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Contributed by Daniel L. Schacter, April 3, 2020 (sent for review February 25, 2020; reviewed by Roberto Cabeza and Joel L. Voss)
Article Figures & SI
Figures
- Fig. 1.
TMS-behavioral results. (A) Mean number of internal and external details for the simulation and control tasks produced following vertex cTBS and left AG cTBS. (B) Mean divergent thinking performance (measured as the total number of appropriate uses generated [fluency] and categories of appropriate uses [flexibility]) following vertex cTBS and left AG cTBS. Error bars denote mean (±1 SE). Asterisks indicate significant results (see TMS Behavioral Results for details).
- Fig. 2.
(A) cTBS target sites for each of the 18 participants overlaid on the across-participant mean T1-weighted anatomical image. Each red square denotes the cTBS target for each participant. The coronal slices are spaced every 1 mm with the most posterior (Upper Left) and anterior (Lower Right) corresponding to y = −71 and y = −61, respectively. (B) Group seed-to-target resting-state connectivity as a function of cTBS site. Error bars denote mean (±1 SE) connectivity. Asterisks indicate significant results (see fMRI-TMS Results, Resting-state analyses for details).
- Fig. 3.
fMRI-TMS results: Hippocampus. (A) Shown in red are hippocampal regions demonstrating greater activity for the episodic simulation and divergent thinking tasks relative to the nonepisodic control task following cTBS to the vertex. (B) Hippocampal regions demonstrating greater activity for the episodic simulation and divergent thinking tasks relative to the nonepisodic control task following cTBS to the AG. Results are overlaid on the across-participant mean T1-weighted anatomical image.
- Fig. 4.
fMRI-TMS results: Hippocampus. (A) Shown in red are hippocampal regions demonstrating a cTBS site by task interaction (i.e., reduced recruitment for constructing imagined events and generating creative uses following AG cTBS compared with cTBS to the vertex with the opposite effect for the control task). The chart depicts percent signal change (extracted from the region’s peak voxel) for each task and cTBS site. Note that error bars are not plotted as a result of potential noise, and significance tests were not run on these data. (B) The fMRI-cTBS effect identified in the hippocampus (shown in red) overlapped the hippocampal seed region targeted with cTBS (shown in blue; i.e., the coordinate employed in the seed-to-voxel analysis to identify the cTBS target region in the left AG). Overlap is shown in magenta. Results are overlaid on the across-participant mean T1-weighted anatomical image.
- Fig. 5.
fMRI-TMS results: Whole-brain. (A) Shown in red are whole-brain regions demonstrating greater activity for the episodic simulation and divergent thinking tasks relative to the nonepisodic control task following cTBS to the vertex. (B) Whole-brain regions demonstrating greater activity for the episodic simulation and divergent thinking tasks relative to the nonepisodic control task following cTBS to the AG. Results are overlaid on the across-participant mean T1-weighted anatomical image.
- Fig. 6.
fMRI-TMS results: Whole-brain. Shown in red are whole-brain regions demonstrating a cTBS site by task interaction (i.e., reduced recruitment for constructing imagined events and generating creative uses following cTBS to the left AG compared with cTBS to the vertex with the opposite effect for the control task). The charts depict percent signal change extracted from peak voxels within two representative clusters within the left lateral temporal cortex (x = −65, y = −30, z = −24) and medial prefrontal cortex (x = 13, y = 46, z = 15) for each task and cTBS site. Note that error bars are not plotted as a result of potential noise, and significance tests were not run on these data. Results are projected onto a cortical surface using the skull-stripped template of MRIcroGL (see ref. 32).
- Fig. 7.
Experimental design. In each task participants were shown an object word for 15 s. For the episodic simulation task (Top), participants were asked to silently imagine a novel future experience related to the object. For the divergent thinking task (Middle), participants were asked to generate creative and unusual uses for the object. For the control task (Bottom), participants were asked to generate two associated objects, put them in a sentence by their relative size, and then generate definitions related to the objects. After each trial, participants rated the level of detail and difficulty on a 5-point scale. The trial ended with a variable fixation period.
- Fig. 8.
Representative-participant cTBS target identification. (A) On an individual participant basis, a seed-to-voxel analysis was conducted using the resting-state data from the no-cTBS session (i.e., session 1). A 6-mm sphere (shown in red) in the left anterior hippocampus was centered on a peak voxel previously associated with divergent thinking, episodic simulation, and episodic memory (x = −25, y = −10, z = −19; see fMRI Aquisition and Analysis, Resting-state analysis for details). (B) Whole-brain correlation images were created by using the averaged time series across all voxels comprising the seed and the time series corresponding to each voxel across the brain with Pearson’s correlation. The AG cTBS target (shown in red) was selected as the peak coordinate in the left AG demonstrating the greatest resting-state connectivity (i.e., Fisher-transformed correlation, r) and that fell within the left Brodmann area 39 (i.e., the left AG). Resting-state results are overlaid onto a representative participant anatomic image.
Tables
MNI coordinates Peak Z Number of above-threshold voxels Region X y z Hippocampus −31 −17 −22 3.99 36 Left hippocampus 27 −13 −22 3.97 24 Right hippocampus Whole brain 42 50 −12 5.39 243 Right inferior frontal gyrus −27 7 17 5.30 111 Left frontal operculum 42 −7 41 3.65 228 Right middle frontal gyrus 5 55 −24 4.83 372 Right ventromedial prefrontal cortex −12 51 −16 Left ventromedial prefrontal cortex 13 0 24 4.59 130 Right caudate nucleus −5 −42 −50 4.52 231 Left cerebellum 5 −39 −38 Right cerebellum −21 −78 −33 4.39 175 Left cerebellum 22 34 −7 4.33 162 Right orbital gyrus 56 −22 −19 4.33 227 Right inferior temporal sulcus 59 −13 −17 Right middle temporal gyrus 47 −24 −27 Right inferior temporal gyrus 13 −49 27 4.31 226 Right posterior cingulate/retrosplenial cortex 44 −53 25 Right angular gyrus −9 −41 63 4.28 110 Left paracentral lobule 3 −30 64 Right paracentral lobule −17 −52 −21 4.27 177 Left cerebellum 18 −76 54 4.21 98 Right superior parietal lobule 17 −85 42 Right superior occipital gyrus 37 4 20 4.19 166 Right frontal operculum −65 −30 −24 4.19 189 Left inferior temporal gyrus −55 −20 −17 Left middle temporal gyrus −10 −80 29 3.99 172 Left superior occipital gyrus 13 46 15 3.94 256 Right dorsomedial prefrontal cortex 12 65 12 Right anterior prefrontal cortex 10 44 39 3.77 158 Right superior frontal gyrus −2 −68 5 3.17 96 Left extrastriate cortex MNI, Montreal Neurological Institute. Coordinates for cluster subpeaks that lie in distinct cortical regions are listed directly below relevant peak cluster.
Data supplements
Supporting Information
Modulation of hippocampal brain networks produces changes in episodic simulation and divergent thinking
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