Effects of left prefrontal transcranial direct current stimulation on the acquisition of contextual and cued fear memory

Document Type : Original Article

Authors

1 Institute for Cognitive Science Studies (ICSS), Tehran, Iran

2 Cognitive and Neuroscience Research Center (CNRC), Tehran Medical Sciences Branch, Islamic Azad University, Tehran, Iran

3 Department of Stem Cells and Regenerative Medicine, National Institute of Genetic Engineering and Biotechnology, Tehran, Iran

4 Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

Abstract

Objective(s): Behavioral and neuroimaging studies have shown that transcranial direct current stimulation, as a non-invasive neuromodulatory technique, beyond regional effects can modify functionally interconnected remote cortical and subcortical areas. In this study, we hypothesized that the induced changes in cortical excitability following the application of cathodal or anodal tDCS over the left frontal cortex as pre-training would affect functional connectivity in resting-state circuits of fear memory and consequently could improve or disturb the acquisition of fear memory.
Materials and Methods: In order to evaluate the polarity-dependent effects of tDCS on the acquisition of fear memory and the functional connectivity, we applied left prefrontal anodal or cathodal stimulation at 200 μA for one session to healthy mice for the durations of 20 and 30 min prior to fear conditioning.
Results: Our results revealed that the administration of left prefrontal anodal (for both 20 and 30 min durations) and cathodal (at 30 min duration) tDCS impaired the acquisition of both contextual and cued fear memory. In addition, we did not observe a direct correlation between stimulation duration and the efficacy of tDCS on the acquisition of contextual and cued fear memory.
Conclusion: In this study, the impairments of both contextual and cued memory further confirmed the previous studies reporting that the administration of transcranial stimulation would affect the activity of deeper structures like amygdala and hippocampus as the main components of the fear memory circuit in acquisition, storage, and expression of the memory.

Keywords


1. Ferrucci R, Bortolomasi M, Vergari M, Tadini L, Salvoro B, Giacopuzzi M, et al. Transcranial direct current stimulation in severe, drug-resistant major depression. J Affect Disord 2009; 118:215-219.
2. Boggio PS, Valasek CA, Campanhã C, Giglio AC, Baptista NI, Lapenta OM, et al. Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Neuropsychol Rehabil 2011; 21:703-716.
3. Boggio PS, Fregni F, Valasek C, Ellwood S, Chi R, Gallate J, et al. Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J Neurol Neurosurg Psychiatry 2009; 80: 444-447.
4. Monti A, Cogiamanian F, Marceglia S, Ferrucci R, Mameli F, Mrakic-Sposta S, et al. Improved naming after transcranial direct current stimulation in aphasia. J Neurol Neurosurg Psychiatry 2008; 79:451-453.
5. Teo F, Hoy KE, Daskalakis ZJ, Fitzgerald PB,et al. Investigating the role of current strength in tDCS modulation of working memory performance in healthy controls. Front Psychiatry 2011; 2:3389.
6. Batsikadze G, Moliadze V, Paulus W, Kuo MF, Nitsche MA. Partially non‐linear stimulation intensity‐dependent effects of direct current stimulation on motor cortex excitability in humans. J Physiol 2013; 591:1987-2000.
7. Filmer HL, Dux PE, Mattingley JB. Applications of transcranial direct current stimulation for understanding brain function. Trends Neurosci 2014;37:42-753.
8. Liebetanz D, Klinker F, Hering D, Koch R, Nitsche MA, Potschka H, Löscher W, et al. Anticonvulsant effects of transcranial direct‐current stimulation (tDCS) in the rat cortical ramp model of focal epilepsy. Epilepsia 2006; 47:1216-1224.
9. Liebetanz D, Fregni F, Monte-Silva KK, Oliveira MB, Amâncio-dos-Santos A, Nitsche MA, et al. After-effects of transcranial direct current stimulation (tDCS) on cortical spreading depression. Neurosci Lett 2006; 398:85-90.
10. Paxinos G, Franklin kB. The mouse brain in stereotaxic coordinates. Gulf Professional Publishing; 2004.
11. Anagnostaras SG, Josselyn SA, Frankland PW, Silva AJ. Computer-assisted behavioral assessment of Pavlovian fear conditioning in mice. Learn Mem 2000; 7:58-72.
12. Stapley NW, Guariglia SR, Chadman KK. Cued and contextual fear conditioning in BTBR mice is improved with training or atomoxetine. Neurosci Lett 2013; 549:120-124.
13. Stevenson CW. Role of amygdala–prefrontal cortex circuitry in regulating the expression of contextual fear memory. Neurobiol Learn Mem 2011; 96:315-323.
14. McDonald A, Mascagni F, Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1996; 71:55-75.
15. Morgan MA, LeDoux JE. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav Neurosci 1995; 109:681.
16. Pitkänen A, Pikkarainen M, Nurminen N, Ylinen A. Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat: a review. Ann N Y Acad Sci 2000; 911:369-391.
17. Kochli DE, Thompson EC, Fricke EA, Postle AF, Quinn JJ. The amygdala is critical for trace, delay, and contextual fear conditioning. Learn Mem 2015; 22:92-100.
18. Fanselow MS, LeDoux JE. Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron 1999; 23:229-232.
19. Nasehi M, Zamanparvar M, Ebrahimi-Ghiri M, Zarrindast MR. Modulation of cannabinoid signaling by hippocampal 5-HT4 serotonergic system in fear conditioning. J Psychopharmacol 2016; 30:936-944.
20. Nasehi M, Davoudi K, Ebrahimi-Ghiri M, Zarrindast MR.  Interplay between serotonin and cannabinoid function in the amygdala in fear conditioning. Brain Res 2016; 1636:142-151.
21. Nasehi M, Kamali-Dolatabadi L, Torabi-Nami M, Zarrindast MR. Possible involvement of the CA1 GABAA receptors upon acquisition and expression of the ACPA-induced place preference in mice. Physiol Behav 2016; 161:155-165.
22.Nasehi M, Meskarian M, Khakpai F, Zarrindast MR. Harmaline-induced amnesia: Possible role of the amygdala dopaminergic system. Neuroscience 2016; 312:1-9.
23. Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, et al. Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 2013; 6:424-432.
24. Baudewig J, Nitsche MA, Paulus W, Frahm J. Regional modulation of BOLD MRI responses to human sensorimotor activation by transcranial direct current
stimulation. Magn Reson Med 2001; 45:196-201.
25. Asthana M, Nueckel K, Mühlberger A, Neueder D, Polak T, Domschke K, et al. Effects of transcranial direct current stimulation on consolidation of fear memory. Front Psychiatry 2013; 4:107.
26. Dudai Y. The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 2004; 55:51-86.
27. McGaugh JL. Memory--a century of consolidation. Science 2000; 287:248-251.
28. Mungee A, Kazzer P, Feeser M, Nitsche MA, Schiller D, Bajbouj M. Transcranial direct current stimulation of the prefrontal cortex: a means to modulate fearmemories. Neuroreport 2014; 25:480-484.
29. Tsuji M, Takeda H, Matsumiya T. Different effects of 5-HT1A receptor agonists and benzodiazepine anxiolytics on the emotional state of naive and stressed mice: a study using the hole-board test. Psychopharmacology 2000; 152:157-166.
30. Takeda H, Tsuji T, Matsumiya T. Changes in head-dipping behavior in the hole-board test reflect the anxiogenic and/or anxiolytic state in mice. Eur J Pharm 1998; 350:21-29.
31. Stone EA, Trullas R, Platt JE. The effect of acute and chronic administration of desmethylimipramine on responses to stress in rats. Prog Neuro-Psychopharmacol Biol Psychiatry 1984; 8:587-592.
32. Echandia ER, Broitman S, Foscolo M. Effect of the chronic ingestion of chlorimipramine and desipramine on the hole board response to acute stresses in male rats. Pharmacol Biochem Behav 1987; 26:207-210.
33. Vazdarjanova A, McGaugh JL. Basolateral amygdala is not critical for cognitive memory of contextual fear conditioning. Proc Natl Acad Sci 1998; 95:15003-15007.