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Effects of Kindling on Spatial Memory

Characteristics and mechanisms

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Kindling 6

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 55))

Abstract

Epilepsy is a chronic disorder defined by the recurrence of spontaneous seizures affecting ∼2% of the population in North America.1 There are a variety of distinct subtypes of the disorder with the most common, temporal lobe epilepsy (TLE), accounting for about 55% of all cases.1, 2 While the seizures themselves can be significantly debilitating, the clinical impact of TLE is exacerbated by the fact that about half of all sufferers exhibit serious disturbances of affect and/or memory function.36 At present, the mechanisms of these TLE-associated psychological impairments are unknown and, although recent studies have begun to explore the potential effectiveness of behavioral interventions,7,8 there is no treatment currently available. Consequently, these problems are often neglected clinically and have a significant adverse effect on patient quality of life.9 There is a clear need, then, for research to provide a better understanding of the bases for epilepsy-associated psychological disturbances and to develop effective treatment strategies. Clinical studies, however, are challenging because of the large number of potentially relevant but difficult to control variables. Thus, progress relies heavily on work with suitable animal models. The present chapter reviews studies on one such model — kindling in rats, and describes characteristics of spatial memory changes in this model, their relation to kindling-related variables, and potential mediating mechanisms.

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3. References

  1. W.A. Hauser, J.F. Annegers, and L.T. Kurland, Prevalence of epilepsy in Rochester, Minnesota: 1940–1980, Epilepsia 32, 429–45 (1991).

    Article  PubMed  CAS  Google Scholar 

  2. O. Devinsky, Interictal behavioral changes in epilepsy, in: Epilepsy and Behavior, edited by O. Devinsky and W. H. Theodore (New York; Wiley-Liss, 1991) pp. 1–21.

    Google Scholar 

  3. O. Devinsky, Therapy for neurobehavioral disorders in epilepsy, Epilepsia 45(Suppl 2), 34–40 (1994).

    Google Scholar 

  4. F. Gilliam, H. Hecimovic, and Y. Sheline, Psychiatric comorbidity, health, and function in epilepsy, Epilepsy Res, 4(Suppl 4), S26–30 (2003).

    Google Scholar 

  5. B.P. Hermann, M. Seidenberg, J. Schoenfeld, and K. Davies, Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy, Arch. Neurol. 54, 369–376 (1997).

    PubMed  CAS  Google Scholar 

  6. B. Pedersen and M. Dam, Memory disturbances in epileptic patients, Acta Neurol. Scand. 74(suppl. 109), 11–14 (1986).

    Google Scholar 

  7. A. Gupta and T. Naorem, Cognitive retraining in epilepsy, Brain Inj. 17, 161–74 (2003).

    Article  PubMed  Google Scholar 

  8. P. Moore and G. Baker, The neuropsychological and emoptional consequences of living with intractable temporal lobe epilepsy: implications for clinical management, Seizure 11, 224–30 (2002).

    Article  PubMed  Google Scholar 

  9. N. H. Engelberts, M. Klein, H. M. van der Ploeg, J. J. Heimans, H. J. Ader, M. P. van Boxtel, J. Jolles, D. G. Kasteleijn-Nolst Trenite, Cognition and health-related quality of life in a well-defined subgroup of patients with partial epilepsy, J. Neurol. 249, 294–9 (2002).

    Article  PubMed  Google Scholar 

  10. K. Perrine and T. Kiolbasa, Cognitive deficits in epilepsy and contribution to psychopathology, Neurology 53, S39–S48 (1999).

    PubMed  CAS  Google Scholar 

  11. J. J. Bortz, Neuropsychiatric and memory issues in epilepsy, Mayo Clinic Proc. 78, 781–7 (2003).

    Google Scholar 

  12. N. Dige and G. Wik, A visual learning and memory test for preoperative evaluation of patients with temporal lobe epilepsy, Int. J. Neurosci. 111, 167–74 (2001).

    Article  PubMed  CAS  Google Scholar 

  13. R. Schwarcz and M. P. Witter, Memory impairment in temporal lobe epilepsy: the role of entorhinal lesions, Epilepsy Res. 50, 161–77 (2002).

    Article  PubMed  Google Scholar 

  14. M. Aikia, R. Kalviainen, and P. J. Riekkinen, Verbal learning and memory in newly diagnosed partial epilepsy, Epilepsy Res. 22, 157–164 (1995).

    Article  PubMed  CAS  Google Scholar 

  15. R.L. Billingsley, M.P. McAndrews, and ML. Smith, Intact perceptual and conceptual priming in temporal lobe epilepsy: neuroanatomical and methodlogical implications, Neuropscyhologia 16, 92–101 (2002).

    Article  Google Scholar 

  16. C. Helmstaedter, Effects of chronic epilepsy on declarative memory systems, Prog. Brain Res. 135, 439–53 (2002).

    Article  PubMed  CAS  Google Scholar 

  17. A. Rahmann, S. Stodieck, I. W. Hustedt, and S. Evers, Pre-attentive cognitive processing in epilepsy. A pilot study on the impact of epilepsy type and anti-epileptic treatment, Eur. Neurol. 48, 146–52 (2002).

    Article  PubMed  Google Scholar 

  18. A.R. Giovagnoli, S. Mascheroni, and G. Avanzini, Self-reporting of everyday memory in patients with epilepsy: relation to neuropsychological, clinical, pathological and treatment factors, Epilepsy Res. 28, 119–128 (1997).

    Article  PubMed  CAS  Google Scholar 

  19. P. J. Thompson and R. Corcoran, Everyday memory failures in people with epilepsy, Epilepsia 33, S18–20 (1992).

    Google Scholar 

  20. A. Grippo, L. Pelosi, V. Mehta, and L. D. Blumhardt, Working memory in temporal lobe epilepsy: an event-related potential study, Eletroencephalogr. Clin. Neurophysiol. 99, 200–213 (1996).

    Article  CAS  Google Scholar 

  21. R. C. Martin, S. Sawrie, J. Hugg, F. Gilliam, E. Faught, and R. Kuzniecky, Cognitive correlates of 1H MRSI-detected hippocampal abnormalities in temporal lobe epilepsy, Neurology 53, 2052–2058 (1999).

    PubMed  CAS  Google Scholar 

  22. S. M. Sawrie, R. C. Martin, R. E. Faught, B. Maton, J. W. Hugg, and R. I. Kuzniecky, Nonlinear trends in hippocampal metabolic function and verbal memory: Evidence of cognitive reserve in temporal lobe epilepsy?, Epilepsy Behav. 1, 106–111 (2000).

    Article  PubMed  Google Scholar 

  23. S. M. Sawrie, R. C. Martin, R. Knowlton, E. Faught, F. Gilliam, and R. Kuzniecky, Relationships among hippocampal volumetry, proton magnetic spectroscopy, and verbal memory in temporal lobe epilepsy, Epilepsia 42, 1403–1407 (2001).

    Article  PubMed  CAS  Google Scholar 

  24. M. E. Corcoran and S. L. Moshé, eds., Kindling 5 (Plenum Press, New York, 1998).

    Google Scholar 

  25. M. Sato, R. J. Racine, and D. C. McIntyre, Kindling: Basic mechanisms and clinical validity, Eletroencephalogr. Clin. Neurophysiol. 76, 459–472 (1990).

    Article  CAS  Google Scholar 

  26. R. Adamec and B. Young, Neuroplasticity in specific limbic system circuits may mediate specific kindling induced changes in animal affect-implications for understanding anxiety associated with epilepsy, Neurosci. Biobehav. Rev. 24, 705–723 (2000).

    Article  PubMed  CAS  Google Scholar 

  27. H. E. Edwards, N. J. MacLusky, and W. M. Burnham, The effect of seizures and kindling on reproductive hormones in the rat, Neurosci. Biobehav. Rev. 24, 753–762 (2000).

    Article  PubMed  CAS  Google Scholar 

  28. D.K. Hannesson and M E. Corcoran, The mnemonic effects of kindling, Neurosci. Biobehav. Rev. 24, 725–751 (2000).

    Article  PubMed  CAS  Google Scholar 

  29. L. E. Kalynchuk, Long-term amygdala kindling in rats as a model for the study of interictal emotionality in temporal lobe epilepsy, Neurosci. Biobehav. Rev. 24, 691–704 (2000).

    Article  PubMed  CAS  Google Scholar 

  30. L. S. Leung, J. Ma, and R. S. McLachlan, Behaviors induced or disrupted by complex partial seizures, Neurosci. Biobehav. Rev. 24, 763–775 (2000).

    Article  PubMed  CAS  Google Scholar 

  31. S. Cammisuli, M. P. Murphy, C. J. Ikeda-Douglas, V. Balkissoon, R. M. D. Holsinger, E. Head, M. Michael, R. J. Racine, and N. W. Milgram, Effects of extended electrical kindling on exploratory behavior and spatial learning, Behav. Brain Res. 89, 179–190 (1997).

    Article  PubMed  CAS  Google Scholar 

  32. K. J. Feasey-Truger, L. Kargl, and G. ten Bruggencate, Differential effects of dentate kindling on working and reference spatial memory in the rat, Neurosci. Lett. 151, 25–28 (1993).

    Article  PubMed  CAS  Google Scholar 

  33. T. H. Gilbert, R. K. McNamara, and M. E. Corcoran, Kindling of hippocampal field CA1 impairs spatial learning and retention in the Morris water maze, Behav. Brain Res. 82, 57–66 (1996).

    Article  PubMed  CAS  Google Scholar 

  34. D. K. Hannesson, J. Howland, M. Pollock, P. Mohapel, A. E. Wallace, and M. E. Corcoran, Dorsal hippocampal kindling produces a selective and enduring disruption of hippocampally mediated behavior, J. Neurosci. 21, 4443–4450 (2001).

    PubMed  CAS  Google Scholar 

  35. D. K. Hannesson, P. Mohapel, and M. E. Corcoran, Kindling of the dorsal hippocampus selectively disrupts spatial learning/short-term memory, Hippocampus 11, 275–286 (2001).

    Article  PubMed  CAS  Google Scholar 

  36. D. K. Hannesson, A. E. Wallace, M. Pollock, S. M. Corley, P. Mohapel, and M. E. Corcoran, The relation between extent of dorsal hippocampal kindling and DMTP performance in the Morris water maze, Epilepsy Res. 58, 145–154 (2004).

    Article  PubMed  CAS  Google Scholar 

  37. L. S. Leung, K. A. Boon, T. Kaibara, and N. K. Innis, Radial maze performance following hippocampal kindling, Behav. Brain Res. 40, 119–129 (1990).

    Article  PubMed  CAS  Google Scholar 

  38. L. S. Leung, D. Brzozowski, and B. Shen, Partial hippocampal kindling affects retention but not acquisition and place but not cue tasks on the radial arm maze, Behav. Neurosci. 110, 1017–1024 (1996).

    Article  PubMed  CAS  Google Scholar 

  39. L. S. Leung and B. Shen, Hippocampal CA1 evoked response and radial 8-arm maze performance after hippocampal kindling, Brain Res. 555, 353–357 (1991).

    Article  PubMed  CAS  Google Scholar 

  40. L. S. Leung, D. Zhao, and B. Shen, Long-lasting effects of partial hippocampal kindling on hippocampal physiology and function, Hippocampus 4, 696–704 (1994).

    Article  PubMed  CAS  Google Scholar 

  41. F. H. Lopes da Silva, J. A. Gorter, and W. J. Wadman, Kindling of the hippocampus induces spatial memory deficits in the rat, Neurosci. Lett. 63, 115–120 (1986).

    Article  PubMed  CAS  Google Scholar 

  42. R. J. Sutherland, L. S. Leung, M. P. Weisend, J. Schlife, and R. J. McDonald, An evaluation of the effect of partial hippocampal kindling on place navigation by rats in the Morris water task, Psychobiology 25, 126–132 (1997).

    Google Scholar 

  43. T. Sutula, S. Lauersdorf, M. Lynch, C. Jurgella, and A. Woodard, Deficits in radial arm maze performance in kindled rats: Evidence for long-lasting memory dysfunction induced by repeated brief seizures, J. Neurosci. 15, 8295–8301 (1995).

    PubMed  CAS  Google Scholar 

  44. J. O’Keefe and L. Nadel, The Hippocampus as a Cognitive Map (Oxford University Press, Oxford, 1978).

    Google Scholar 

  45. R. D’Hooge and P. P. De Deyn, Applications of the Morris water maze in the study of learning and memory. Brain Res. Rev. 36, 60–90 (2001).

    Article  PubMed  CAS  Google Scholar 

  46. K. Nakazawa, T. J. McHugh, M. A. Wilson, and S. Tonegawa, NMDA receptors, place cells and hippocampal spatial memory, Nature Rev. Neurosci. 5, 361–372 (2004).

    Article  CAS  Google Scholar 

  47. M. Shapiro, Plasticity, hippocampal place cells, and cognitive maps, Arch. Neurol. 58, 874–881 (2001).

    Article  PubMed  CAS  Google Scholar 

  48. H. Hodges, Maze procedures: the radial-arm and water maze compared, Cog. Brain Res. 3, 167–181 (1996).

    Article  CAS  Google Scholar 

  49. H. Eichenbaum, The hippocampus and mechanisms of declarative memory, Behav. Brain Res. 103, 123–133 (1999).

    Article  PubMed  CAS  Google Scholar 

  50. M. E. Corcoran, L. L. Armitage, T. H. Gilbert, D. K. Hannesson, and P. Mohapel, Kindling and spatial cognition, in: Kindling 5, edited by M. E. Corcoran and S. L. Moshé, (Plenum Press: New York, 1998), pp 377–393.

    Google Scholar 

  51. G. L. Holmes, A. Chronopoulos, C. E. Stafstrom, M. A. Mikati, S. J. Thurber, P. A. Hyde, and J. L. Thompson, Effects of kindling on subsequent learning, memory, behavior, and seizure susceptibility, Dev. Brain Res. 73, 71–77 (1993).

    Article  CAS  Google Scholar 

  52. R. K. McNamara, R. D. Kirkby, G. E. dePape, and M. E. Corcoran, Limbic seizures, but not kindling, reversibly impair place learning in the Morris water maze, Behav. Brain Res. 50, 167–175 (1992).

    Article  PubMed  CAS  Google Scholar 

  53. S. A. Nieminen, J. Sirvio, K. Teittinen, A. Pitkanen, M. M. Airaksinen, and P. Riekkinen, Amygdala kindling increased fear-response, but did not impair spatial memory in rats, Physiol. Behav. 51, 845–849 (1992).

    Article  PubMed  CAS  Google Scholar 

  54. G. B. Robinson, H. A. McNeill, and G. D. Reed, Comparison of the short-and long-lasting effects of perforant path kindling on radial maze learning, Behav. Neurosci. 107, 988–995 (1993).

    Article  PubMed  CAS  Google Scholar 

  55. R. J. Racine, Modification of seizure activity by electrical stimulation: II. Motor seizure, Eletroencephalogr. Clin. Neurophysiol. 32, 281–294 (1972).

    Article  CAS  Google Scholar 

  56. M. A. Lynch, Long-term potentiation and memory. Physiol, Rev. 84, 87–136 (2004).

    Article  CAS  Google Scholar 

  57. R. G. Morris, E. I. Moser, G. Riedel, S. J. Martin, J. Sandin, M. Day, and C. O’Carroll, Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory, Phil. Trans. Royal Soc. Lond. B Biol. Sci. 358, 773–786 (2003).

    Article  CAS  Google Scholar 

  58. W. C. Abraham and W. P. Tate, Metaplasticity: a new vista across the field of synaptic plasticity, Prog. Neurobiol. 52, 303–323 (1997).

    Article  PubMed  CAS  Google Scholar 

  59. L. S. Leung and C. Wu, Kindling suppresses primed-burst-induced long-term potentiation in hippocampal CA1, NeuroReport 14, 211–214 (2003).

    Google Scholar 

  60. V. Neugebauer, N. B. Keele, and P. Shinnick-Gallagher, Loss of long-lasting potentiation mediated by group III mGluRs in amygdala neurons in kindling-induced epileptogenesis. J. Neurophys. 78, 3475–3478 (1997).

    CAS  Google Scholar 

  61. S. J. Wang and P. W. Gean, Long-term depression of excitatory synaptic transmission in the rat amygdale, J. Neurosci. 19, 10656–10663 (1999).

    PubMed  CAS  Google Scholar 

  62. K. Akiyama, M. Ono, I. Kohira, A. Daigen, T. Ishihara, and S. Kuroda, Long-lasting increase in protein kinase C activity in the hippocampus of amygdala-kindled rat, Brain Res. 679, 212–220 (1995).

    Article  PubMed  CAS  Google Scholar 

  63. J. M. Bronstein, D. B. Farber, and C. G. Wasterlain, Regulation of type-II calmodulin kinase: functional implications, Brain Res. Rev. 18, 135–147 (1993).

    Article  PubMed  CAS  Google Scholar 

  64. B. S. Meldrum, M. T. Akbar, and A. G. Chapman, Glutamate receptors and transporters in genetic and acquired models of epilepsy, Epilepsy Res. 36, 189–204 (1999).

    Article  PubMed  CAS  Google Scholar 

  65. M. Krug, M. Koch, G. Grecksch, and K. Schulzeck, Pentylenetetrazol kindling changes the ability to induce potentiation phenomena in the hippocampal CA1 region, Physiol. Behav. 62, 721–727 (1997).

    Article  PubMed  CAS  Google Scholar 

  66. M. Lynch, U. Sayin, J. Bownds, S. Janumpalli, and T. Sutula, Long-term consequences of early postnatal seizures on hippocampal learning and plasticity, Eur. J. Neurosci. 12, 2252–2264 (2000).

    Article  PubMed  CAS  Google Scholar 

  67. H. Beck, I. V. Goussakov, A. Lie, C. Helmstaedter, and C. E. Elger, Synaptic plasticity in the human dentate gyrus, J. Neurosci., 20, 7080–7086 (2000).

    PubMed  CAS  Google Scholar 

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Hannesson, D.K., Wolfe, K., Corcoran, M.E. (2005). Effects of Kindling on Spatial Memory. In: Corcoran, M.E., Moshé, S.L. (eds) Kindling 6. Advances in Behavioral Biology, vol 55. Springer, Boston, MA. https://doi.org/10.1007/0-387-26144-3_27

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