Figures and data in Suppression weakens unwanted memories via a sustained reduction of neural reactivation

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5 figures, 7 tables and 1 additional file

Figures

Figure 1

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Experimental procedure, univariate MRI, and behavioral results.

(a) Illustration of the adapted Think/No-Think procedure. Participants studied associations between unique objects and aversive scenes. Both during a pre- and a post-test, they covertly recalled all the scenes in response to the objects and rated the vividness of their recollection. In between these two tests, they performed the Think/No-Think phase. Specifically, for objects presented in a green frame, participants repeatedly recalled the associated scene (*recall condition*). By contrast, for objects presented in a red frame, they suppressed the retrieval of the associated scene (*suppress condition*). Note that we did not present a third of the objects during this phase (*baseline condition*). Afterwards, participants performed a one-back task that served to train a pattern classifier in detecting evidence for scene reactivation. Finally, participants once more recalled the memories outside the MRI scanner (now shown in this figure). The complete experimental procedure is comprehensively described in the methods. (NB) Following the IAPS user agreement, we have replaced the original pictures with similar scenes for this figure. In the original stimulus set, each object cue also features in its paired scene. (b) The suppression phase yielded the typical activity pattern associated with retrieval suppression, including greater activation in the right dorsolateral prefrontal cortex (dlPFC) and reduced activation in the hippocampus (HPC) and parahippocampal cortex (PhC) during *suppress* versus *recall* trials. For display purposes, the images are thresholded at *p <* .001, uncorrected, with a minimum cluster size of 50 voxels. (c) Suppression caused a reduction in self-reported vividness from the pre- to post-test that exceeded any change due to the passage of time as indexed by the *baseline* condition. This effect replicated across the fMRI study (n = 33) and a behavioral study (n = 30) with an independent sample. Large dots indicate the mean, error bars the standard error of the mean. *** p < .001, ** p < .01, * p < .05.

Figure 2

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Effects of suppression on scene reactivation.

(a) A linear support vector machine was trained on data of an independent task to discriminate neural activity patterns associated with the perception of intact versus morphed aversive scenes. (NB) Following the IAPS user agreement, we have replaced the original pictures with similar scenes for this figure. The dot product of the resulting weight pattern and single-trial t-maps was used as a proxy for reactivated scene information. We compared such scene evidence between conditions globally across the grey matter and more locally in the left and right parahippocampal cortices (PhC, manually segmented on the individual structural images). (b) Across the grey matter and locally in left PhC, there is less scene evidence while participants suppress than recall scene memories. (c) The suppression-induced reduction in scene evidence lingers on after suppression: scene evidence decreases from the pre- to the post- test for suppressed memories but not for baseline memories. This was the case across the grey matter and in the PhC. Larger dots indicate the mean, error bars the standard error of the mean. *** p < .001, ** p < .01, * p < .05, n = 33.

Figure 3

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A greater suppression-induced reduction in vividness is associated with a greater suppression-induced reduction in scene evidence in right PhC as indicated by a robust skipped Spearman's correlation.

The left PhC showed a non-significant trend only for this effect. Black lines indicate linear regression lines, dark grey shades indicate 95%- confidence intervals, PhC: parahippocampal cortex.

Figure 4

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Effects of suppression on individual memory representations.

(a) We estimated the reinstatement of the neural memory representations by assessing the similarity of the activity patterns across the pre- and the post-test. We take the difference between the same-item and different-item similarity as an index of neural reinstatement. (NB) Following the IAPS user agreement, we have replaced the original pictures with similar scenes for this figure. (b) In the PhC, the difference between same- and different-item similarity was significant for the baseline memories. These memories thus seem to have been consistently reinstated across the two tests. By contrast, the suppressed memories only showed a trend for this effect, though the critical interaction was not significant. Large dots indicate the mean, error bars the standard error of the mean. (c) A greater suppression-induced reduction in vividness was associated with a greater suppression-induced reduction in reinstatement in the right PhC (as indicated by a robust skipped Spearman's correlation). Black lines indicate linear regression lines, dark grey shades indicate 95% - confidence intervals, PhC: parahippocampal cortex. ** p < .01, * p < .05, ° p < .1, n = 33.

Appendix 1—figure 1

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Effects of retrieval practice.

(a) Retrieval retained vividness from the pre- to post-test as compared with the baseline condition. (b) Retrieval induced a reduction in scene evidence in left PhC: scene evidence decreased from the pre- to the post- test for recalled memories but not for baseline memories. Larger dots indicate the mean, error bars the standard error of the mean. (c) A greater above-baseline increase in vividness is associated with a greater above-baseline increase in scene evidence in left PhC as indicated by a robust skipped Spearman’s correlation. (d) This greater above-baseline increase in vividness is also associated with a greater above-baseline increase in reinstatement in left PhC. Black lines indicate linear regression lines, dark grey shades indicate 95% - confidence intervals, PhC: parahippocampal cortex. ** p < .01, * p < .05, n = 33.

Tables

Table 1

Software resources used.

Designation	Source/ Reference	Identifier
R version 4.0.3,RStudio	R Project for Statistical Computing	https://www.r-project.org/
MATLAB, 2017	Mathworks	https://mathworks.com/
Psychtoolbox 3	Pelli, 1997	https://psychtoolbox.org/
FMRIPrep	Poldrack Lab,Standford University	https://fmriprep.org/en/1.5.0/
SPM12	Wellcome Centre for Neuroimaging, UCL	https://fil.ion.ucl.ac.uk/spm/
The decoding toolbox	Hebart et al., 2014	https://sites.google.com/site/tdtdecodingtoolbox/
RSA toolbox	Nili et al., 2014	https://github.com/rsagroup/rsatoolbox
ITK-SNAP	Yushkevich et al., 2006	http://itksnap.org/

Appendix 1—table 1

Demographic information.

Study	Sample size	Age in yearsM(SD)	TCAQ	BDI	STAI-S	STAI-T
Behavioral Study	30(15 female)	23.83 (1.76)	81.61 (15.11)
fMRI study	33(17 female)	24.85 (2.14)	87.94 (16.2)	4.27 (5.06)	34.78 (8.37)	35.78 (8.87)

Note: Of the questionnaire data, exploratory analyses only suggested a relationship between the TCAQ and suppression-induced reductions in vividness. There was a trend for a skipped Spearman correlation in the MRI study (r = 0.32, 95% CI = [–0.08 0.58]) and a significant correlation across the two studies (r = 0.27, 95% CI = [0.004 0.49]).

Appendix 1—table 2

Control regions: Suppress >Recall.

Region	~BA	Hemi-sphere	Voxels	x	MNIy	z	t-value
Occipital, inferior temporal	18	L	10,034	-28	-88	10	10.83
	19	L		-46	-80	-8	10.26
	19	L		-30	-90	20	9.79
Occipital, inferior temporal	18	R	9,037	40	-90	4	9.03
	37	R		36	-44	-18	8.82
	7	R		30	-68	30	8.68
Superior & middle frontal *	6	L/R	10,089	8	22	62	8.89
	13	R		28	20	-12	8.59
	6	R		48	6	28	7.84
Thalamus		L/R	681	2	-6	18	6.54
		R		4	-22	18	5.48
		R		12	-14	18	5.07
Inferior frontal	13	L	723	-36	20	-4	6.51
	13	L		-30	20	-12	6.51
	45	L		-42	22	8	6.51
Middle frontal	6	L	738	-48	4	30	6
	6	L		-56	8	44	5.12
	6	L		-48	14	42	4.95
Orbitofrontal	47	L	166	-34	46	-14	4.88
Orbitofrontal	47	L	166	-46	44	-14	4.5
Superior & middle frontal	9	L	219	-24	46	34	4.59
	10	L		-24	50	26	4.59
	10	L		-30	56	20	4.03

Note. Thresholded at p < .05, FWE cluster corrected, with a cluster forming threshold of p < .001; local maxima more than 8 mm apart, minimum of 10 voxels. BA = Brodmann area.
*

includes peak for direct suppression by Benoit and Anderson, 2012

Appendix 1—table 3

Modulated regions: Suppress <Recall.

Region	~BA	Hemisphere	Voxels	x	MNIy	z	t-value
Cuneus, precuneus, HPC, amygdala, PhC	19	L/R	31,631	-10	-82	34	9.88
	23	L		12	-56	24	9.85
	18	L		-18	-62	22	9.34
Cerebellum		L	185	12	-52	-62	5.59
		L		22	-48	-52	5.22
		L		18	-58	-48	4.2

Note. Thresholded at p < .05, FWE cluster corrected, with a cluster forming threshold of p < .001; local maxima more than 8 mm apart, minimum of 10 voxels. BA = Brodmann area, HPC = Hippocampus, PhC = Parahippocampal cortex.

Appendix 1—table 4

Suppression-induced reductions in univariate brain activity: (Baseline_Post > Suppress_Post) > (Baseline_Pre > Suppress_Pre).

Region	~BA	Hemi-sphere	Voxels	x	MNIy	z	t-value
Middle temporal, fusiform, inferior occipital	37	R	290	54	-70	2	6.17
Precentral, Postcentral	6	L	344	-64-34 -28	-18-14-34	446270	5.375.234.72
Lingual	18/19	R	132	2026	-76-70	-4-4	5.224.18
Supplementary motor area	6	L	180	-6-14-10	-14-16-6	564650	5.074.883.87
Middle Temporal	19	L	156	-52-40	-70-70	812	4.814.25
Hippocampus		R	133	302416	-6-14-8	-2616-18	4.674.553.97
Superior occipital	19	L	126	-18-12	-84-84	3434	4.594.59
Lingual, cerebellum	37/19	R	118	263020	-44-56-54	-10-24-12	4.254.363.96

Note. Thresholded at p < .05, FWE cluster corrected, with a cluster forming threshold of p < .001; local maxima more than 8 mm apart, minimum of 10 voxels. BA = Brodmann area.

Appendix 1—table 5

Results of candidate control regions.

ROI	Classifier accuracyM (SD)	Reduced scene reactivation following suppression	Correlation between suppression-induced reductions in scene reactivation and in vividness	Reinstatement: same-item similarity >different item similarity	Correlation between suppression-induced reductions in reinstatement and in vividness
Amygdala	62.4% (21.2)t(32) = 3.6,p = .002	M_B pre = –0.001M_B post = –0.003M_S pre = –0.003M_S post = –0.007F(1,32) = 1.13,p = .29	r = 0.06,95% CI = [–0.35 0.43]	M_B same = 0.021M_B different = 0.018M_S same = 0.019M_S different = 0.022F(1,32) = 0.34,p = .56	r = –0.02,95% CI = [–0.38 0.35]
Angular gyrus	76.8% (16)t(32) = 9.6,p < .001	M_B pre = –0.030M_B post = –0.023M_S pre = –0–028M_S post = –0–021F(1,32) = 0.0,p = .97	r = 0.49,95% CI = [–0.04 0.67]	M_B same = 0.146M_B different = 0.125M_S same = 0.132M_S different = 0.123F(1,32) = 2.1,p = .16	r = 0.1,95% CI = [–0.23 0.41]
Precuneus	80.6% (13.8)t(32) = 12.8,p < .001	M_B pre = 0.004M_B post = 0.008M_S pre = 0.007M_S post = 0.009F(1,32) = 0.15,p = .71	r = 0.32,95% CI = [–0.05 0.61]	M_B same = 0.103M_B different = 0.093M_S same = 0.108M_S different = 0.092F(1,32) = 2.1,p = .16	r = –0.09,95% CI = [–0.42 0.23]
V1	70.7% (14.5)t(32) = 8.2,p < .001	M_B pre = –0.096M_B post = –0.089M_S pre = –0.088M_S post = –0.097F(1,32) = 3.29,p = .08	r = 0.2,95% CI = [–0.21 0.58]	M_B same = 0.524M_B different = 0.482M_S same = 0.542M_S different = 0.483F(1,32) = 3.94,p = .056	r = 0.05,95% CI = [–0.21 0.58]

Note. B = Baseline, S = Suppress. Robust skipped spearman correlations

Appendix 1—table 6

Behavioral results of the final memory test.

Study	Measure	BaselineM (SD)	SuppressM (SD)	RecallM (SD)
Behavioral Study	Identification	0.94 (0.18)	0.92 (0.19)	0.94 (0.18)
	Gist	0.52 (0.20)	0.48 (0.19)	0.5 (0.19)
	Details	9.24 (2.71)	9.07 (2.73)	9.47 (2.84)
fMRI study	Identification	0.98 (0.05)	0.96 (0.07)	0.96 (0.06)
	Gist	0.55 (0.15)	0.54 (0.14)	0.55 (0.15)
	Details	9.77 (1.61)	9.66 (1.74)	9.71 (1.75)