We addressed whether a particular gaze deviation affected behavioral aspects of finger movements by computing the reaction time (RT) of finger movements (elapsed time between the green cue appearing and the first tap, see ) by testing the null-hypothesis of no difference of RT for each target, using a one-way ANOVA. This analysis revealed no difference in RT across the nine targets, F8,117 = 0.35, with the mean (±SD) RT = 328 ± 30 ms (averaged across all nine targets; range: 290–370 ms). We also considered whether participants, contrary to the instructions, performed an unequal number of taps for different targets. The output of the one-way ANOVA failed to reject the null hypothesis that tap quantity did not differ across the nine gaze positions, with a mean number of finger taps per target of 3.05 ± 0.05 (averaged across targets; F8,117 = 1.11). These results indicate that behavior had similarity across the various gaze locations.
Finger movement-dependent gaze effects
We identified seven clusters that exhibited finger movement-related activation; their location appears in and provides additional details about these activation clusters. The largest of these finger movement related clusters appeared in occipital lobe and encompassed portions of the visual cortex, lingual gyrus (BA18, BA19), cuneus bilaterally, and right SPL (BA7); its location had consistency with prior work in our laboratory showing involvement of occipital cortical areas in visually paced tapping (Kim et al. 2005
). We also found clusters in more classical motor regions, including the left M1 (BA4), right cerebellum (CR-IV-V), left ACC (BA24), right SPL (BA7), left SMA (BA6), and right putamen.
depicts the percent signal change for each cluster as a function of gaze positions in the horizontal dimension; the data revealed that all clusters exhibited increased activation as gaze deviated rightward. Our analyses did not reveal any cluster with the greatest movement-related activation when participants gazed leftward. All seven clusters had slopes significantly different than zero (all p < 0.0005) as gaze deviated increasingly rightward, indicating significant gaze effects on finger movement-related activation. Note that for the clusters in SPL and visual cortex the functional MRI signal was deactivated for all gaze positions; thus, gaze deviations toward the right yielded less deactivation, in other words, a relative increase in activation as gaze position moved from the left to the right. The regression analysis using the non-linear [1 2 2] model also indicated that all clusters had slopes significantly different than zero. However, we found that not all of the gaze-related patterns from individual voxels within any particular cluster exhibited a positive slope (). To evaluate the distribution of gaze-related patterns types within a cluster, we tabulated the percentage of voxels that exhibited a gaze-related pattern with a positive slope and ascertained whether this percentage occurred by chance. For all clusters, but the putamen, the percentage of positive slopes differed significantly than what was expected by chance (X2 > 3.84 (df = 1), p < 0.05). In the putamen, activation for 10/12 voxels exhibited a gaze-related positive slope. The lack of significance likely relates to power issue as 11/12 voxels with positive slope would have been significantly different than chance.
Fig. 3 Gaze effects of the finger movement-related activation for the horizontal and vertical dimensions. a Activation for horizontal gaze shifts (pooled across vertical dimension). Movement-related activation increases as gaze deviates towards the right for (more ...)
For vertical gaze, all but one of the clusters with movement-related activation exhibited slopes significantly different than zero. The clusters in the SMA, ACC, SPL, cerebellum, and visual cortex showed increased activation as gaze deviated upward, whereas the putamen had increased activation as gaze deviated downward (all p < 0.002). The activation in M1 did not exhibit a vertical gaze effect, i.e., slopes were not significantly different than zero (p = 0.66). We also tabulated the percentage of voxels within each cluster that exhibited activation having positive slope as gaze increasing deviated downward. This analysis revealed that all, but M1, had more negative slopes than what was expected by chance; the putamen had more positive slopes than expected by chance ().
We found that all seven clusters with finger movement-related activation had slopes significantly different than zero for the LL-UR model (all p < 0.005), and all clusters but the one located in the putamen showed increased activation for gaze deviating toward the upper-right; the putamen exhibited increased activation for gaze deviating towards the lower left. For the UL-LR model all clusters but the ACC and SMA (p > 0.01) had slopes significantly different than zero and these showed increased of activation as gaze deviated towards the lower-right. illustrates the finger movement-related activation for all gaze positions for the cerebellum, SPL, and putamen.
We also note that participants experienced asymmetric visual input to the two hemispheres when they looked to the left or to the right targets. Since the targets remained visible throughout the procedures, it is possible that some of the observed activation patterns related to asymmetries in visual input, especially regarding lateralization of possible activation patterns. To address this potential confound, we examined the spatial distribution of the positive and negative slopes within the activation clusters relative to gaze deviating from left to right. We found that the cluster located in the region of the visual cortex exhibited a clear spatial dependence on visual input such that voxels in the left hemisphere had negative activation slopes, that is, less activation as gaze deviated increasingly rightward, whereas voxels in the right hemisphere had positive slopes, that is, more activation as gaze deviated increasingly rightward. No other activation cluster showed similar hemispheric effects related to deviations of gaze angle. We found no spatial effects for gaze in the vertical dimension.
Finger-movement independent gaze effects
We next identified brain regions that exhibited systematic gaze-related modulation of activation independent of finger-movement activation. For the horizontal regression [1 2 3] model, we identified only a single cluster that exhibited increasing activation as gaze deviated from left to right; the cluster was located in the occipital cortex (104 voxels; x = −13, y = 7, z = −1; max R2 = 0.24). The cluster in the occipital cortex found with the horizontal [1 2 3] model largely overlapped (81%; the remaining voxels formed a small cluster of 10 voxels and the rest of the 9 voxels were scattered; not shown) with a cluster in the occipital gyrus/lingual gyrus (BA18) activated according to the horizontal [1 2 2] model (). We also found 12 voxels in the left MFG that exhibited increasing activation as gaze deviated rightward. However, these voxels did not form a reliable and contiguous cluster since the activation of a single voxel in this region was slightly below (p = 0.0015) the rigorous statistical threshold (dark pink label in axial slices in ). We found four clusters with an activation pattern that conformed to the [1 2 2] horizontal model (, ). We found four activation clusters for the [1 2 2] model with two clusters located in an expanse of right visual cortex (, red label; on the coronal view they are separated by the dashed line) involving BA17, BA18, and BA19, the lingual and fusiform gyrus, and the right cuneus (most superior cluster). The analysis also revealed a cluster in the left pre-frontal cortex (BA46) and one in the right medial frontal gyrus (MFG, BA8; axial slices). also illustrates the locations of these clusters and corresponding overlap with those clusters showing activation conforming to the horizontal [1 2 3] model (red and yellow labels, respectively).
Cluster report for the horizontal regression analysis: [1 2 2] model
Fig. 4 Horizontal, vertical, and diagonal gaze effects. a Horizontal gaze effects: brain responses principally for horizontal gaze shifts showing activation in the frontal gyrus bilaterally and occipital cortex (see for all activated areas). Numbers (more ...)
Deviations in vertical gaze yielded systematic variation in activation independent of finger movement for 11 clusters, 6 that exhibited increased activation as gaze deviated increasingly downward and 5 clusters that showed more activation as gaze deviated increasingly upward (in , red and blue labels, respectively, ). From those five clusters with upward gaze effects, we found three adjacent clusters in the occipital cortex with one cluster located in the occipital gyrus extending superiorly to the pre-cuneus and SPL (BA18, 7; inferior saggital image) and two clusters in the left cuneus (BA18; most superior saggital image); they showed increasing activation as gaze shifted from the lower to the upper targets. We found two other clusters with this effect in the left IFG (BA10; not shown) and parahippocampal gyrus (37; axial image). The six activated clusters best related to downward gaze appeared in the parahippocampal formation (BA37; axial image) bilaterally and in the anterior orbito-frontal gyrus bilaterally (BA11; axial image) and medially (BA11; saggital image) and right fusiform gyrus (BA37; not shown).
Cluster report for the vertical regression analysis: [1 2 3] model
We also found activation that tracked linear gaze shifts along the diagonal of the target array. Application of the LL-UR regression model (; ) revealed seven clusters with two of these clusters exhibiting increased activation as gaze deviated progressively from the lower-left toward the upper-right portions of the visual workspace (, red label). We found a large activation cluster posteriorly and principally in the right hemisphere that involved the lingual gyrus, the cuneus, and the visual cortex (BA17, BA18, and BA19) and extended superiorly to the right SPL (BA7). There was also a cluster in the left cerebellum (CR-I) that showed the same effect. Clusters that exhibited increasing activation as gaze deviated from the upper-right toward the lower-left of the target array (, blue label) occurred bilaterally in the orbito-frontal gyrus (BA11; note that we found two clusters in each hemisphere) and the left parahippocampal gyrus (BA37). Finally, the UL-LR regression revealed four clusters (green labels) located in the orbito-frontal gyrus bilaterally (BA11), left superior temporal gyrus (BA38; not shown), and right lingual gyrus (BA18).
Cluster report for the LL-UR and UL-LR diagonal regressions analysis