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.
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