Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-25T19:40:20.744Z Has data issue: false hasContentIssue false

Kindling and Quenching: Conceptual Links to rTMS

Published online by Cambridge University Press:  07 November 2014

Abstract

Unlike the other articles in this series on rTMS, this paper will not include clinical research or magnetic stimulation experiments. Instead, we will focus on an animal model of epilepsy called kindling and a procedure that we have recently developed to inhibit kindled seizures called quenching. Both procedures involve direct intracerebral electrical stimulation of the brain. We demonstrate that low-frequency stimulation, which does not disrupt ongoing behavior, can have profound and long-lasting effects on both seizure development and fully kindled seizures.

At this point, we do not know how well these models relate, either mechanistically or phenomenologically, to the effects of repeated transcranial magnetic stimulation (rTMS); however, we believe that at the very least, some of the principles emerging from studying these phenomena may be relevant to our thinking about rTMS and its potential treatment utility. Specifically, we discuss the possible relationship between quenching and rTMS with regards to parameters of induction, possible common mechanisms, and potential treatment implications.

Type
Feature Articles
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Goddard, LS, McIntyre, DC, Leech, CK. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol. 1969;25:295330.Google Scholar
2.Racine, R. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32:281294.CrossRefGoogle ScholarPubMed
3.Post, RM. Central stimulants: clinical and experimental evidence on tolerance and sensitization. In: Israel, Y, Glaser, F, Kalant, H, Popham, RE, Schmidt, W, Smart, R, eds. Research Advances in Alcohol and Drug Problems, 6. New York: Plenum Press; 1981:165.Google Scholar
4.Post, RM. Lidocaine kindled limbic seizures: behavioral implications. In: Wada, JA, ed. Kindling 2. New York: Raven Press; 1981:149160.Google Scholar
5.Little, H, Nutt, D, Taylor, S. Selective changes in the in vivo effects of benzodiazepine receptor ligands after chemical kindling with FG 7142. Neuropsychopharm. 1987;26:2531.Google Scholar
6.Cain, DP, Corcoran, ME. Intracerebral beta-endorphin, metenkephalin and morphine: kindling of seizures and handling-induced potentiation of epileptiform effects. Life Sci., 1984;34:25352542.Google Scholar
7.Post, R, Weiss, S. Kindling: implications for the course of treatment of affective disorders. In: Modigh, K, Robak, O, Vestergaard, P, eds. Anticonvulsants in Psychiatry. Hampshire, UK: Wrightson Biomedical; 1994:113137.Google Scholar
8.Post, R, Weiss, S, Smith, M. Sensitization and kindling: implications for the evolving neural substrates of PTSD. In: Friedman, M, Charney, D, Deutch, A, eds. Neuwbiology and Clinical Consequences of Stress from Normal Adaptation to PTSD. New York: Raven Press; 1995:203224.Google Scholar
9.Loscher, W, Fisher, JE, Nau, H, Honack, D. Valproic acid in amygdala-kindled rats: alterations in anticonvulsant efficacy, adverse effects and drug and metabolite levels in various brain regions during chronic treatment. J Pharmacol Exp Ther. 1989;250:10671078.Google Scholar
10.Loscher, W, Honack, D. Anticonvulsant and behavioral effects of 2 novel competitive N-methyl-D-aspartic acid receptor antagonist, CGP 37849 and CGP 39551, in the kindling model of epilepsy. Comparison with MK-801 and carbamazepine. J Pharm Exp Ther. 1991;256:432440.Google Scholar
11.Weiss, SRB, Post, RM. Carbamazepine and carbamazepine-10, 11-epoxide inhibit amygdala-kindled seizures in the rat but do not block their development. Clin Neuropharmacol. 1987;10:272279.Google Scholar
12.Weiss, SRB, Post, RM, Szele, F, Woodward, R, Nierenberg, J. Chronic carbamazepine inhibits the development of local anesthetic seizures kindled by cocaine and lidocaine. Brain Res., 1989;497:7279.Google Scholar
13.Pinel, J. Spontaneous kindled motor seizures in rats. In: Wada, J, ed. Kindling II. New York: Raven Press; 1981.Google Scholar
14.Goddard, GV, Douglas, RM. Does the engram of kindling model the engram of normal long term memory. Can J Neurological Sci. 1975;2:385398.Google Scholar
15.Racine, R. Kindling: the first decade. Neurosurgery. 1978;3:234252.Google Scholar
16.Clark, M, Post, RM, Weiss, SRB, Cain, CJ, Nakajima, T. Regional expression of c-fos mRNA in rat brain during the evolution of amygdala kindled seizures. Mol Brain Res. 1991;11:5564.Google Scholar
17.Hosford, D, Simonato, M, Cao, Z, et al.Differences in anatomic distribution of immediate-early gene expression in amygdala and angular bundle kindling development. J Neurosci. 1995;15:25132523.CrossRefGoogle ScholarPubMed
18.Kraus, JE, Yeh, GC, Bonhaus, DW, Nadler, JV, McNamara, JO. Kindling induces the long-lasting expression of a novel population of NMDA receptors in hippocampal region CA3. Eur J Neurosci. 1994;6:587596.Google Scholar
19.McNamara, J. Analyses of the molecular basis of kindling development. Psychiatry Clin Neurosci. 1995;49:175178.Google Scholar
20.Rosen, JB, Cain, CJ, Weiss, SRB, Post, RM. Alterations in mRNA of enkephalin, dynorphin and thyrotropin releasing hormone during amygdala kindling: an in situ hybridization study. Mol Brain Res. 1992;15:247255.Google Scholar
21.Weiss, SRB, Clark, M, Rosen, JB, Smith, MA, Post, RM. Contingent tolerance to the anticonvulsant effects of carbamazepine: relationship to loss of endogenous adaptive mechanisms. Br Res Rev. 1995;20:305325.CrossRefGoogle Scholar
22.Post, RM, Altschuler, LL, Ketter, T, Denicoff, K, Weiss, SRB. Antiepileptic drugs in affective illness: clinical and theoretical implications. In: Smith, DB, Treiman, DM, Trimble, MR, ed. Advances in Neurology, 55. New York: Raven Press; 1991:239277.Google Scholar
23.Post, RM, Weiss, SRB, Chang, D-M, Ketter, TA. Mechanisms of action of carbamazepine in seizure and affective disorders. In: Joffe, RT, Calabrese, JR, eds. Anticonvulsants in Mood Disorders. New York: Marcel Dekker; 1994:4392.Google Scholar
24.Loscher, W. Development of tolerance to anticonvulsant effects of GABA-mimetic drugs in animal models of seizure states. In: Koella, WP, ed. Tolerance to Beneficial and Adverse Effects of Antiepileptic Drugs. New York: Raven Press; 1986:3747Google Scholar
25.Loscher, W, Schwark, WS. Development of tolerance to the anticonvulsant effect of diazepam in amygdala-kindled rats. Exp Neurology. 1985;90:373384.Google Scholar
26.Mana, MJ, Kim, CK, Pinel, JPJ, Jones, CH. Contingent tolerance to the anticonvulsant effects of carbamazepine, diazepam, and sodium valproate in kindled rats. Pharmacol Biochem Behav. 1992;41:121126.Google Scholar
27.Pinel, JPJ. Mana, MJ, Renfrey, G. Contingent tolerance to the anticonvulsant effects of alcohol. Alcohol. 1985;2:495499.Google Scholar
28.Weiss, SRB, Post, RM. Development and reversal of contingent inefficacy and tolerance to the anticonvulsant effects of carbamazepine. Epilepsia. 1991;32:140145.Google Scholar
29.Bliss, T, Collingridge, A. synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993;361:3139.Google Scholar
30.Bliss, T, Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232:331356.Google Scholar
31.Madison, D, Malenka, R, Nicoll, R. Mechanisms underlying long-term potentiation of synaptic transmission. Ann Rev Neurosci. 1991;14:379397.Google Scholar
32.Barrionuevo, G, Schottler, F, Lynch, G. The effects of repetitive low frequency stimulation on control and potentiated synaptics responses in the hippocampus. Life Sci. 1980;27:23852389.Google Scholar
33.Bashir, ZI, Collingridge, GL. An investigation of depotentiation of long-term potentiation in the Ca1 region of the hippocampus. Exp Br Res. 1994;100:437443.Google Scholar
34.Bear, MF, Malenka, RC. Synaptic plasticity: LTP and LTD. Curr Op in Neurobiol. 1994;4:389399.Google Scholar
35.Christie, BR, Kerr, DS, Abraham, WC. Flip side of synaptic plasticity: long-term depression mechanisms in the hippocampus. Hippocampus. 1994;4:127135.Google Scholar
36.Linden, DJ. Long-term synaptic depression in the mammalian brain. Neuron. 1994;12:457472.Google Scholar
37.Malenka, RC. Synaptic plasticity in the hippocampus: LTP and LTD. Cell. 1994;78:535538.Google Scholar
38.O'Dell, TJ, Kandel, ER. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learning and Memory. 1994;1:129139.Google Scholar
39.Cain, D. Long-term potentiation and kindling: how similar are the mechanisms? TINS. 1989;12:610.Google Scholar
40.Matsuura, S, Hirayama, K, Murata, R. Enhancement of synaptic facilitation during the progression of kindling epilepsy by amygdala stimulations. J Neurophys. 1993;70:602609.Google Scholar
41.Racine, RJ, Moore, KA, Evans, C. Kindling-induced potentiation in the piriform cortex. Brain Res. 1991;556:218225.Google Scholar
42.Cain, P. Kindling in genetically altered mice. In: Corcoran, M, Moshe, S, eds. Kindling 5. New York: Plenum Press; 1996; in pressGoogle Scholar
43.Weiss, S, Li, X-L, Noguera, E, et al.Quenching: persistent alterations in seizure and afterdischarge threshold following low-frequency stimulation. In: Corcoran, M, Moshe, S, eds. Kindling V. New York: Plenum Press. In press.Google Scholar
44.Weiss, SRB, Li, X-L, Rosen, JB, Li, H, Heynen, T, Post, RM. Quenching: inhibition of development and expression of amygdala kindled seizures with low frequency stimulation. NeuroReport. 1995;4:21712176.Google Scholar
45.Paxinos, G, Watson, C. The Rat Brain in Stereotaxic Coordinates. Sydney: Academic Press; 1982.Google Scholar
46.Post, RM, Putnam, F, Uhde, TW, Weiss, SRB. ECT as an anticonvulsant: implications for its mechanism of action in affective illness. Ann NY Acad Sci. 1986;462:376388.Google Scholar
47.Sackheim, HA, Decina, P, Portnoy, S, Neeley, P, Malitz, S. Studies of dosage, seizure threshold, and seizure duration in ECT. Biol Psych. 1987;22:249268.CrossRefGoogle Scholar
48.Froc, D, Trepel, C, Racine, R. Induction of neocortical depotentiation and long-term depression in the adult behaving rat. Soc Neurosci Abstract, 1996;22:1504. [Abstract]Google Scholar
49.Bashir, ZI, Bortolotto, ZA, Davies, CH, et al.Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature. 1993;363:347350.Google Scholar
50.O'Mara, SM, Rowan, MJ, Anwyl, R. Metabotropic glutamate receptor-induced homosynaptic long-term depression and depotentiation in the dentate gyrus of the rat hippocampus in vitro. Neuropharm. 1995;34:983989.Google Scholar