Skip to main content
SpringerLink
Log in

Long-term potentiation in the hippocampus in conditions of inhibition of caspase-3: Analysis of facilitation in paired-pulse stimulation

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Abstract

Treatment of hippocampal slices with the caspase-3 inhibitor Z-DEVD-FMK led to a decrease in the magnitude of long-term potentiation (LTP), which developed over time. Testing with paired stimuli separated by an interval of 70 msec showed that after caspase-3 inhibition, as compared with control slices, the second response in the pair showed no increase in amplitude in conditions of LTP. In these conditions, the magnitude of LTP depended on differences in the amplitudes of the first and second responses before induction of LTP. LTP was absent in slices with initially highly efficient afferent stimulation and correspondingly low levels of facilitation in paired-pulse stimulation. It is suggested that inhibition of caspase-3 prevents the structural rearrangements in LTP associated with the involvement of new synapses and neurons in the response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. N. V. Gulyaeva, “Non-apoptotic functions of caspase-3 in nervous tissue,” Biokhimiya, 68, No. 11, 1459–1470 (2003).

    Google Scholar 

  2. I. E. Kudryashov, A. A. Yakovlev, I. V. Kudryashova, and N. V. Gulyaeva, “Inhibition of caspase-3 blocks long-term potentiation in hippocampal slices,” Zh. Vyssh. Nerv. Deyat., 53, No. 5, 537–540 (2003).

    CAS  Google Scholar 

  3. V. V. Sherstnev, M. A. Gruden’, Z. I. Storozheva, and A. T. Proshin, “Heterochronous involvement of neurotrophic factors in the neurochemical organization of learning and memory processes in the mature organism,” Ros. Fiziol. Zh. im. I. M. Sechenova, 87, No. 6, 752–761 (2001).

    CAS  Google Scholar 

  4. N. Agnihotry, J. C. Lopez-Garcia, R. D. Hawkins, and O. Arancio, “Morphological changes associated with long-term potentiation,” Histol. Histopathol., 13, No. 4, 1155–1162 (1998).

    Google Scholar 

  5. R. Anwyl, D. Mulkeen, and M. J. Rowen, “The role of N-methyl-D-aspartate receptors in the generation of short-term potentiation in the rat hippocampus,” Brain Res., 503, No. 1, 148–151 (1989).

    Article  PubMed  CAS  Google Scholar 

  6. F. Asztely, M. Y. Xiao, and B. Gustafsson, “Long-term potentiation and paired-pulse facilitation in the hippocampal CA1 region,” Neuroreport, 7, No. 10, 1609–1612 (1996).

    PubMed  CAS  Google Scholar 

  7. T. Bonhoeffer and R. Yuste, “Spine motility. Phenomenology, mechanisms, and function,” Neuron, 35, No. 6, 1019–1027 (2001).

    Article  Google Scholar 

  8. S. Chang and P. De Camilli, “Glutamate regulates actin-based motility in axonal filopodia,” Nat. Neurosci., 4, No. 8, 787–793 (2001).

    Article  PubMed  CAS  Google Scholar 

  9. R. Creager, T. Dunwiddie, and G. Lynch, “Paired pulse and frequency facilitation in the CA1 region of the in vitro rat hippocampus,” J. Physiol. (London), 299, 409–424 (1980).

    CAS  Google Scholar 

  10. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi, “Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo, ” Neuron, 38, No. 3, 447–460 (2003).

    Article  PubMed  CAS  Google Scholar 

  11. C. P. Gilman and M. P. Mattson, “Do apoptotic mechanisms regulate synaptic plasticity and growth cone motility?” Neuromolecular Med., 2, No. 2, 197–214 (2002).

    Article  PubMed  CAS  Google Scholar 

  12. W. Gottschalk, L. D. Pozzo-Miller, A. Figurov, and B. Lu, “Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus,” J. Neurosci., 18, No. 17, 6830–6839 (1998).

    PubMed  CAS  Google Scholar 

  13. N. V. Gulyaeva, “’Apoptotic’ mechanisms in normal brain plasticity: caspase-3 and long-term-potentiation,” Zh. Vyssh. Nerv. Deyat., 54, No. 3, 472–482 (2004).

    Google Scholar 

  14. N. V. Gulyaeva, I. E. Kudryashov, and I. V. Kudryashova, “Caspase activity is essential for long-term potentiation,” J Neurosci. Res., 73, 853–864 (2003).

    Article  PubMed  CAS  Google Scholar 

  15. H. Hama, C. Hara, K. Yamaguchi, and A. Miyawaki, “PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes,” Neuron, 41, No. 3, 405–415 (2004).

    Article  PubMed  CAS  Google Scholar 

  16. A. S. Harris and J. S. Morrow, “Proteolytic processing of human brain alpha spectrin (fodrin): identification of a hypersensitive site,” J. Neurosci., 8, 2640–2651 (1988).

    PubMed  CAS  Google Scholar 

  17. Y. Izaki, M. Takita, M. Nomura, and T. Akema, “Differences between paired-pulse facilitation and long-term potentiation in the dorsal and ventral hippocampal CAl-prefrontal pathways of rats,” Brain Res., 992, No. 1, 142–145 (2003).

    Article  PubMed  CAS  Google Scholar 

  18. R. U. Janicke, P. Ng, M. L. Sprengart, and A. G. Porter, “Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis,” J. Biol. Chem., 273, 15540–15545 (1998).

    Google Scholar 

  19. T. Katafuchi, A.-J. Li, S. Hirota, Y. Mitamura, and T. Hori, xxx201CxImpairment of spatial learning and “hippocampal synaptic potentiation in c-kit mutant rats,” Ken. Mem., 7, No. 6, 383–392 (2000).

    CAS  Google Scholar 

  20. T. Krucker, G. R. Siggins, and S. Halpain, “Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus,” Proc. Natl. Acad. Sci. USA, 97, No. 12, 6856–6861 (2000).

    Article  PubMed  CAS  Google Scholar 

  21. U. Kuhnt and L. Voronin, “Interaction between paired-pulse facilitation and long-term potentiation in area CA1 of guinea pig hippocampal slices: application of quantal analysis,” Neurosci., 62, 391–397 (1994).

    Article  CAS  Google Scholar 

  22. V. Lessman, K. Gottman, and M. Malcangio, “Neurotrophin secretion: current facts and future prospects,” Prog. Neurobiol., 69, No. 5, 341–374 (2003).

    Article  CAS  Google Scholar 

  23. J. E. Lisman and A. M. Zhabotinsky, “A model of synaptic memory: a Ca MKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly,” Neuron, 31, No. 2, 191–201 (2001).

    Article  PubMed  CAS  Google Scholar 

  24. J. Lisman, “Actin’s actions in LTP-induced synapse growth,” Neuron, 39, No. 3, 361–362 (2003).

    Article  Google Scholar 

  25. D. C. Lo, “Neurotrophic factors and synaptic plasticity,” Neuron, 15, 979–998 (1995).

    Article  PubMed  CAS  Google Scholar 

  26. B. Lu and A. Figurov, “Role of neurotrophins in synapse development and plasticity,” Rev. Neurosci., 8, 1–12 (1997).

    PubMed  CAS  Google Scholar 

  27. G. Lynch and M. Baudry, “Brain spectrin, calpain and long-term changes in synaptic efficacy,” Brain Res. Bull., 18, 809–815 (1987).

    Article  PubMed  CAS  Google Scholar 

  28. G. Lynch, “Memory and the brain: Unexpected chemistries and a new pharmacology,” Neurobiol. Learn. Mem., 70, 82–100 (1998).

    Article  PubMed  CAS  Google Scholar 

  29. T. Manabe, D. J. A. Wyllie, D. J. Perkel, and R. A. Nicoll, “Modulation of synaptic transmission and long-term potentiation: effect on paired-pulse facilitation and EPSC variance in the CA1 region of the hippocampus,” J. Neurophysiol., 70, 1451–1459 (1993).

    PubMed  CAS  Google Scholar 

  30. D. F. Marrone and T. L. Petit, “The role of synaptic morphology in neural plasticity: structural interactions underlying synaptic power,” Brain Res. Rev., 38, No. 3, 291–308 (2002).

    Article  PubMed  Google Scholar 

  31. K. Maruki, Y. Izaki, M. Nomura, and T. Yamauchi, “Differences in paired-pulse facilitation and long-term potentiation between dorsal and ventral CA1 regions in anesthetized rats,” Hippocampus, 11, No. 6, 655–661 (2001).

    Article  PubMed  CAS  Google Scholar 

  32. M. P. Mattson and W. Duan, “’Apoptotic’ biochemical cascades in synaptic compartments: roles in adaptive plasticity and neurodegenerative disorders,” J. Neurosci. Res., 58, 152–166 (1999).

    Article  PubMed  CAS  Google Scholar 

  33. A. K. McAlister, L. C. Katz, and D. C. Lo, “Neurotrophin regulation of cortical dendritic growth requires activity,” Neuron, 17, 1057–1064 (1996).

    Article  Google Scholar 

  34. J. Meier, J. Akyeli, S. Kirischuk, and R. Grantyn, “GABA(A) receptor activity and PKC control inhibitory synaptogenesis in CNS tissue slices,” Mol. Cell. Neurosci., 23, No. 4, 600–613 (2003).

    Article  PubMed  CAS  Google Scholar 

  35. D. Muller and G. Lynch, “Evidence that changes in presynaptic calcium currents are not responsible for long-term potentiation in hippocampus,” Brain Res., 479, No. 2, 290–299 (1989).

    Article  PubMed  CAS  Google Scholar 

  36. D. Muller, N. Toni, and P. A. Buchs, “Spine changes associated with long-term potentiation,” Hippocampus, 10, No. 5, 596–604 (2000).

    Article  PubMed  CAS  Google Scholar 

  37. D. Muller, I. Nikonenko, P. Jourdain, and S. Alberi, “LTP, memory and structural plasticity,” Curr. Mol. Med., 2, No. 7, 605–611 (2002).

    Article  PubMed  CAS  Google Scholar 

  38. S. Narkilahti, J. Nissinen, and A. Pitkanen, “Administration of caspase 3 inhibitor during and after status epilepticus in rat: effect on neuronal damage and epileptogenesis,” Neuropharmacology, 44, No. 8, 1068–1088 (2003).

    Article  PubMed  CAS  Google Scholar 

  39. R. B. Nelson, D. J. Linden, C. Hyman, K. H. Pfenninger, and A. Routtenberg, “The two major phosphoproteins in growth cones are probably identical to two protein kinase C substrates correlated with persistence of long-term potentiation,” J. Neurosci., 9, No. 2, 381–389 (1989).

    PubMed  CAS  Google Scholar 

  40. S. L. Patterson, L. M. Grover, P. A. Schwartzkroin, and M. Bothwell, “Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs,” Neuron, 9, No. 6, 1081–1088 (1992).

    Article  PubMed  CAS  Google Scholar 

  41. S. L. Patterson, T. Abel, T. A. Deuel, K. C. Martin, J. C. Rose, and E. R. Kandel, “Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knock-out mice,” Neuron, 16, 1137–1145 (1996).

    Article  PubMed  CAS  Google Scholar 

  42. K. Pfenninger, B. A. de la Houssaye, S. M. Helmke, and S. Quiroga, “Growth-regulated proteins and neuronal plasticity. A commentary,” Mol. Neurobiol., 5, No. 2–4, 143–151 (1991).

    Article  PubMed  CAS  Google Scholar 

  43. P. E. Schultz, E. P. Cook, and D. Johnston, “Changes in paired-pulse facilitation suggests pre-synaptic involvement in long-term potentiation,” J. Neurosci., 14, 5325–5337 (1994).

    Google Scholar 

  44. P. E. Schultz, “Long-term potentiation involves increases in the probability of neurotransmitter release,” Proc. Natl. Acad. Sci. USA, 94, 5888–5893 (1997).

    Article  Google Scholar 

  45. M. Segal and P. Andersen, “Dendritic spines shaped by synaptic activity,” Curr. Opin. Neurobiol., 10, No. 5, 582–586 (2000).

    Article  PubMed  CAS  Google Scholar 

  46. Y. Shinoda, K. Tominaga-Yoshino, and A. Ogura, “The dendritic layer-specific persistent enhancement of synaptic transmission induced by repetitive activation of protein kinase A,” Neurosci. Res., 47, No. 2, 191–200 (2003).

    Article  PubMed  CAS  Google Scholar 

  47. A. Tashiro, A. Dunaevsky, R. Blazeski, C. A. Mason, and R. Yuster, “Bidirectional regulation of hippocampal mossy fiber filopodial motility by kainite receptors: a two-step model of synaptogenesis,” Neuron, 38, No. 5, 773–784 (2003).

    Article  PubMed  CAS  Google Scholar 

  48. H. Thoenen, “Neurotrophins and neuronal plasticity,” Science, 270, 593–596 (1995).

    PubMed  CAS  Google Scholar 

  49. Y. Tomimatsu, S. Idemotoa, S. Mariguchia, S. Watanabe, and H. Nakanishia, “Proteases involved in long-term potentiation,” Life Sci., 72, 355–361 (2002).

    Article  PubMed  CAS  Google Scholar 

  50. K. Tominaga-Yoshino, S. Kondo, S. Tomotsu, and A. Ogura, “Repetitive activation of protein kinase A induces slow and persistent potentiation associated with synaptogenesis in cultured hippocampus,” Neurosci. Res., 44, No. 4, 357–367 (2002).

    Article  PubMed  CAS  Google Scholar 

  51. N. Toni, P. A. Puchs, I. Nokonenko, C. R. Bron, and D. Muller, “LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite,” Nature, 402, No. 6760, 421–425 (1999).

    Article  PubMed  CAS  Google Scholar 

  52. M. Volgushev, L. L. Voronin, M. Chistiakova, and W. Singer, “Relations between long-term synaptic modifications and paired-pulse interactions in the rat neocortex,” Eur. J. Neurosci., 9, 1656–1665 (1997).

    Article  PubMed  CAS  Google Scholar 

  53. J. H. Wang and P. T. Kelly, “Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms,” J. Neurophysiol., 78, 2707–2716 (1997).

    PubMed  CAS  Google Scholar 

  54. K. K. Wang, R. Posmantur, R. Nadimpalli, R. Nath, P. Mohan, R. A. Nixon, R. V. Talanian, M. Keegan, L. Herzog, and H. Allen, “Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis,” Arch. Biochem. Biophys., 356, 187–196 (1998).

    Article  PubMed  CAS  Google Scholar 

  55. R. Yuste and T. Bonhoeffer, “Morphological changes in dendritic spines associated with long-term synaptic plasticity,” Ann. Rev. Neurosci., 24, 1071–1089 (2001).

    Article  PubMed  CAS  Google Scholar 

  56. J. Zhou, F. Zhang, and Y. Zhang, “Corticosterone inhibits generation of long-term potentiation in rat hippocampal slice: involvement of brain-derived neurotrophic factor,” Brain Res., 885, No. 2, 182–191 (2000).

    Article  PubMed  CAS  Google Scholar 

  57. R. S. Zucker, “Short-term synaptic plasticity,” Ann. Rev. Neurosci., 12, 13–31 (1989).

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, 5a Butlerov Street, 117485, Moscow, Russia

    I. V. Kudryashova, I. E. Kudryashov & N. V. Gulyaeva

Authors
  1. I. V. Kudryashova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. I. E. Kudryashov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. V. Gulyaeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

__________

Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 91, No. 8, pp. 915–926 August, 2005.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kudryashova, I.V., Kudryashov, I.E. & Gulyaeva, N.V. Long-term potentiation in the hippocampus in conditions of inhibition of caspase-3: Analysis of facilitation in paired-pulse stimulation. Neurosci Behav Physiol 36, 817–824 (2006). https://doi.org/10.1007/s11055-006-0092-y

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11055-006-0092-y

Key words

Search

Navigation