Offline tDCS modulates prefrontal-cortical-subcortical-cerebellar fear pathways in delayed fear extinction

doi:10.1007/s00221-021-06248-9

. 2022 Jan;240(1):221-235.

doi: 10.1007/s00221-021-06248-9. Epub 2021 Oct 25.

Offline tDCS modulates prefrontal-cortical-subcortical-cerebellar fear pathways in delayed fear extinction

Ana Ganho-Ávila^{1

2

3

4}, Raquel Guiomar^{5

6}, Daniela Valério^{5

6}, Óscar F Gonçalves^{7

8

9}, Jorge Almeida^{5

6}

Affiliations

¹ Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3001-802, Coimbra, Portugal. ganhoavila@fpce.uc.pt.
² Center for Research in Neuropsychology and Cognitive Behavioral Intervention - CINEICC of the Faculty of Psychology and Educational Sciences, University of Coimbra, Rua do Colégio Novo, 3000-115, Coimbra, Portugal. ganhoavila@fpce.uc.pt.
³ Clinical & Developmental Neurosciences, CIPSI, University of Minho, 4710-057, Braga, Portugal. ganhoavila@fpce.uc.pt.
⁴ School of Psychology, University of Minho, 4710-057, Braga, Portugal. ganhoavila@fpce.uc.pt.
⁵ Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3001-802, Coimbra, Portugal.
⁶ Center for Research in Neuropsychology and Cognitive Behavioral Intervention - CINEICC of the Faculty of Psychology and Educational Sciences, University of Coimbra, Rua do Colégio Novo, 3000-115, Coimbra, Portugal.
⁷ Clinical & Developmental Neurosciences, CIPSI, University of Minho, 4710-057, Braga, Portugal.
⁸ School of Psychology, University of Minho, 4710-057, Braga, Portugal.
⁹ Department of Applied Psychology, Northeastern University, Boston, MA, 02115, USA.

PMID: 34694466
DOI: 10.1007/s00221-021-06248-9

Offline tDCS modulates prefrontal-cortical-subcortical-cerebellar fear pathways in delayed fear extinction

Ana Ganho-Ávila et al. Exp Brain Res. 2022 Jan.

. 2022 Jan;240(1):221-235.

doi: 10.1007/s00221-021-06248-9. Epub 2021 Oct 25.

Authors

Ana Ganho-Ávila^{1

2

3

4}, Raquel Guiomar^{5

6}, Daniela Valério^{5

6}, Óscar F Gonçalves^{7

8

9}, Jorge Almeida^{5

6}

Affiliations

¹ Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3001-802, Coimbra, Portugal. ganhoavila@fpce.uc.pt.
² Center for Research in Neuropsychology and Cognitive Behavioral Intervention - CINEICC of the Faculty of Psychology and Educational Sciences, University of Coimbra, Rua do Colégio Novo, 3000-115, Coimbra, Portugal. ganhoavila@fpce.uc.pt.
³ Clinical & Developmental Neurosciences, CIPSI, University of Minho, 4710-057, Braga, Portugal. ganhoavila@fpce.uc.pt.
⁴ School of Psychology, University of Minho, 4710-057, Braga, Portugal. ganhoavila@fpce.uc.pt.
⁵ Proaction Laboratory, Faculty of Psychology and Educational Sciences, University of Coimbra, 3001-802, Coimbra, Portugal.
⁶ Center for Research in Neuropsychology and Cognitive Behavioral Intervention - CINEICC of the Faculty of Psychology and Educational Sciences, University of Coimbra, Rua do Colégio Novo, 3000-115, Coimbra, Portugal.
⁷ Clinical & Developmental Neurosciences, CIPSI, University of Minho, 4710-057, Braga, Portugal.
⁸ School of Psychology, University of Minho, 4710-057, Braga, Portugal.
⁹ Department of Applied Psychology, Northeastern University, Boston, MA, 02115, USA.

PMID: 34694466
DOI: 10.1007/s00221-021-06248-9

Abstract

Transcranial direct current stimulation (tDCS) has been studied to enhance extinction-based treatments for anxiety disorders. However, the field shows conflicting results about its anxiolytic effect and only a few studies have observed the extinction of consolidated memories. We looked to study the effect of offline 1 mA tDCS over the right dorsolateral pre-frontal cortex across the fear pathways, in consolidated fear response during delayed extinction. Participants (N = 34 women) underwent in a two-day fear conditioning procedure. On day 1, participants were assigned to the control group (N = 18) or the tDCS group (N = 16) and went through a fear acquisition procedure. On day 2, the tDCS group received 20 min tDCS before extinction and while inside the MRI scanner. The control group completed the extinction procedure only. The tDCS session (for the tDCS group) and the fMRI scan (for both groups) were completed just on the second day. Univariate fMRI analysis showed stimulation-dependent activity during late extinction with the tDCS group showing decreased neural activity during the processing of threat cues (CS +) and increased activity during the processing of safety cues (CS -), in prefrontal, postcentral and paracentral regions, during late extinction. ROI to whole-brain psychophysiological interaction (PPI) analysis showed the tDCS effect on the connectivity between the left dorsolateral prefrontal cortex three cortical-amygdalo-hippocampal-cerebellar pathway clusters during the processing of the CS + in late extinction (TFCE corrected; p < 0.05). Increased neuronal activity during the processing of safety cues and stronger coupling during the processing of threat cues might be the mechanisms by which tDCS contributes to stimuli discrimination.

Keywords: Anxiety; Cortical––Amygdalo–Hippocampal–Cerebellar pathways; Delayed extinction; Partial fear conditioning; Psychophysiological analysis; tDCS.

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References

1. Abend R, van ’t Wout M (2018) Commentary: augmentation of fear extinction by transcranial direct current stimulation (tDCS). Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2018.00121 - DOI - PubMed - PMC
1. Abend R, Jalon I, Gurevitch G, Sar-El R, Shechner T, Pine DS, Hendler T, Bar-Haim Y (2016) Modulation of fear extinction processes using transcranial electrical stimulation. Transl Psychiatry 6:e913–e913. https://doi.org/10.1038/tp.2016.197 - DOI - PubMed - PMC
1. Agren T, Engman J, Frick A, Bjorkstrand J, Larsson E-M, Furmark T, Fredrikson M (2012) Disruption of reconsolidation. Science 337:1550–1552. https://doi.org/10.1126/science.1223006 - DOI - PubMed
1. Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci off J Soc Neurosci 28:6211–6219. https://doi.org/10.1523/JNEUROSCI.1246-08.2008 - DOI
1. Antal A, Bikson M, Datta A, Lafon B, Dechent P, Parra LC, Paulus W (2014) Imaging artifacts induced by electrical stimulation during conventional fMRI of the brain. NeuroImage Neuro-Enhanc 85:1040–1047. https://doi.org/10.1016/j.neuroimage.2012.10.026 - DOI

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[1] Abend R, van ’t Wout M (2018) Commentary: augmentation of fear extinction by transcranial direct current stimulation (tDCS). Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2018.00121 - DOI - PubMed - PMC

[2] Abend R, van ’t Wout M (2018) Commentary: augmentation of fear extinction by transcranial direct current stimulation (tDCS). Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2018.00121 - DOI - PubMed - PMC

[3] Abend R, Jalon I, Gurevitch G, Sar-El R, Shechner T, Pine DS, Hendler T, Bar-Haim Y (2016) Modulation of fear extinction processes using transcranial electrical stimulation. Transl Psychiatry 6:e913–e913. https://doi.org/10.1038/tp.2016.197 - DOI - PubMed - PMC

[4] Abend R, Jalon I, Gurevitch G, Sar-El R, Shechner T, Pine DS, Hendler T, Bar-Haim Y (2016) Modulation of fear extinction processes using transcranial electrical stimulation. Transl Psychiatry 6:e913–e913. https://doi.org/10.1038/tp.2016.197 - DOI - PubMed - PMC

[5] Agren T, Engman J, Frick A, Bjorkstrand J, Larsson E-M, Furmark T, Fredrikson M (2012) Disruption of reconsolidation. Science 337:1550–1552. https://doi.org/10.1126/science.1223006 - DOI - PubMed

[6] Agren T, Engman J, Frick A, Bjorkstrand J, Larsson E-M, Furmark T, Fredrikson M (2012) Disruption of reconsolidation. Science 337:1550–1552. https://doi.org/10.1126/science.1223006 - DOI - PubMed

[7] Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci off J Soc Neurosci 28:6211–6219. https://doi.org/10.1523/JNEUROSCI.1246-08.2008 - DOI

[8] Alvarez RP, Biggs A, Chen G, Pine DS, Grillon C (2008) Contextual fear conditioning in humans: cortical-hippocampal and amygdala contributions. J Neurosci off J Soc Neurosci 28:6211–6219. https://doi.org/10.1523/JNEUROSCI.1246-08.2008 - DOI

[9] Antal A, Bikson M, Datta A, Lafon B, Dechent P, Parra LC, Paulus W (2014) Imaging artifacts induced by electrical stimulation during conventional fMRI of the brain. NeuroImage Neuro-Enhanc 85:1040–1047. https://doi.org/10.1016/j.neuroimage.2012.10.026 - DOI

[10] Antal A, Bikson M, Datta A, Lafon B, Dechent P, Parra LC, Paulus W (2014) Imaging artifacts induced by electrical stimulation during conventional fMRI of the brain. NeuroImage Neuro-Enhanc 85:1040–1047. https://doi.org/10.1016/j.neuroimage.2012.10.026 - DOI

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Offline tDCS modulates prefrontal-cortical-subcortical-cerebellar fear pathways in delayed fear extinction

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Offline tDCS modulates prefrontal-cortical-subcortical-cerebellar fear pathways in delayed fear extinction

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Abstract

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