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Spatial memory impairment in Morris water maze after electroconvulsive seizures

Published online by Cambridge University Press:  03 May 2016

Maria Svensson
Affiliation:
Department of Clinical Sciences Lund, Psychiatric Neuromodulation Unit, Lund University, Lund, Sweden
Thord Hallin
Affiliation:
Department of Clinical Sciences Lund, Psychiatric Neuromodulation Unit, Lund University, Lund, Sweden
Jonas Broms
Affiliation:
Department of Clinical Sciences Lund, Psychiatric Neuromodulation Unit, Lund University, Lund, Sweden
Joakim Ekstrand
Affiliation:
Department of Clinical Sciences Lund, Psychiatric Neuromodulation Unit, Lund University, Lund, Sweden
Anders Tingström*
Affiliation:
Department of Clinical Sciences Lund, Psychiatric Neuromodulation Unit, Lund University, Lund, Sweden
*
*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: [email protected]

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.

Type
Original Articles
Copyright
© Scandinavian College of Neuropsychopharmacology 2016 

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References

1. Pagnin, D, de Queiroz, V, Pini, S, Cassano, GB. Efficacy of ECT in depression: a meta-analytic review. J ECT 2004;20:1320.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
6. Fink, M. Convulsive therapy: a review of the first 55 years. J Affect Disord 2001;63:115.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
9. Malberg, JE, Eisch, AJ, Nestler, EJ, Duman, RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 2000;20:91049110.CrossRefGoogle ScholarPubMed
10. Scott, BW, Wojtowicz, JM, Burnham, WM. Neurogenesis in the dentate gyrus of the rat following electroconvulsive shock seizures. Exp Neurol 2000;165:231236.CrossRefGoogle ScholarPubMed
11. Bolwig, TG. How does electroconvulsive therapy work? Theories on its mechanism. Can J Psychiatry 2011;56:1318.CrossRefGoogle ScholarPubMed
12. Santarelli, L, Saxe, M, Gross, C et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003;301:805809.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
15. Clelland, CD, Choi, M, Romberg, C et al. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 2009;325:210213.CrossRefGoogle ScholarPubMed
16. Sahay, A, Scobie, KN, Hill, AS et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011;472:466470.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
18. Snyder, JS, Hong, NS, McDonald, RJ, Wojtowicz, JM. A role for adult neurogenesis in spatial long-term memory. Neuroscience 2005;130:843852.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
21. Burghardt, NS, Park, EH, Hen, R, Fenton, AA. Adult‐born hippocampal neurons promote cognitive flexibility in mice. Hippocampus 2012;22:17951808.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
24. Frankland, PW, Köhler, S, Josselyn, SA. Hippocampal neurogenesis and forgetting. Trends Neurosci 2013;36:497503.CrossRefGoogle ScholarPubMed
25. Akers, KG, Martinez-Canabal, A, Restivo, L et al. Hippocampal neurogenesis regulates forgetting during adulthood and infancy. Science 2014;344:598602.CrossRefGoogle ScholarPubMed
26. Morris, R. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 1984;11:4760.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
28. Jansson, L, Wennström, M, Johanson, A, Tingström, A. Glial cell activation in response to electroconvulsive seizures. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:11191128.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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].CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
34. Miller, AL, Faber, RA, Hatch, JP, Alexander, HE. Factors affecting amnesia, seizure duration, and efficacy in ECT. Am J Psychiatry 1985;142:692696.Google ScholarPubMed
35. Vaidya, VA, Siuciak, JA, Du, F, Duman, RS. Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures. Neuroscience 1999;89:157166.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
39. Berman, RM, Cappiello, A, Anand, A et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000;47:351354.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
41. Meltzer, LA, Yabaluri, R, Deisseroth, K. A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 2005;28:653660.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
47. Phillips, RG, LeDoux, JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992;106:274285.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
50. Alberini, CM, Milekic, MH, Tronel, S. Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 2006;63:9991008.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
52. Misanin, JR, Miller, RR, Lewis, DJ. Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace. Science 1968;160:554555.CrossRefGoogle ScholarPubMed
53. Lewis, DJ, Bregman, NJ, Mahan, JJ. Cue-dependent amnesia in rats. J Comp Physiol Psychol 1972;81:243247.CrossRefGoogle ScholarPubMed