction between paired-pulse facilitation and long-term potentiation in the projection from hippocampal area CA1 to the subiculum. NeuroReport 9: 4109–4113.
11. Commins, S., J. Gigg, M. Anderson, and S. M. O’Mara. 1998b. The projection from hippocampal area CA1 to the subiculum sustains long-term potentiation. NeuroReport 9: 847–850.
12. Commins, S., L. A. O’Neill, and S. M. O’Mara. 2001. The effects of the bacterial endotoxin lipopolysaccharide on synaptic transmission and plasticity in the CA1-subiculum pathway in vivo. Neuroscience 102: 273–280.
13. Commins, S., J. P. Aggleton, and S.M. O’Mara. 2002. Physiological evidence for a possible projection from dorsal subiculum to hippocampal area CA1. Exp. Brain Res. 146: 155–160.
14. Deadwyler, S. A., and R. E. Hampson. 2004. Differential but complementary mnemonic functions of the hippocampus and subiculum. Neuron 42: 465–476.
15. Diamond, D. M., and G. M. Rose. 1994. Stress impairs LTP and hippocampal-dependent memory. Ann. N. Y. Acad. Sci. 746: 411–414.
16. Diamond, D. M., A. M. Campbell, C. R. Park, J. Halonen, and P. R. Zoladz. 2007. The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast. 2007: 60803.
17. Fidzinski, P., O. Shor, and J. Behr. 2008. Target-cell-specific bidirectional synaptic plasticity at hippocampal output synapses. Eur. J. Neurosci. 27: 1111–1118.
18. Fox, C. J., K. Russell, A. K. Titterness, Y. T. Wang, and B. R. Christie. 2007. Tyrosine phosphorylation of the GluR2 subunit is required for long-term depression of synaptic efficacy in young animals in vivo. Hippocampus 17: 600–605.
19. Habib, D., and H. C. Dringenberg. 2010. Low-frequency-induced synaptic potentiation: a paradigm shift in the field of memory-related plasticity mechanisms? Hippocampus 20: 29–35.
20. Howland, J. G., and Y. T. Wang. 2008. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog. Brain Res. 169: 145–158.
21. Huang, Y. Y., and E. R. Kandel. 2005. Theta frequency stimulation up-regulates the synaptic strength of the pathway from CA1 to subiculum region of hippocampus. Proc. Natl. Acad. Sci. USA 102: 232–237.
22. Joels, M., Z. Pu, O. Wiegert, M. S. Oitzl, and H. J. Krugers. 2006. Learning under stress: how does it work? Trends Cogn. Sci. 10: 152–158.
23. Joels, M., R. A. Sarabdjitsingh, and H. Karst. 2012. Unraveling the time domains of corticosteroid hormone influences on brain activity: rapid, slow, and chronic modes. Pharmacol. Rev. 64: 901–938.
24. Karst, H., S. Berger, M. Turiault, F. Tronche, G. Schutz, and M. Joels. 2005. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. USA 102: 19204–19207.
25. Kim, J. J., and D. M. Diamond. 2002. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3: 453–462.
26. Kim, J. J., M. R. Foy, and R. F. Thompson. 1996. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc. Natl. Acad. Sci. USA 93: 4750–4753.
27. Kim, J. J., J. W. Koo, H. J. Lee, and J. S. Han. 2005. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 25: 1532–1539.
28. Klug, A., J. G. Borst, B. A. Carlson, C. Kopp-Scheinpflug, V. A. Klyachko, and M. A. Xu-Friedman. 2012. How do short-term changes at synapses fine-tune information processing? J. Neurosci. 32: 14058–14063.
29. MacDougall, M. J., and J. G. Howland. 2013. Acute stress, but not corticosterone, disrupts short-and long-term synaptic plasticity in rat dorsal subiculum via glucocorticoid receptor activation. Cereb. Cortex (in press). PMID: 22918985.
30. Maggio, N., and M. Segal. 2007. Striking variations in corti costeroid modulation of long-term potentiation along the septotemporal axis of the hippocampus. J. Neurosci. 27: 5757–5765.
31. Malenka, R. C., and M. F. Bear. 2004. LTP and LTD: an embarrassment of riches. Neuron 44: 5–21.
32. Martin, S. J., P. D. Grimwood, and R. G. Morris. 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23: 649–711.
33. Massey, P. V., and Z. I. Bashir. 2007. Long-term depression: multiple forms and implications for brain function. Trends Neurosci. 30: 176–184.
34. McNaughton, B. L., C. A. Barnes, J. L. Gerrard, K. Gothard, M. W. Jung, J. J. Knierim, et al. 1996. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J. Exp. Biol. 199: 173–185.
35. Morris, R. G., F. Schenk, F. Tweedie, and L. E. Jarrard. 1990. Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 2: 1016–1028.
36. Naber, P. A., F. H. Lopes da Silva, and M. P. Witter. 2001a. Reciprocal connections between the entorhinal cortex and hippocampal fields CA1 and the subiculum are in register with the projections from CA1 to the subiculum. Hippocampus 11: 99–104.
37. Naber, P. A., M. P. Witter, and F. H. Lopes da Silva. 2001b. Evidence for a direct projection from the postrhinal cortex to the subiculum in the rat. Hippocampus 11: 105–117.
38. O’Keefe, J., and L. Nadel. 1978. The hippocampus as a cognitive map. Oxford Univ. Press, Oxford, U.K.
39. O’Mara, S. M., S. Commins, M. Anderson, and J. Gigg. 2001. The subiculum: a review of form, physiology and function. Prog. Neurobiol. 64: 129–155.
40. O’Mara, S. M., M. V. Sanchez-Vives, J. R. Brotons-Mas, and E. O’Hare. 2009. Roles for the subiculum in spatial information processing, memory, motivation and the temporal control of behaviour. Prog. Neuropsychopharmacol. Biol. Psychiatry 33: 782–790.
41. Passecker, J., V. Hok, A. Della-Chiesa, E. Chah, and S. M. O’Mara. 2011. Dissociation of dorsal hippocampal regional activation under the influence of stress in freely behaving rats. Front. Behav. Neurosci. 5: 66.
42. Paxinos, G., and C. Watson. 1997. The rat brain in stereotaxic coordinates. Academic Press, New York, NY.
43. Scharfman, H. E. 1994. Evidence from simultaneous intracellular recordings in rat hippocampal slices that area CA3 pyramidal cells innervate dentate hilar mossy cells. J. Neurophysiol. 72: 2167–2180.
44. Segal, M., G. Richter-Levin, and N. Maggio. 2010. Stress-induced dynamic routing of hippocampal connectivity: a hypothesis. Hippocampus 20: 1332–1338.
45. Shors, T. J., and R. F. Thompson. 1992. Acute stress impairs (or induces) synaptic long-term potentiation (LTP) but does not affect paired-pulse facilitation in the stratum radiatum of rat hippocampus. Synapse 11: 262–265.
46. van Strien, N. M., N. L. Cappaert, and M. P. Witter. 2009. The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 10: 272–282.
47. Vouimba, R. M., D. Yaniv, D. Diamond, and G. Richter-Levin. 2004. Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. Eur. J. Neurosci. 19: 1887–1894.
48. Whitlock, J. R., A. J. Heynen, M. G. Shuler, and M. F. Bear. 2006. Learning induces long-term potentiation in the hippocampus. Science 313: 1093–1097.
49. Witter, M. P. 2007. Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. Learn. Mem. 14: 705–713.
50. Wong, T. P., J. G. Howland, J. M. Robillard, Y. Ge, W. Yu, A. K. Titterness, et al. 2007. Hippocampal long-term depression mediates acute stress-induced spatial memory retrieval impairment. Proc. Natl. Acad. Sci. USA 104: 11471–11476.
51. Xu, L., R. Anwyl, and M. J. Rowan. 1997. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387: 497–500.
52. Xu, L., C. Holscher, R. Anwyl, and M. J. Rowan. 1998. Glucocorticoid receptor and protein/RNA synthesis-dependent mechanisms underlie the control of synaptic plasticity by stress. Proc. Natl. Acad. Sci. USA 95: 3204–3208.
53. Yaniv, D., R. M. Vouimba, D. M. Diamond, and G. Richter-Levin. 2003. Simultaneous induction of long-term potentiation in the hippocampus and the amygdala by entorhinal cortex activation: mechanistic and temporal profiles. Neuroscience 120: 1125–1135.