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Effective connectivity during animacy perception--dynamic causal modelling of Human Connectome Project data.

Hillebrandt H, Friston KJ, Blakemore SJ - Sci Rep (2014)

Bottom Line: Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion.We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion.These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute of Cognitive Neuroscience, University College London, London, WC1N 3AR, United Kingdom [2] Moral Cognition Laboratory, Department of Psychology, Harvard University, Cambridge, MA, 02138, United States.

ABSTRACT
Biological agents are the most complex systems humans have to model and predict. In predictive coding, high-level cortical areas inform sensory cortex about incoming sensory signals, a comparison between the predicted and actual sensory feedback is made, and information about unpredicted sensory information is passed forward to higher-level areas. Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion. We tested this hypothesis by investigating effective connectivity in a large-scale fMRI dataset from the Human Connectome Project. 132 participants viewed animations of triangles that were designed to move in a way that appeared animate (moving intentionally), or inanimate (moving in a mechanical way). We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion. These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies.

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(A) Brain map showing the left and right V5 VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location. (B) Brain map showing the left and right pSTS VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location.
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f3: (A) Brain map showing the left and right V5 VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location. (B) Brain map showing the left and right pSTS VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location.

Mentions: To identify and summarise regional responses for further dynamic causal modelling we used standard procedures37. Timeseries from VOIs associated with the above contrasts were summarised using the SPM12b Eigenvariate toolbox: we extracted each participant's principal eigenvariate around the participant-specific local maxima activations nearest to the peak voxel of the group (between subject) GLM analysis (see Table 1 and 2). The radii of the VOI spheres were 6 mm and the search radii for local maxima from the group analysis were restricted to 20 mm. All voxels contributing to the eigenvariates were significant at p < 0.05 uncorrected and adjusted at p < 0.05 for the effects of interest (i.e. only for those regressors that were used in the DCMs for input or modulation). In order to replicate the results across sessions and hemispheres, we created separate DCMs for each hemisphere and each of the two sessions (four DCMs overall), which were then analysed together with repeated measures ANOVAs (see Figure 2B for a schematic of the model and Figure 4 for the results aggregated across participants, hemispheres and sessions). For each model, the first volume of interest (VOI) was based on maxima in the most active cluster of the All motion contrast (which was Animate and Inanimate motion over the implicit fixation baseline). These maxima were assigned by the SPM anatomy toolbox38 to MT+/V5 (sometimes called human occipital lobe area 5 (hOC5); right: 44 −64 4; left: −44 −74 4; see Table 1 and 2 for GLM results. Figure 3A and 3B show brain maps of the means of the extracted voxels of individual participants.). V5 was the most active region in our All Motion contrast, and has been shown to be highly sensitive to visual motion12. The second VOI was extracted at the local maxima of the most active clusters in each hemisphere based on the results of a conjunction analysis3940. A conjunction of activations allows one to infer a co-occurrence of several effects in one area40: an activation map of a conjunction analysis will show those voxels as significant that would be significant in the two conjoined effects. The conjunction used here was the effect of the contrast [All Motion > Fixation Cross] & (logical AND) the contrast [Animate > Inanimate Motion] – i.e. [All motion > Fixation cross & Animate – inanimate motion]. The conjunction was performed to consider areas more active in Animate vs. Inanimate motion, but only in motion sensitive areas (activated by any type of motion). We used the more conservative test, testing against the conjunction , instead of testing against the global 40. The second VOI was extracted from the pSTS (sometimes called inferior parietal cortex (IPC; more specifically PGa and PFm), right: 54 −50 16; left: −56 −52 10). The pSTS was highly active bilaterally: the peaks were local maxima in the most active cluster of each hemisphere with t-values above 8. The pSTS has been frequently implicated in animate motion processing (see discussion). Note that V5 was not significantly more active in this contrast, which might suggest that the stimuli were indeed well matched in terms of low-level motion properties. Finally, V5 and the pSTS have been shown to have strong (and reciprocal) anatomical connectivity41.


Effective connectivity during animacy perception--dynamic causal modelling of Human Connectome Project data.

Hillebrandt H, Friston KJ, Blakemore SJ - Sci Rep (2014)

(A) Brain map showing the left and right V5 VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location. (B) Brain map showing the left and right pSTS VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150124&req=5

f3: (A) Brain map showing the left and right V5 VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location. (B) Brain map showing the left and right pSTS VOIs. The colour gradient bar indicates how many participants had the mean of their extracted voxels at a given location.
Mentions: To identify and summarise regional responses for further dynamic causal modelling we used standard procedures37. Timeseries from VOIs associated with the above contrasts were summarised using the SPM12b Eigenvariate toolbox: we extracted each participant's principal eigenvariate around the participant-specific local maxima activations nearest to the peak voxel of the group (between subject) GLM analysis (see Table 1 and 2). The radii of the VOI spheres were 6 mm and the search radii for local maxima from the group analysis were restricted to 20 mm. All voxels contributing to the eigenvariates were significant at p < 0.05 uncorrected and adjusted at p < 0.05 for the effects of interest (i.e. only for those regressors that were used in the DCMs for input or modulation). In order to replicate the results across sessions and hemispheres, we created separate DCMs for each hemisphere and each of the two sessions (four DCMs overall), which were then analysed together with repeated measures ANOVAs (see Figure 2B for a schematic of the model and Figure 4 for the results aggregated across participants, hemispheres and sessions). For each model, the first volume of interest (VOI) was based on maxima in the most active cluster of the All motion contrast (which was Animate and Inanimate motion over the implicit fixation baseline). These maxima were assigned by the SPM anatomy toolbox38 to MT+/V5 (sometimes called human occipital lobe area 5 (hOC5); right: 44 −64 4; left: −44 −74 4; see Table 1 and 2 for GLM results. Figure 3A and 3B show brain maps of the means of the extracted voxels of individual participants.). V5 was the most active region in our All Motion contrast, and has been shown to be highly sensitive to visual motion12. The second VOI was extracted at the local maxima of the most active clusters in each hemisphere based on the results of a conjunction analysis3940. A conjunction of activations allows one to infer a co-occurrence of several effects in one area40: an activation map of a conjunction analysis will show those voxels as significant that would be significant in the two conjoined effects. The conjunction used here was the effect of the contrast [All Motion > Fixation Cross] & (logical AND) the contrast [Animate > Inanimate Motion] – i.e. [All motion > Fixation cross & Animate – inanimate motion]. The conjunction was performed to consider areas more active in Animate vs. Inanimate motion, but only in motion sensitive areas (activated by any type of motion). We used the more conservative test, testing against the conjunction , instead of testing against the global 40. The second VOI was extracted from the pSTS (sometimes called inferior parietal cortex (IPC; more specifically PGa and PFm), right: 54 −50 16; left: −56 −52 10). The pSTS was highly active bilaterally: the peaks were local maxima in the most active cluster of each hemisphere with t-values above 8. The pSTS has been frequently implicated in animate motion processing (see discussion). Note that V5 was not significantly more active in this contrast, which might suggest that the stimuli were indeed well matched in terms of low-level motion properties. Finally, V5 and the pSTS have been shown to have strong (and reciprocal) anatomical connectivity41.

Bottom Line: Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion.We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion.These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute of Cognitive Neuroscience, University College London, London, WC1N 3AR, United Kingdom [2] Moral Cognition Laboratory, Department of Psychology, Harvard University, Cambridge, MA, 02138, United States.

ABSTRACT
Biological agents are the most complex systems humans have to model and predict. In predictive coding, high-level cortical areas inform sensory cortex about incoming sensory signals, a comparison between the predicted and actual sensory feedback is made, and information about unpredicted sensory information is passed forward to higher-level areas. Predictions about animate motion - relative to inanimate motion - should result in prediction error and increase signal passing from lower level sensory area MT+/V5, which is responsive to all motion, to higher-order posterior superior temporal sulcus (pSTS), which is selectively activated by animate motion. We tested this hypothesis by investigating effective connectivity in a large-scale fMRI dataset from the Human Connectome Project. 132 participants viewed animations of triangles that were designed to move in a way that appeared animate (moving intentionally), or inanimate (moving in a mechanical way). We found that forward connectivity from V5 to the pSTS increased, and inhibitory self-connection in the pSTS decreased, when viewing intentional motion versus inanimate motion. These prediction errors associated with animate motion may be the cause for increased attention to animate stimuli found in previous studies.

Show MeSH