Demonstration of Tuning to Stimulus Orientation in the Human Visual Cortex: A High-Resolution fMRI Study with a Novel Continuous and Periodic Stimulation Paradigm

Cerebral Cortex, Jul 2013

Cells in the animal early visual cortex are sensitive to contour orientations and form repeated structures known as orientation columns. At the behavioral level, there exist 2 well-known global biases in orientation perception (oblique effect and radial bias) in both animals and humans. However, their neural bases are still under debate. To unveil how these behavioral biases are achieved in the early visual cortex, we conducted high-resolution functional magnetic resonance imaging experiments with a novel continuous and periodic stimulation paradigm. By inserting resting recovery periods between successive stimulation periods and introducing a pair of orthogonal stimulation conditions that differed by 90° continuously, we focused on analyzing a blood oxygenation level-dependent response modulated by the change in stimulus orientation and reliably extracted orientation preferences of single voxels. We found that there are more voxels preferring horizontal and vertical orientations, a physiological substrate underlying the oblique effect, and that these over-representations of horizontal and vertical orientations are prevalent in the cortical regions near the horizontal- and vertical-meridian representations, a phenomenon related to the radial bias. Behaviorally, we also confirmed that there exists perceptual superiority for horizontal and vertical orientations around horizontal and vertical meridians, respectively. Our results, thus, refined the neural mechanisms of these 2 global biases in orientation perception.

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Demonstration of Tuning to Stimulus Orientation in the Human Visual Cortex: A High-Resolution fMRI Study with a Novel Continuous and Periodic Stimulation Paradigm

Pei Sun 2 Justin L. Gardner 1 Mauro Costagli 2 3 Kenichi Ueno 0 R. Allen Waggoner 2 Keiji Tanaka 2 Kang Cheng 0 2 0 Support Unit for Functional Magnetic Resonance Imaging, RIKEN Brain Science Institute , 2-1 Hirosawa, Wako, Saitama 351-0198, Japan 1 Gardner Research Unit 2 RIKEN Brain Science Institute , 2-1 Hirosawa, Wako, Saitama 351-0198, Japan 3 Fondazione IMAGO7, IRCCS Stella Maris, Viale del Tirreno 341/ABC, Pisa , Calambrone 56128, Italy Cells in the animal early visual cortex are sensitive to contour orientations and form repeated structures known as orientation columns. At the behavioral level, there exist 2 well-known global biases in orientation perception (oblique effect and radial bias) in both animals and humans. However, their neural bases are still under debate. To unveil how these behavioral biases are achieved in the early visual cortex, we conducted high-resolution functional magnetic resonance imaging experiments with a novel continuous and periodic stimulation paradigm. By inserting resting recovery periods between successive stimulation periods and introducing a pair of orthogonal stimulation conditions that differed by 90 continuously, we focused on analyzing a blood oxygenation leveldependent response modulated by the change in stimulus orientation and reliably extracted orientation preferences of single voxels. We found that there are more voxels preferring horizontal and vertical orientations, a physiological substrate underlying the oblique effect, and that these over-representations of horizontal and vertical orientations are prevalent in the cortical regions near the horizontal- and vertical-meridian representations, a phenomenon related to the radial bias. Behaviorally, we also confirmed that there exists perceptual superiority for horizontal and vertical orientations around horizontal and vertical meridians, respectively. Our results, thus, refined the neural mechanisms of these 2 global biases in orientation perception. Introduction Cells in the early visual cortex in many species of animals are sensitive to contour orientations (Hubel and Wiesel 1962, 1968). Using functional magnetic resonance imaging (fMRI), preferences for stimulus orientation have also been inferred (Tootell, Hadjikhani, Vanduffel et al. 1998; Boynton and Finney 2003; Fang et al. 2005; Liu et al. 2006; Serences et al. 2009; Weigelt et al. 2012) and decoded (Haynes and Rees 2005; Kamitani and Tong 2005; Harrison and Tong 2009; Swisher et al. 2010) in the human visual cortex. Orientation preferences are continuously represented, forming repeated structures known as orientation columns (Blasdel and Salama 1986; Grinvald et al. 1986). High-resolution fMRI has been successfully used for visualizing orientation columns in cats (Kim et al. 2000; Duong et al. 2001; Fukuda et al. 2006; Moon et al. 2007) and humans (Yacoub et al. 2008). At the behavioral level, there are 2 well-known global biases in orientation perception. One is the oblique effect, referring to the observation that both humans and animals have a greater behavioral sensitivity to the gratings of cardinal (horizontal and vertical) orientations than to the gratings of oblique orientations (Appelle 1972). The other is the radial bias, describing a biased sensitivity to radial orientations at particular angles (Sasaki et al. 2006; Freeman et al. 2011). However, it is still unclear how these behavioral superiorities for certain orientations are achieved within the early visual cortex. Alternative neural mechanisms have been hypothesized, with one proposing that the more cortical area is devoted to achieve this superiority (e.g. Maffei and Campbell 1970), and the other suggesting that stronger neuronal responses could be the source (e.g. Mansfield and Ronner 1978). In comparison to numerous animal single-unit and optical imaging studies, human fMRI studies so far have provided only limited evidence that can contribute to this debate, as blood oxygenation level-dependent (BOLD) responses to different orientations were compared with relatively coarse spatial resolutions in the previous studies (e.g. Furmanski and Engel 2000; Sasaki et al. 2006; Mannion et al. 2009, 2010; Freeman et al. 2011). Thus, it is necessary to address these issues at higher spatial resolutions, preferentially at the columnar (sub-millimeter) resolutions. Furthermore, to deal with the increased scan time that accompanies the high-resolution fMRI approaches, it is desirable to utilize more efficient stimulation paradigms (in comparison with traditional, time-consuming block designs) so that orientation preferences at the singlevoxel level can be revealed within a limited experimental time. A continuous stimulation paradigm, in which a grating rotates continuously, thus covering all orientations over a short period of time, has been used to reveal orientationtuning properties of single voxels in high-resolution fMRI studies (Fukuda et al. 2006; Moon et al. 2007; Yacoub et al. (...truncated)


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Pei Sun, Justin L. Gardner, Mauro Costagli, Kenichi Ueno, R. Allen Waggoner, Keiji Tanaka, Kang Cheng. Demonstration of Tuning to Stimulus Orientation in the Human Visual Cortex: A High-Resolution fMRI Study with a Novel Continuous and Periodic Stimulation Paradigm, Cerebral Cortex, 2013, pp. 1618-1629, 23/7, DOI: 10.1093/cercor/bhs149