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Attention network modulation via tRNS correlates with attention gain

  1. Federica Contò  Is a corresponding author
  2. Grace Edwards
  3. Sarah Tyler
  4. Danielle Parrott
  5. Emily Grossman
  6. Lorella Battelli
  1. Center for Neuroscience and Cognitive Systems@UniTn, Istituto Italiano di Tecnologia, Italy
  2. Center for Mind/Brain Sciences, University of Trento, Italy
  3. Department of Psychology, Harvard University, United States
  4. Butte College, United States
  5. Department of Cognitive Sciences, University of California, Irvine, United States
  6. Department of Neurology, Berenson-Allen Center for Noninvasive Brain Stimulation, Beth Israel, Deaconess Medical Center, Harvard Medical School, United States
Research Article
Cite this article as: eLife 2021;10:e63782 doi: 10.7554/eLife.63782
10 figures, 4 tables and 1 additional file

Figures

Procedure and stimulation sites.

(A) Experiment timeline. Thresholds for OD and TOJ tasks were performed at the beginning of the multi-session experimental procedure (green section). On the pre-test session, subjects were tested on the tasks while fMRI data were collected (blue section). A resting-state scan was also collected during this session. Next, subjects underwent behavioral training concurrently with tRNS for 25 min (Training Day 1, Training Day 2, Training Day 3, and Training Day 4, orange section). Post-test session was a repeat of the pre-test session (blue section). For detailed information on fMRI data acquisition order, see Materials and methods section. (B) Stimulation settings. Location of stimulation sites were localized using EEG 10/20 system. Saline-soaked electrodes was placed over P3 (red filled circle) and P4 (blue filled circle) for bilateral parietal and Sham stimulation, and over P07 (red filled circle) and P08 (blue filled circle) for hMT+ stimulation. (C) Intermixed trials sequence example: two types of attention tasks were randomly presented within each block, the OD and the TOJ task. (D). Example trial. The visual information was the same for TOJ and OD tasks. The cue at the beginning of the trial dictated which feature (time or orientation) should be attended. Red outline boxes are used to highlight the Gabors stimuli (black and white oriented bars) in the illustration but they were not present during the experiment. OD, orientation discrimination; TOJ, temporal order judgment.

Behavioral performance on the OD and the TOJ task during and following stimulation and training.

(A) Box plots for behavioral improvement by stimulation condition on the OD and (B) the TOJ task normalized to performance at baseline, prior to stimulation. The center line in the middle of the box is the median of each data distribution, while the box represents the interquartile range (IQR), with the lower quartile representing the 25th percentile (Q1) and the upper quartile representing the 75th percentile (Q3). (C) Change in accuracy across training days for all conditions on the OD and on the TOJ task (D) during training and stimulation sessions. Each line represents a different stimulation condition (green for parietal, orange for Sham, and blue for hMT+ group), error bars represent SEM. Asterisks indicate significant differences relative to the first training session (*<0.05, **<0.01). OD, orientation discrimination; TOJ, temporal order judgment.

Pre- and post-stimulation functional connectivity (FC) changes.

Box plots for overall mean FC of the dorsal and ventral attention network averaged per stimulation condition (Parietal, hMT+, and Sham) and per fMRI session (pre- and post-test sessions). Asterisks indicate significant difference (**<0.01).

Modulation of resting-state functional connectivity (FC) of the DVAN.

Left Panel: z-scores frequency distribution pre- (light blue bars) and post-test (light red bars) multi-session hf-tRNS coupled with training per each stimulation condition (A. Parietal, B. hMT+, C. Sham). Dark red indicates the overlapping distribution between pre- and post-test sessions. Dotted red and blue lines indicated the mean for each z-scores distribution. Right Panel: Correlation matrices represent the result of the computed difference between FC scores pre- and post-test sessions (Δ=FC(S2)−FC(S1)) depicted by condition (A. Parietal, B. hMT+, C. Sham). Each correlation difference between ROI pairs was first calculated at subject level and then averaged across subjects (detailed information on ROIs are reported in the Materials and methods section). Colors bars indicate the strength and direction of correlation change values for each regions’ pair (red colors indicate higher connectivity; blue colors indicate lower connectivity). DVAN, dorsal and ventral attention network; ROI, region of interest; tRNS, transcranial random noise stimulation.

Functional connectivity within the DVAN after multi-session hf-tRNS coupled with training (post-test session).

Correlations of all ROI pairs (z-scores) constituting the DVAN are represented separately for the three stimulation conditions (Parietal, Sham, and hMT+). Asterisks represents significant differences (**p<0.01). DVAN, dorsal and ventral attention network; ROI, region of interest; tRNS, transcranial random noise stimulation.

Functional connectivity (FC) changes between pre- and post-stimulation.

Box plots for overall change in functional connectivity (calculated as the difference in connectivity between the post- and the pre-stimulation session) for the default mode network (A) and the dorsal ventral attention network (B) depicted per stimulation condition (Parietal, hMT+, and Sham). Gray dots within each box represent the mean change in FC per condition.

Modulation of resting-state functional connectivity of the DMN.

Left Panel: z-scores frequency distribution pre- (light blue bars) and post- (light red bars) multi-session hf-tRNS coupled with training per each stimulation condition (A. Parietal, B. hMT+, C. Sham). Dark red indicates the overlapping distribution between pre- and post-sessions. Dotted red and blue lines indicated the mean for each z-scores distribution. Right Panel: Correlation matrices represent the result of the computed difference between FC scores pre- and post-test sessions (Δ=FC(S2)−FC(S1)) depicted by condition (A. Parietal, B. hMT+, C. Sham). Each correlation difference between ROI pairs was first calculated at subject level and then averaged across subjects. Colors bars indicate the strength and direction of correlation change values for each regions’ pair (red colors indicate higher connectivity; blue colors indicate lower connectivity). DMN, default mode network; ROI, region of interest; tRNS, transcranial random noise stimulation.

Task-related activity for the orientation discrimination (OD) task and electric field distribution after stimulation.

Panel A: group GLM contrasting neural activity in OD and TOJ trials versus rest (see Task-evoked brain activity section). All regions are significant at q<0.05 (FDR corrected). Yellow and red (for the OD task) and yellow and purple (for the TOJ task) colors indicate significantly positive activation. Panel B: electric field distribution on the brain induced by Parietal stimulation. Panel C: electric field distribution on the brain induced by hMT stimulation. FDR, false discovery rate; GLM, general linear model; TOJ, temporal order judgment.

Appendix 1—figure 1
Pre- and post-stimulation functional connectivity (FC) changes within the default mode network (DMN).

Overall mean FC of the DMN averaged per stimulation condition (Parietal, hMT+, and Sham) and per fMRI session (pre- and post-stimulation sessions).

Appendix 1—figure 2
Functional connectivity within the DMN after multi-session hf-tRNS coupled with training (post-stimulation session).

Correlations of all ROI pairs (z-scores) constituting the DMN are represented separately for the three stimulation conditions (Parietal, Sham, and hMT+). No differences were found between stimulation conditions. DMN, default mode network; ROI, region of interest; tRNS, transcranial random noise stimulation

Tables

Table 1
Brain coordinates.

Group mean Talairach X, Y, and Z coordinates for the centroid of each region of interest (left and right hemisphere) for the DVAN.

ROIs standardized coordinates
Left HemisphereRight Hemisphere
XYZXYZ
DVANIPS–26–634825–6048
hMT+–44–67344–716
FEF–30–54830–548
TPJ–48–542648–5421
VFC–4212–140174
Table 2
Clusters peak activation.

Peak activation coordinates of significant voxel clusters for the OD task are reported in Talairach space with relative number of voxels included in each cluster. Talairach Client was used to identy related anatomical/functional brain location and associated Broadmann Areas.

OD
ClusterX coorY coorZ coorNo. of VoxelsHemisphereBrain areaBroadmann area
129–443510,156Right cerebrumParietal lobeVisuoMotor areaBroadmann area 7
247121714Right cerebrumFrontal lobeInferior frontal gyrusBrodmann area 9
335–59–244067Right cerebellumCerebellumCulmen*
43537212337Right cerebrumFrontal lobeMiddle frontal gyrusBrodmann area 10
526–5511203Right cerebrumFrontal lobeMiddle frontal gyrusBrodmann area 6
611–2915862Right cerebrumSub-lobarThalamusPulvinar
7–47486029Left cerebrumFrontal lobeSuperior frontal gyrusBrodmann area 6
8–43–50–1511,400Left cerebrumTemporal lobeFusiform gyrusBrodmann area 37
9–16–518470Left cerebrumSub-lobarCaudateCaudate body
10–40–83919,818Left cerebrumFrontal lobePrecentral gyrusBrodmann area 6
11–40–383021,367Left cerebrumParietal lobeSupramarginal gyrusBrodmann area 40
12–31139569Left cerebrumSub-lobarInsulaBrodmann area 13
13–58–1718327Left cerebrumParietal lobePostcentral gyrusBrodmann area 43
Table 3
Peak activation coordinates of significant voxel clusters and the TOJ task are reported in Talairach space with relative number of voxels included in each cluster.

Talairach Client was used to identy related anatomical/functional brain location and associated Broadmann areas.

TOJ
ClusterX coorY coorZ coorHemisphereBrain areaBroadmann area
1471211499Right cerebrumFrontal lobeInferior frontal gyrusBrodmann area 9
229–47338339Right cerebrumParietal lobeVisuoMotor areaBroadmann area 7
329–65–272278Right cerebellumPosterior lobePyramis*
43537212564Right cerebrumFrontal lobeMiddle frontal gyrusBrodmann area 10
511–2915359Right cerebrumSub-lobarThalamusPulvinar
6–77486975Left cerebrumFrontal lobeMedial frontal gyrusBrodmann area 6
7–19–4166430Left cerebrumLimbic lobeParahippocampal gyrusBrodmann area 30
8–40–83923,304Left cerebrumFrontal lobePrecentral gyrusBrodmann area 6
9–43–413319,411Left cerebrumParietal lobeSupramarginal gyrusBrodmann area 40
Author response table 1
Bayes Factor Analysis on Orientation Discrimination data.

Table 1a and 1b reports the results of the BF analysis that tested the two models, null and Stimulation Condition (Condition). P(M) indicates the prior probabilities of each model to be equal (prior model odds). P(M|data) reports the updated probabilities having taken into consideration the data (posterior model probabilities); BFM indicates how much the data have changed the prior model odds. BF10 indicates the Bayes factors for each model (the BF10 for stimulation condition indicates how many times data are more likely to fall under the stimulation model, rather than the null model). Error % indicates the sensitivity to numerical fluctuations. Table 1c reports the results of the post-hoc Tests BF analysis. The posterior odds have been corrected for multiple testing by fixing to 0.5 the prior probability that the null hypothesis holds across all comparisons (Westfall et al. 1997). Individual comparisons are based on the default t-test with a Cauchy (0, r = 1/sqrt(2)) prior. The "U" in the Bayes factor denotes that it is uncorrected.

Table 1a
Bayesian Repeated Measures ANOVA
Data Input: OD pre, and post-stimulation performance
Model Comparison
ModelsP(M)P(MIdata)BFmBF10Error %
Null model (inc. subject)0.2000.0110.0461.000
RM Factor + Condition + RM * Condition0.2000.94569.33583.9622.528
RM Factor0.2000.0310.1262.7136.920
RM Factor + Condition0.2000.0090.0380.8342.510
Condition0.2000.0030.0130.2970.664
Note. All models include subject
Table 1b
Bayesian ANOVA
Data Input: OD performance changes
Model Comparison
ModelsP(M)P(MIdata)BFmBF10error %
Null model0.5000.0100.0101.00
Condition0.5000.99099.95699.9565.865e -4
Table 1c
Bayesian ANOVA
Post Hoc Comparison – Cond
ModelsPrior OddsPosterior OddsBF10,uerror %
Parietal vs Sham0.58718.10330.8182.505e -4
Parietal vs hMT0.58711.30419.2438.095e 4
Sham vs hMT0.5870.2990.5106.066e -4

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