Attention alters orientation processing in the human lateral geniculate nucleus

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.

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 null distribution in all conditions for every individual participant (24/24 cases), and that LGN decoding performance fell outside of the bounds of the null 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.

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.