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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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Attention selectively augments orientation representation in the human LGN. a) LGN region of interest in a representative subject, identified by the intersection (green) of functional localizers (orange) and proton density-weighted structural imaging (blue). b) Accuracy of orientation decoding (d’ units) for multivariate activity patterns in LGN and V1, for attended and unattended gratings. Attention led to enhanced orientation-selective responses in V1 for all orientation conditions, whereas in the LGN only oblique orientations were modulated by attention. Oblique and cardinal orientation pairs were tested on different scan sessions. Individual points correspond to individual subjects. A non-parametric permutation test confirmed that V1 decoding performance fell outside of the 95% CI bounds of the  distribution in all conditions for every individual participant (24/24 cases), and that LGN decoding performance fell outside of the bounds of the  in 12/12 cases in the attended condition, and 9/12 cases for the unattended condition. c) Attention had comparable effects on mean BOLD activity across orientations, in both the LGN and V1. BOLD response was normalized by the mean intensity across the time series for each run. d) Attentional modulation indices (AMI) for decoding performance of oblique (green) and cardinal (blue) orientations, in LGN and V1. Higher positive values indicate larger effects of attention. Whereas attentional modulation was comparable for cardinal and oblique orientations in area V1, attention selectively modulated responses to oblique orientations in the LGN. Error bars denote ±1 s.e.m.
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Figure 1: Attention selectively augments orientation representation in the human LGN. a) LGN region of interest in a representative subject, identified by the intersection (green) of functional localizers (orange) and proton density-weighted structural imaging (blue). b) Accuracy of orientation decoding (d’ units) for multivariate activity patterns in LGN and V1, for attended and unattended gratings. Attention led to enhanced orientation-selective responses in V1 for all orientation conditions, whereas in the LGN only oblique orientations were modulated by attention. Oblique and cardinal orientation pairs were tested on different scan sessions. Individual points correspond to individual subjects. A non-parametric permutation test confirmed that V1 decoding performance fell outside of the 95% CI bounds of the distribution in all conditions for every individual participant (24/24 cases), and that LGN decoding performance fell outside of the bounds of the in 12/12 cases in the attended condition, and 9/12 cases for the unattended condition. c) Attention had comparable effects on mean BOLD activity across orientations, in both the LGN and V1. BOLD response was normalized by the mean intensity across the time series for each run. d) Attentional modulation indices (AMI) for decoding performance of oblique (green) and cardinal (blue) orientations, in LGN and V1. Higher positive values indicate larger effects of attention. Whereas attentional modulation was comparable for cardinal and oblique orientations in area V1, attention selectively modulated responses to oblique orientations in the LGN. Error bars denote ±1 s.e.m.

Mentions: Our first goal was to determine whether viewed orientation could be successfully classified from voxel activity patterns in the LGN. We localized the LGN region of interest in individual participants using a combination of functional11,12 and anatomical localization methods (Fig. 1a & Supplementary Fig. 1a). Our pattern analysis results indicated that reliable orientation information was present not only in V1, but in the human LGN, as well (Fig. 1b; all p’s<0.01). Next, we asked whether the top-down effects of attentional feedback might influence orientation-selective responses in the LGN. To do so, we measured the extent to which attention improved orientation classification performance, separately for oblique and cardinal orientations, based on the hypothesis that cortical feedback might selectively bolster the representation of oblique orientations in the LGN5. We observed a significant interaction between the effects of attentional modulation, orientation, and visual area on classification performance, F(4,40) = 5.51, p = 0.001. In V1, attention increased the strength of orientation responses for both oblique and cardinal orientations (Fig. 1b, all p’s < .01) to a comparable extent, t(5) = 0.39, p = 0.71. In the LGN, however, the attentional effect was significantly greater for oblique orientations than for cardinal orientations (Fig. 1b; t(5) = 4.76, p = 0.002). Specifically, the withdrawal of attentional feedback led to substantially weaker orientation-selective activity patterns for oblique orientations in the LGN, but had no reliable effect on cardinal orientations (Fig. 1d). The qualitatively different pattern of results observed in the LGN and V1 suggests that a distinct type of feature-selective modulation is occurring in the LGN, leading to the selective enhancement of oblique orientations (Supplementary Figs. 1b & 2).


Attention alters orientation processing in the human lateral geniculate nucleus.

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

Attention selectively augments orientation representation in the human LGN. a) LGN region of interest in a representative subject, identified by the intersection (green) of functional localizers (orange) and proton density-weighted structural imaging (blue). b) Accuracy of orientation decoding (d’ units) for multivariate activity patterns in LGN and V1, for attended and unattended gratings. Attention led to enhanced orientation-selective responses in V1 for all orientation conditions, whereas in the LGN only oblique orientations were modulated by attention. Oblique and cardinal orientation pairs were tested on different scan sessions. Individual points correspond to individual subjects. A non-parametric permutation test confirmed that V1 decoding performance fell outside of the 95% CI bounds of the  distribution in all conditions for every individual participant (24/24 cases), and that LGN decoding performance fell outside of the bounds of the  in 12/12 cases in the attended condition, and 9/12 cases for the unattended condition. c) Attention had comparable effects on mean BOLD activity across orientations, in both the LGN and V1. BOLD response was normalized by the mean intensity across the time series for each run. d) Attentional modulation indices (AMI) for decoding performance of oblique (green) and cardinal (blue) orientations, in LGN and V1. Higher positive values indicate larger effects of attention. Whereas attentional modulation was comparable for cardinal and oblique orientations in area V1, attention selectively modulated responses to oblique orientations in the LGN. Error bars denote ±1 s.e.m.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4556110&req=5

Figure 1: Attention selectively augments orientation representation in the human LGN. a) LGN region of interest in a representative subject, identified by the intersection (green) of functional localizers (orange) and proton density-weighted structural imaging (blue). b) Accuracy of orientation decoding (d’ units) for multivariate activity patterns in LGN and V1, for attended and unattended gratings. Attention led to enhanced orientation-selective responses in V1 for all orientation conditions, whereas in the LGN only oblique orientations were modulated by attention. Oblique and cardinal orientation pairs were tested on different scan sessions. Individual points correspond to individual subjects. A non-parametric permutation test confirmed that V1 decoding performance fell outside of the 95% CI bounds of the distribution in all conditions for every individual participant (24/24 cases), and that LGN decoding performance fell outside of the bounds of the in 12/12 cases in the attended condition, and 9/12 cases for the unattended condition. c) Attention had comparable effects on mean BOLD activity across orientations, in both the LGN and V1. BOLD response was normalized by the mean intensity across the time series for each run. d) Attentional modulation indices (AMI) for decoding performance of oblique (green) and cardinal (blue) orientations, in LGN and V1. Higher positive values indicate larger effects of attention. Whereas attentional modulation was comparable for cardinal and oblique orientations in area V1, attention selectively modulated responses to oblique orientations in the LGN. Error bars denote ±1 s.e.m.
Mentions: Our first goal was to determine whether viewed orientation could be successfully classified from voxel activity patterns in the LGN. We localized the LGN region of interest in individual participants using a combination of functional11,12 and anatomical localization methods (Fig. 1a & Supplementary Fig. 1a). Our pattern analysis results indicated that reliable orientation information was present not only in V1, but in the human LGN, as well (Fig. 1b; all p’s<0.01). Next, we asked whether the top-down effects of attentional feedback might influence orientation-selective responses in the LGN. To do so, we measured the extent to which attention improved orientation classification performance, separately for oblique and cardinal orientations, based on the hypothesis that cortical feedback might selectively bolster the representation of oblique orientations in the LGN5. We observed a significant interaction between the effects of attentional modulation, orientation, and visual area on classification performance, F(4,40) = 5.51, p = 0.001. In V1, attention increased the strength of orientation responses for both oblique and cardinal orientations (Fig. 1b, all p’s < .01) to a comparable extent, t(5) = 0.39, p = 0.71. In the LGN, however, the attentional effect was significantly greater for oblique orientations than for cardinal orientations (Fig. 1b; t(5) = 4.76, p = 0.002). Specifically, the withdrawal of attentional feedback led to substantially weaker orientation-selective activity patterns for oblique orientations in the LGN, but had no reliable effect on cardinal orientations (Fig. 1d). The qualitatively different pattern of results observed in the LGN and V1 suggests that a distinct type of feature-selective modulation is occurring in the LGN, leading to the selective enhancement of oblique orientations (Supplementary Figs. 1b & 2).

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