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Spatial memory impairment in Morris water maze after electroconvulsive seizures

  • Maria Svensson (a1), Thord Hallin (a1), Jonas Broms (a1), Joakim Ekstrand (a1) and Anders Tingström (a1)...

Abstract

Objective

Electroconvulsive therapy (ECT) is one of the most efficient treatments for severe major depression, but some patients suffer from retrograde memory loss after treatment. Electroconvulsive seizures (ECS), an animal model of ECT, have repeatedly been shown to increase hippocampal neurogenesis, and multiple ECS treatments cause retrograde amnesia in hippocampus-dependent memory tasks. Since recent studies propose that addition of newborn hippocampal neurons might degrade existing memories, we investigated whether the memory impairment after multiple ECS treatments is a cumulative effect of repeated treatments, or if it is the result of a delayed effect after a single ECS.

Methods

We used the hippocampus-dependent memory task Morris water maze (MWM) to evaluate spatial memory. Rats were exposed to an 8-day training paradigm before receiving either a single ECS or sham treatment and tested in the MWM 24 h, 72 h, or 7 days after this treatment, or multiple (four) ECS or sham treatments and tested 7 days after the first treatment.

Results

A single ECS treatment was not sufficient to cause retrograde amnesia whereas multiple ECS treatments strongly disrupted spatial memory in the MWM.

Conclusion

The retrograde amnesia after multiple ECS is a cumulative effect of repeated treatments rather than a delayed effect after a single ECS.

Copyright

Corresponding author

*Prof. Anders Tingström, Psychiatric Neuromodulation Unit (PNU), Department of Clinical Sciences, Lund, Lund University, BMC D11, Klinikgatan 30, 222 42, Lund, Sweden. Tel: +46 46 222 06 11; Fax: +46 46 222 84 39; E-mail: anders.tingstrom@med.lu.se

References

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1. Pagnin, D, de Queiroz, V, Pini, S, Cassano, GB. Efficacy of ECT in depression: a meta-analytic review. J ECT 2004;20:1320.
2. American Psychiatric Association. Practice guideline for the treatment of patients with major depressive disorder, 3rd edn. American Psychiatric Association, The American Journal of Psychiatry, 2010.
3. Semkovska, M, McLoughlin, DM. Objective cognitive performance associated with electroconvulsive therapy for depression: a systematic review and meta-analysis. Biol Psychiatry 2010;68:568577.
4. Lisanby, SH, Maddox, JH, Prudic, J, Devanand, DP, Sackeim, HA. The effects of electroconvulsive therapy on memory of autobiographical and public events. Arch Gen Psychiatry 2000;57:581590.
5. Meeter, M, Murre, JMJ, Janssen, SMJ, Birkenhager, T, van den Broek, WW. Retrograde amnesia after electroconvulsive therapy: a temporary effect? J Affect Disord 2011;132:216222.
6. Fink, M. Convulsive therapy: a review of the first 55 years. J Affect Disord 2001;63:115.
7. Kyeremanteng, C, MacKay, JC, James, JS et al. Effects of electroconvulsive seizures on depression-related behavior, memory and neurochemical changes in Wistar and Wistar-Kyoto rats. Prog Neuropsychopharmacol Biol Psychiatry 2014;54:170178.
8. Madsen, TM, Treschow, A, Bengzon, J, Bolwig, TG, Lindvall, O, Tingström, A. Increased neurogenesis in a model of electroconvulsive therapy. Biol Psychiatry 2000;47:10431049.
9. Malberg, JE, Eisch, AJ, Nestler, EJ, Duman, RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000;20:91049110.
10. Scott, BW, Wojtowicz, JM, Burnham, WM. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 2000;165:231236.
11. Bolwig, TG. How does electroconvulsive therapy work? Theories on its mechanism. Can J Psychiatry 2011;56:1318.
12. Santarelli, L, Saxe, M, Gross, C et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003;301:805809.
13. Perera, TD, Dwork, AJ, Keegan, KA et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS One 2011;6:e17600.
14. Schloesser, RJ, Orvoen, S, Jimenez, DV et al. Antidepressant-like effects of electroconvulsive seizures require adult neurogenesis in a neuroendocrine model of depression. Brain Stimul 2015;8:862867.
15. Clelland, CD, Choi, M, Romberg, C et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009;325:210213.
16. Sahay, A, Scobie, KN, Hill, AS et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011;472:466470.
17. Nakashiba, T, Cushman, JD, Pelkey, KA et al. Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 2012;149:188201.
18. Snyder, JS, Hong, NS, McDonald, RJ, Wojtowicz, JM. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005;130:843852.
19. Deng, W, Saxe, MD, Gallina, IS, Gage, FH. Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci 2009;29:1353213542.
20. Ben Abdallah, NM-B, Filipkowski, RK, Pruschy, M et al. Impaired long-term memory retention: common denominator for acutely or genetically reduced hippocampal neurogenesis in adult mice. Behav Brain Res 2013;252:275286.
21. Burghardt, NS, Park, EH, Hen, R, Fenton, AA. Adult‐born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 2012;22:17951808.
22. Swan, AA, Clutton, JE, Chary, PK, Cook, SG, Liu, GG, Drew, MR. Characterization of the role of adult neurogenesis in touch‐screen discrimination learning. Hippocampus 2014;24:15811591.
23. Yasuda, M, Johnson-Venkatesh, EM, Zhang, H, Parent, JM, Sutton, MA, Umemori, H. Multiple forms of activity-dependent competition refine hippocampal circuits in vivo. Neuron 2011;70:11281142.
24. Frankland, PW, Köhler, S, Josselyn, SA. Hippocampal neurogenesis and forgetting. Trends Neurosci 2013;36:497503.
25. Akers, KG, Martinez-Canabal, A, Restivo, L et al. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 2014;344:598602.
26. Morris, R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984;11:4760.
27. Maei, HR, Zaslavsky, K, Teixeira, CM, Frankland, PW. What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 2009;3:4.
28. Jansson, L, Wennström, M, Johanson, A, Tingström, A. Glial cell activation in response to electroconvulsive seizures. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:11191128.
29. Svensson, M, Grahm, M, Ekstrand, J, Movahed-Rad, P, Johansson, M, Tingström, A. Effect of electroconvulsive seizures on pattern separation. Hippocampus 2015;25:13511360.
30. Andrade, C, Suresh, S, Krishnan, J, Venkataraman, BV. Effects of stimulus parameters on seizure duration and ECS-induced retrograde amnesia. J ECT 2002;18:3137.
31. Svensson, M, Grahm, M, Ekstrand, J, Höglund, P, Johansson, M, Tingström, A. Effect of electroconvulsive seizures on cognitive flexibility. Hippocampus 2016, doi:10.1002/hipo.22573. [Epub ahead of print].
32. Sackeim, HA, Decina, P, Portnoy, S, Neeley, P, Malitz, S. Studies of dosage, seizure threshold, and seizure duration in ECT. Biol Psychiatry 1987;22:249268.
33. Sackeim, HA, Devanand, DP, Prudic, J. Stimulus intensity, seizure threshold, and seizure duration: impact on the efficacy and safety of electroconvulsive therapy. Psychiatr Clin North Am 1991;14:803843.
34. Miller, AL, Faber, RA, Hatch, JP, Alexander, HE. Factors affecting amnesia, seizure duration, and efficacy in ECT. Am J Psychiatry 1985;142:692696.
35. Vaidya, VA, Siuciak, JA, Du, F, Duman, RS. Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures. Neuroscience 1999;89:157166.
36. Gregory-Roberts, EM, Naismith, SL, Cullen, KM, Hickie, IB. Electroconvulsive therapy-induced persistent retrograde amnesia: could it be minimised by ketamine or other pharmacological approaches? J Affect Disord 2010;126:3945.
37. Krystal, AD, Weiner, RD, Dean, MD et al. Comparison of seizure duration, ictal EEG, and cognitive effects of ketamine and methohexital anesthesia with ECT. J Neuropsychiatry Clin Neurosci 2003;15:2734.
38. McDaniel, WW, Sahota, AK, Vyas, BV, Laguerta, N, Hategan, L, Oswald, J. Ketamine appears associated with better word recall than etomidate after a course of 6 electroconvulsive therapies. J ECT 2006;22:103106.
39. Berman, RM, Cappiello, A, Anand, A et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000;47:351354.
40. Chen, AC, Shin, KH, Duman, RS, Sanacora, G. ECS-Induced mossy fiber sprouting and BDNF expression are attenuated by ketamine pretreatment. J ECT 2001;17:2732.
41. Meltzer, LA, Yabaluri, R, Deisseroth, K. A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 2005;28:653660.
42. Tanti, A, Belzung, C. Hippocampal neurogenesis: a biomarker for depression or antidepressant effects? Methodological considerations and perspectives for future research. Cell Tissue Res 2013;354:203219.
43. Zhao, C, Warner-Schmidt, J, Duman, RS, Gage, FH. Electroconvulsive seizure promotes spine maturation in newborn dentate granule cells in adult rat. Dev Neurobiol 2012;72:937942.
44. Yanpallewar, SU, Barrick, CA, Palko, ME, Fulgenzi, G, Tessarollo, L. Tamalin is a critical mediator of electroconvulsive shock-induced adult neuroplasticity. J Neurosci 2012;32:22522262.
45. Chen, F, Madsen, TM, Wegener, G, Nyengaard, JR. Repeated electroconvulsive seizures increase the total number of synapses in adult male rat hippocampus. Eur Neuropsychopharmacol 2009;19:329338.
46. Nordgren, M, Karlsson, T, Svensson, M et al. Orchestrated regulation of nogo receptors, lotus, AMPA receptors and BDNF in an ECT model suggests opening and closure of a window of synaptic plasticity. PLoS One 2013;8:e78778.
47. Phillips, RG, LeDoux, JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274285.
48. Andrade, C, Thyagarajan, S, Vinod, PS, Srikanth, SN, Rao, NSK, Chandra, JS. Effect of stimulus intensity and number of treatments on ECS-related seizure duration and retrograde amnesia in rats. J ECT 2002;18:197202.
49. Lerer, B, Stanley, M, Keegan, M, Altman, H. Proactive and retroactive effects of repeated electroconvulsive shock on passive avoidance retention in rats. Physiol Behav 1986;36:471475.
50. Alberini, CM, Milekic, MH, Tronel, S. Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 2006;63:9991008.
51. Kroes, MCW, Tendolkar, I, van Wingen, GA, van Waarde, JA, Strange, BA, Fernández, G. An electroconvulsive therapy procedure impairs reconsolidation of episodic memories in humans. Nat Neurosci 2014;17:204206.
52. Misanin, JR, Miller, RR, Lewis, DJ. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 1968;160:554555.
53. Lewis, DJ, Bregman, NJ, Mahan, JJ. Cue-dependent amnesia in rats. J Comp Physiol Psychol 1972;81:243247.

Keywords

Spatial memory impairment in Morris water maze after electroconvulsive seizures

  • Maria Svensson (a1), Thord Hallin (a1), Jonas Broms (a1), Joakim Ekstrand (a1) and Anders Tingström (a1)...

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