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Attention alters orientation processing in the human lateral geniculate nucleus.

Ling S, Pratte MS, Tong F - Nat. Neurosci. (2015)

Bottom Line: Orientation selectivity is a cornerstone property of vision, commonly believed to emerge in the primary visual cortex.We found that reliable orientation information could be detected even earlier, in the human lateral geniculate nucleus, and that attentional feedback selectively altered these orientation responses.This attentional modulation may allow the visual system to modify incoming feature-specific signals at the earliest possible processing site.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Psychological and Brain Sciences, and the Center for Computational Neuroscience and Neural Technology, Boston University, Boston, Massachusetts, USA. [2] Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.

ABSTRACT
Orientation selectivity is a cornerstone property of vision, commonly believed to emerge in the primary visual cortex. We found that reliable orientation information could be detected even earlier, in the human lateral geniculate nucleus, and that attentional feedback selectively altered these orientation responses. This attentional modulation may allow the visual system to modify incoming feature-specific signals at the earliest possible processing site.

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Retinotopic preference for radial orientation and effects of orientation-specific masking in the human LGN and V1. a) Schematic of configurations used to test for radial bias. Functional localizers were used to determine voxels with retinotopic preference that fell along either the 45° or 135° axis (depicted by green shaded areas with diagonally opposing quadrants). We then presented a series of full-field gratings, which were oriented 45° or 135°. The relationship between localizer configuration and stimulus orientation determined the Collinear and Orthogonal conditions. b) Radial bias indices for mean BOLD responses in both LGN and V1. Higher positive values indicate larger radial biases. The results reveal that, in both V1 and LGN, the strength of the response depended critically on the match between the orientation of a stimulus, and the retinotopic preference of a region of interest. c) Illustration of stimuli used to test for orientation-tuned masking in LGN and V1. Stimuli were composed of linear sinusoidal gratings summed with orientation bandpass filtered noise. The noise orientation and grating were configured either collinear or orthogonal to each other. d) Orientation masking indices for mean BOLD responses in both LGN and V1 revealed that collinear stimuli had stronger suppression (lower BOLD response) than orthogonal stimuli. Error bars denote ±1 s.e.m.
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Figure 2: Retinotopic preference for radial orientation and effects of orientation-specific masking in the human LGN and V1. a) Schematic of configurations used to test for radial bias. Functional localizers were used to determine voxels with retinotopic preference that fell along either the 45° or 135° axis (depicted by green shaded areas with diagonally opposing quadrants). We then presented a series of full-field gratings, which were oriented 45° or 135°. The relationship between localizer configuration and stimulus orientation determined the Collinear and Orthogonal conditions. b) Radial bias indices for mean BOLD responses in both LGN and V1. Higher positive values indicate larger radial biases. The results reveal that, in both V1 and LGN, the strength of the response depended critically on the match between the orientation of a stimulus, and the retinotopic preference of a region of interest. c) Illustration of stimuli used to test for orientation-tuned masking in LGN and V1. Stimuli were composed of linear sinusoidal gratings summed with orientation bandpass filtered noise. The noise orientation and grating were configured either collinear or orthogonal to each other. d) Orientation masking indices for mean BOLD responses in both LGN and V1 revealed that collinear stimuli had stronger suppression (lower BOLD response) than orthogonal stimuli. Error bars denote ±1 s.e.m.

Mentions: The amount of orientation information we observed in LGN activity patterns was modest, when compared to the high classification performance of area V1. This was to be expected due to several factors, including broader orientation selectivity of LGN neurons, poorer quality of fMRI signals from subcortical than cortical regions10, and the relatively smaller size of the LGN structure. Nevertheless, we observe reliable orientation-selective responses in the human LGN, and these may arise from several sources. For example, animal studies have suggested that ganglion cell receptive fields are not uniformly circular13, but instead exhibit modest orientation preferences organized at both fine14 and coarse spatial scales14. To determine whether one such coarse-scale orientation bias, known as the radial bias, exists in the human LGN, we conducted an additional experiment to examine whether LGN responses depend on the correspondence between stimulus orientation and retinotopic preference15. LGN voxels were localized based on their retinotopic preference for either of the two diagonal radial axes (Fig. 2a), and mean BOLD responses were significantly greater for full-field gratings that were collinear rather than orthogonal to a voxel’s preferred radial axis (Fig. 2b, Supplementary Fig. 3, LGN: t(3) = 6.649, p = .003; V1: t(3) = 7.536; p = .002). These results indicate that the human LGN exhibits a coarse-scale preference for radial orientations, similar to what has been previously found in the human V1. In another experiment, we found that that the orientation of logarithmic spiral gratings could also be decoded from LGN activity patterns, indicating the presence of other sources of orientation preference in human LGN, distinct from radial bias16 (Supplementary Fig. 4).


Attention alters orientation processing in the human lateral geniculate nucleus.

Ling S, Pratte MS, Tong F - Nat. Neurosci. (2015)

Retinotopic preference for radial orientation and effects of orientation-specific masking in the human LGN and V1. a) Schematic of configurations used to test for radial bias. Functional localizers were used to determine voxels with retinotopic preference that fell along either the 45° or 135° axis (depicted by green shaded areas with diagonally opposing quadrants). We then presented a series of full-field gratings, which were oriented 45° or 135°. The relationship between localizer configuration and stimulus orientation determined the Collinear and Orthogonal conditions. b) Radial bias indices for mean BOLD responses in both LGN and V1. Higher positive values indicate larger radial biases. The results reveal that, in both V1 and LGN, the strength of the response depended critically on the match between the orientation of a stimulus, and the retinotopic preference of a region of interest. c) Illustration of stimuli used to test for orientation-tuned masking in LGN and V1. Stimuli were composed of linear sinusoidal gratings summed with orientation bandpass filtered noise. The noise orientation and grating were configured either collinear or orthogonal to each other. d) Orientation masking indices for mean BOLD responses in both LGN and V1 revealed that collinear stimuli had stronger suppression (lower BOLD response) than orthogonal stimuli. Error bars denote ±1 s.e.m.
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Related In: Results  -  Collection

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Figure 2: Retinotopic preference for radial orientation and effects of orientation-specific masking in the human LGN and V1. a) Schematic of configurations used to test for radial bias. Functional localizers were used to determine voxels with retinotopic preference that fell along either the 45° or 135° axis (depicted by green shaded areas with diagonally opposing quadrants). We then presented a series of full-field gratings, which were oriented 45° or 135°. The relationship between localizer configuration and stimulus orientation determined the Collinear and Orthogonal conditions. b) Radial bias indices for mean BOLD responses in both LGN and V1. Higher positive values indicate larger radial biases. The results reveal that, in both V1 and LGN, the strength of the response depended critically on the match between the orientation of a stimulus, and the retinotopic preference of a region of interest. c) Illustration of stimuli used to test for orientation-tuned masking in LGN and V1. Stimuli were composed of linear sinusoidal gratings summed with orientation bandpass filtered noise. The noise orientation and grating were configured either collinear or orthogonal to each other. d) Orientation masking indices for mean BOLD responses in both LGN and V1 revealed that collinear stimuli had stronger suppression (lower BOLD response) than orthogonal stimuli. Error bars denote ±1 s.e.m.
Mentions: The amount of orientation information we observed in LGN activity patterns was modest, when compared to the high classification performance of area V1. This was to be expected due to several factors, including broader orientation selectivity of LGN neurons, poorer quality of fMRI signals from subcortical than cortical regions10, and the relatively smaller size of the LGN structure. Nevertheless, we observe reliable orientation-selective responses in the human LGN, and these may arise from several sources. For example, animal studies have suggested that ganglion cell receptive fields are not uniformly circular13, but instead exhibit modest orientation preferences organized at both fine14 and coarse spatial scales14. To determine whether one such coarse-scale orientation bias, known as the radial bias, exists in the human LGN, we conducted an additional experiment to examine whether LGN responses depend on the correspondence between stimulus orientation and retinotopic preference15. LGN voxels were localized based on their retinotopic preference for either of the two diagonal radial axes (Fig. 2a), and mean BOLD responses were significantly greater for full-field gratings that were collinear rather than orthogonal to a voxel’s preferred radial axis (Fig. 2b, Supplementary Fig. 3, LGN: t(3) = 6.649, p = .003; V1: t(3) = 7.536; p = .002). These results indicate that the human LGN exhibits a coarse-scale preference for radial orientations, similar to what has been previously found in the human V1. In another experiment, we found that that the orientation of logarithmic spiral gratings could also be decoded from LGN activity patterns, indicating the presence of other sources of orientation preference in human LGN, distinct from radial bias16 (Supplementary Fig. 4).

Bottom Line: Orientation selectivity is a cornerstone property of vision, commonly believed to emerge in the primary visual cortex.We found that reliable orientation information could be detected even earlier, in the human lateral geniculate nucleus, and that attentional feedback selectively altered these orientation responses.This attentional modulation may allow the visual system to modify incoming feature-specific signals at the earliest possible processing site.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Psychological and Brain Sciences, and the Center for Computational Neuroscience and Neural Technology, Boston University, Boston, Massachusetts, USA. [2] Donders Institute for Brain, Cognition and Behavior, Radboud University, Nijmegen, The Netherlands.

ABSTRACT
Orientation selectivity is a cornerstone property of vision, commonly believed to emerge in the primary visual cortex. We found that reliable orientation information could be detected even earlier, in the human lateral geniculate nucleus, and that attentional feedback selectively altered these orientation responses. This attentional modulation may allow the visual system to modify incoming feature-specific signals at the earliest possible processing site.

Show MeSH
Related in: MedlinePlus