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Feedback of visual object information to foveal retinotopic cortex - PubMed

. 2008 Dec;11(12):1439-45.

doi: 10.1038/nn.2218. Epub 2008 Nov 2.

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Feedback of visual object information to foveal retinotopic cortex

Mark A Williams et al. Nat Neurosci. 2008 Dec.

Abstract

The mammalian visual system contains an extensive web of feedback connections projecting from higher cortical areas to lower areas, including primary visual cortex. Although multiple theories have been proposed, the role of these connections in perceptual processing is not understood. We found that the pattern of functional magnetic resonance imaging response in human foveal retinotopic cortex contained information about objects presented in the periphery, far away from the fovea, which has not been predicted by prior theories of feedback. This information was position invariant, correlated with perceptual discrimination accuracy and was found only in foveal, but not peripheral, retinotopic cortex. Our data cannot be explained by differential eye movements, activation from the fixation cross, or spillover activation from peripheral retinotopic cortex or from lateral occipital complex. Instead, our findings indicate that position-invariant object information from higher cortical areas is fed back to foveal retinotopic cortex, enhancing task performance.

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Competing Interests Statement

The authors declare that they have no competing financial interests.

Figures

Figure 1
Figure 1

A) A single exemplar from each of the three stimulus categories; for information on the slight variations across exemplars in each category see . B) Example of the presentation display with identical ‘smoothies’ present in the top left and bottom right quadrants (left diagonal). C) Example of the presentation display with different ‘smoothies’ present in the top right and bottom left quadrants (right diagonal). Objects had a mean width of 1. 8° visual angle and were presented 7° from fixation.

Figure 2
Figure 2

ROIs in one example subject. A) Native functional slices 4 to 15 (see Methods), with this subject’s functionally-defined ROIs in color: lateral occipital complex (LOC; Objects>Scrambled from localiser experiment) in yellow, foveal retinotopic cortex (All>Rest from the Localiser runs, including active voxels only at the occipital poles) in red, and peripheral retinotopic ROIs (smoothies, spikies, cubies > rest from half the experimental runs) in blue; in each analysis, the union of two peripheral (blue) regions constitute the Same Location ROI (the cortical region corresponding to the location where the stimuli occur, e.g. in the upper right and lower left visual field) and the union of the two other peripheral (blue) regions constitute the Different Location ROI (the cortical region corresponding to the location where stimuli occur in the other stimulus location condition, e.g. upper left and lower right). B) Inflated cortical surface from the same subject showing the location of these retinotopic ROIs on the cortical surface (inflation was performed using Freesurfer 34).

Figure 3
Figure 3

Mean correlations (± 1 SE) for same (black bars) versus different (grey bars) categories and for same versus different locations for the four ROIs in Experiment 1. A) Lateral Occipital Complex (LOC; objects>scrambled objects); B) Object Location ROI is the region of the peripheral retinotopic cortex corresponding to the location where the stimuli occur; C) Between Locations ROI is a peripheral retinotopic region corresponding to the gap between stimulus locations; D) The Foveal Region in retinotopic cortex (Foveal; central object presentation > fixation).

Figure 4
Figure 4

Mean correlations (± 1 SE) within- and between-categories (always between locations) for two ROIs in Experiment 2. Three subjects participated in this experiment, which was identical to Experiment 1 except that no central fixation was presented. A) Lateral Occipital Complex (LOC; objects>scrambled objects); B) The foveal representation in retinotopic cortex (Foveal; central object presentation>fixation).

Figure 5
Figure 5

ROIs in one example subject and the corresponding mean correlations. A) Inflated cortical surface with this subject’s functionally-defined ROIs in color: Outer Ring (Object Location; Outer Ring>Middle Ring) in blue, Middle Ring (Middle Ring > Outer Ring + Foveal Ring) in green and; Foveal retinotopic cortex (Foveal Ring>Mddle Ring) in red, on the cortical surface (inflation was performed using Freesurfer 34). B) Mean correlations (± 1 SE) within- and between-categories (always between locations) for three ROIs in Experiment 3. Five subjects participated in this experiment, which was identical to Experiment 1 except that a checkerboard eccentricity mapping and meridian mapping were conducted.

Figure 6
Figure 6

Correlations within and between categories (always between locations) for LOC and the foveal retinotopic cortex in Experiment 4, showing that task modulates object information more strongly in the foveal ROI than in LOC. A) Results from the Object Discrimination task showing object information in both LOC and foveal retinotopic cortex; B) Results from the Color Task demonstrating object category information in LOC but not in foveal retinotopic cortex.

Figure 7
Figure 7. Time course and behavioral relevance of position-invariant information in foveal retinotopic ROI in Experiments 1 and 4

A) Top graph: Time course of appearance of object category information (Between Locations) across each block, for foveal ROI, LOC, and Object Location ROI; each time bin represents two trials and four seconds. Bottom graph: Corresponding behavioral data collected from the same subjects during scanning, showing that performance increases across trials within a block, mirroring the increase in category information in the foveal ROI. B) Scatterplots showing the correlation across subjects between the amount of increase in performance from the beginning to the end of blocks, and the increase in the amount of object information in each ROI. Note that only for foveal retinotopic cortex is category information correlated with behavioral performance.

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