Hippocampal brain-network coordination during volitionally controlled exploratory behavior enhances learning

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1 Online supplementary information for: Hippocampal brain-network coordination during volitionally controlled exploratory behavior enhances learning Joel L. Voss, Brian D. Gonsalves, Kara D. Federmeier, Daniel Tranel and Neal J. Cohen Content list: Supplementary Table 1 Supplementary Table 2 Supplementary Table 3 Supplementary Figure 1 Supplementary Figure 2 Spatial positioning Object recognition Brief range (ms) Long range (ms) Brief range (ms) Long range (ms) Exp. 1&3 Volitional Passive Exp 2 Deterministic Passive Supplementary Table 1. Average study duration ranges for brief and long conditions for Exp. 1-3.

2 Spatial positioning Object recognition WAIS-III WCS 2X2 3X3 4X4 2X2 3X3 4X4 Subject Age Edu. Sex FS GMI Cat. Per. Hipp. Vol. Pass. Vol. Pass. Vol. Pass. Vol. Pass. Vol. Pass. Vol. Pass M ** C M M C M F C F Supplementary Table 2. Descriptive and behavioral data for patients (indicated by code) and matched controls (indicated by code plus C ), including age (years), education (years), sex, WAIS-III full-scale IQ score (FS), WAIS-III general memory index score (GMI). Wisconsin card sorting test (WCS) categories (Cat.) and perseveration errors (Per.), and residual hippocampal volume (number of Z scores from average) are provided for patients only. Additional neuropsychological score details for patients are provided in reference 25. Spatial performance for patients and controls is provided as bullseye hits and near hits, respectively, as in Fig. 4, for the volitional (Vol.) and passive (Pass.) conditions. Object recognition is provided as d. **The hippocampus is destroyed bilaterally in patient 1951, and damage extends to other medial temporal structures, especially in the right hemisphere.

3 Page 2 of 4 Region BA CM X CM Y CM Z Bilateral lingual gyrus, cuneus, and precuneus Spatial extent (mm 3 ) r values 7, 17-18, 23, , /.35 Left middle and superior frontal gyrus 6, , /.26 Left middle frontal gyrus , /.38 Left parahippocampal gyrus , /.29 Right superior frontal gyrus , /.35 Right cingulate gyrus , /.31 Right middle and superior frontal gyrus 13, , /.34 Left lateral parietal cortex / supramarginal gyrus , /.35 Left thalamus (ventral lateral) , /.38 Right middle and superior frontal gyrus Left cerebellum (vermis lobule VIII and tonsil) 6, , / , /.33 Supplementary Table 3. Summary of clusters showing correlated fmri activity with the hippocampus, including Brodmann Areas (BA), center of mass (CM) in X, Y, and Z stereotactic coordinates, and the average correlation value with the hippocampus (r value) for the passive and volitional conditions (listed respectively).

4 Page 3 of 4 Supplementary Figure 1. Contrast in brain activity between volitional and passive study. A standard univariate contrast was performed between activity during volitional study and during passive study, estimated via a blocked design and analysis strategy, as described in the main text. The voxelwise statistical threshold was set to P<0.001 and a cluster extent threshold of 40 continuous suprathreshold voxels was determined via Monte Carlo simulation to yield a combined threshold of P< The analysis was performed such that both positive and negative differences could be identified, but only voxels showing more activity for volitional than for passive study were identified. Six spatially distinct clusters were identified, including: (1) a very large cluster spanning bilateral superior cerebellum, bilateral fusiform gyrus, bilateral parahippocampal gyrus, and bilateral inferior occipital gyrus (volume = 96,471mm 3 ; centroid (X,Y,Z) = +4, +50, -15), (2) a cluster spanning medial prefrontal cortex and left primary and supplementary motor areas (volume = 20,655 mm 3 ; centroid (X,Y,Z) = +17, +12, +54), (3) a cluster spanning right superior occipital cortex and lateral inferior parietal cortex (volume = 6,561 mm 3 ; centroid (X,Y,Z) = -26, +70, +28), (4) a cluster spanning several basal ganglia structures bilaterally (especially putamen and lentiform nucleus) and thalamus (volume = 2,405 mm 3 ; centroid (X,Y,Z) = +27, - 6, +8), (5) a cluster spanning bilateral inferior cerebellum (volume = 2,214 mm 3, centroid (X,Y,Z) = +18, +41, -43), and (6) a cluster within left superior parietal lobule (volume = 1,485 mm 3 ; centroid (X,Y,Z) = +32, +53, +57). These activation clusters are shown overlaid on a template brain. Thus, structures that were more active for volitional vs. passive study included many of those that were also defined based on correlated activity with the hippocampus (Figure 5), including prefrontal cortex, cerebellum, and superior and lateral parietal cortex. However, there were also regions identified that were not identified via correlation with the hippocampus, such as basal ganglia structures and primary/supplementary motor cortex. These additional activations suggest that the manual passive control condition was not entirely successful in limiting differences between volitional and passive study in terms of neural correlates of motor control, which was likely more demanding in the volitional condition. Additional behavioral manipulations would be needed to tease apart the functional significance of the various structures encompassed by these relatively large activation clusters. The correlational analysis described in the main text is thus advantageous in its identification of relatively segregated structures for which activity is related to memory performance (Figure 6). Note that activity in the first cluster described above overlaps the hippocampus at many locations, but that the analysis described in the text for defining the hippocampus anatomically in each subject provided a superior method for demonstrating more hippocampal activity for volitional vs. passive study, as reported in the main text.

Page 4 of 4 Supplementary Figure 2. Elements of the volitional network dissociate based on their contributions to spatial and item-specific memory.

5 Page 4 of 4 Supplementary Figure 2. Elements of the volitional network dissociate based on their contributions to spatial and item-specific memory. (a) Schematic diagram showing that differences in correlation with the hippocampus between volitional and passive learning in (b) bilateral DLPFC and cerebellum (CB) predicted the volitional benefit to spatial recall memory (difference in spatial positioning error for volitional versus passive). Critically, the selectivity of coupling with the hippocampus to predict spatial recall performance was shown by significantly higher correlations with spatial recall performance than with object recognition memory performance in each region [left DLPFC t(13)=2.5, P=0.01; right DLPFC t(13)=1.8, P=0.04; cerebellum t(13)=2.4; P=0.01]. (c) In contrast, the volitional benefit to object recognition memory (difference in hit rates for volitional versus passive) was predicted by the volitional/passive difference in correlation between the hippocampus, IPL and PHC/FG. All difference values are provided as z-scores. Critically, the selectivity of coupling with the hippocampus to predict object recognition performance was shown by significantly higher correlations with object recognition performance than with spatial recall performance in each region [LPC t(13)=2.3, P=0.02; PHC/FG t(13)=1.9, P=0.04]. Thus, although PHC processing has been characterized as spatial, the current selectivity suggests that its role in volitional control concerns processing objects within scenes, as relevant for the object recognition test but not the spatial recall test.

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