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A Cross-Modal System Linking Primary Auditory and Visual Cortices: Evidence from Intrinsic Fmri Connectivity Analysis

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A Cross-Modal System Linking Primary Auditory and Visual Cortices: Evidence from Intrinsic Fmri Connectivity Analysis r Human Brain Mapping 29:848–857 (2008) r A Cross-Modal System Linking Primary Auditory and Visual Cortices: Evidence From Intrinsic fMRI Connectivity Analysis Mark A. Eckert,1* Nirav V. Kamdar,2 Catherine E. Chang,3 Christian F. Beckmann,4 Michael D. Greicius,2,5 and Vinod Menon2,6 1Department of Otolaryngology, Medical University of South Carolina, Charleston, South Carolina 2Department of Psychiatry, Stanford University Medical Center, Stanford, California 3Department of Electrical Engineering, Stanford University Medical Center, Stanford, California 4Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford, United Kingdom 5Department of Neurology and Neurological Sciences, Stanford University Medical Center, Stanford, California 6Neurosciences Program, Stanford University Medical Center, Stanford, California Abstract: Recent anatomical and electrophysiological evidence in primates indicates the presence of direct connections between primary auditory and primary visual cortex that constitute cross-modal sys- tems. We examined the intrinsic functional connectivity (fcMRI) of putative primary auditory cortex in 32 young adults during resting state scanning. We found that the medial Heschl’s gyrus was strongly coupled, in particular, to visual cortex along the anterior banks of the calcarine fissure. This observa- tion was confirmed using novel group-level, tensor-based independent components analysis. fcMRI analysis revealed that although overall coupling between the auditory and visual cortex was signifi- cantly reduced when subjects performed a visual perception task, coupling between the anterior calcar- ine cortex and auditory cortex was not disrupted. These results suggest that primary auditory cortex has a functionally distinct relationship with the anterior visual cortex, which is known to represent the peripheral visual field. Our study provides novel, fcMRI-based, support for a neural system involving low-level auditory and visual cortices. Hum Brain Mapp 29:848–857, 2008. VC 2008 Wiley-Liss, Inc. Key words: functional connectivity; cross-modal; multisensory; primary auditory cortex; primary visual cortex This article contains supplementary material available via the *Correspondence to: Mark A. Eckert, Department of Otolaryngol- Internet at http://www.interscience.wiley.com/jpages/1065-9471/ ogy/Research, Medical University of South Carolina, 135 Rutledge suppmat Avenue, P.O. Box 550, Charleston, SC 29425. E-mail: [email protected] Contract grant sponsor: National Institutes of Health; Contract grant numbers: MH19938, MH01142, HD31715, HD40761, NS048302, Received for publication 13 July 2007; Accepted 1 February 2008 MH62430, HD33113, HD047520, NS058899; Contract grant sponsor: DOI: 10.1002/hbm.20560 National Center for Research Resources; Contract grant number: C06 Published online 15 April 2008 in Wiley InterScience (www. RR014516; Contract grant sponsor: National Science Foundation; interscience.wiley.com). Contract grant number: BCS0449927, BCS-0449927; Contract grant sponsors: Alzheimer’s Association, Sinclair Fund. VC 2008 Wiley-Liss, Inc. r APrimary Auditory-Visual System r INTRODUCTION Together, the findings from functional and anatomical studies of cross-modal connections suggest there are Historically, sensory cortex has been characterized as locally specific regions of low-level sensory cortex that hierarchical with association cortex providing the linkage engages in cross-modal processing through direct connec- between sensory systems [Todd, 1912]. More recently there tions with other low-level sensory regions, as well as influ- is tract tracing, electrophysiology, and neuroimaging evi- ences through association cortex. In particular, the tract dence for direct connections between low-level sensory cor- tracing studies suggest that functional connectivity should tex [Brosch et al., 2005; Cappe and Barone, 2005; Clavagnier be most prominent between medial Heschl’s gyrus and an- et al., 2004; Falchier et al., 2002; Foxe et al., 2002; Ghazanfar terior calcarine regions. et al., 2005; Johnson and Zatorre, 2006; Kayser et al., 2005; fcMRI is a functional-imaging method that can be used Laurienti et al., 2002; Lehmann et al., 2006; Martuzzi et al., to examine the strength of functional connectivity 2007; Nir et al., 2006; Rockland and Ojima, 2003; Rockland between two anatomical regions during tasks and when and Van Hoesen, 1994; Schroeder and Foxe, 2005; Tanabe subjects are not given a specific task or when there is not et al., 2005; Watkins et al., 2006]. The cross-modal results attention demanding task. fcMRI has been used to exam- across neuroimaging experiments generally fall into two ine tonically active sensory, motor, and cognitive net- classes in which low level sensory interactions can be works observed in resting state data [Biswal et al., 1997; attributed to (1) indirect interactions because of the influ- Greicius et al., 2003]. These studies have highlighted ence of association cortex and (2) direct connections robust coupling between homologous regions across the between sensory cortices. cerebral hemispheres [Salvador et al., 2005]. For example, The majority of neuroimaging studies involving multi- left and right hemisphere auditory cortices demonstrate sensory experiments demonstrate that association cortex highly correlated patterns of activity [van de Ven et al., drives the interactions between sensory cortex. Posterior 2004]. In this fcMRI study we used regions-of-interest association and frontal lobe cortex appear to influence (ROIs), defined by each individual’s unique anatomy, to low-level multisensory processing in functional imaging identify the functional pathways associated with low- studies requiring attention to a sensory stimulus [Calvert level primary auditory cortex during the resting state. In et al., 2000; Macaluso et al., 2000] and high cognitive load addition to characterizing auditory pathways in resting [Crottaz-Herbette et al., 2004; Johnson and Zatorre, 2007], state data, we asked whether auditory and visual cortex respectively. For example, Macaluso et al. [2000] demon- would exhibit positively correlated activity when there strated that activity in multisensory parietal lobe cortex was no specific task, and whether these regions would was selectively correlated with activity in occipital cortex exhibit negatively correlated activity when subjects were when tactile stimuli were observed to elicit increased occipi- engaged in a visual task. tal responses to a visual stimulus, suggesting that parietal lobe cortex was responsible for the occipital cortex responses to tactile stimuli. In addition, cross-modal inhibition between MATERIALS AND METHODS sensory cortices has been observed when the cognitive load Participants is high (e.g., a two-back working memory task), suggesting the occurrence of top-down inhibitory control by executive Thirty-two Stanford University students (17 female) function systems [Crottaz-Herbette et al., 2004]. were recruited for functional imaging tasks over a 4-year Evidence that association cortex and prefrontal cortex period (mean age 21.12, 62.10 years). Fourteen of these drive low-level multisensory interactions does not pre- participants also performed a visual perception task. These clude, however, that there are direct interactions between studies were approved by the Stanford University Institu- low-level sensory cortex. Evidence for direct connections tional Review Board and these tasks were undertaken with between low-level sensory cortices has been reported in the understanding and written assent and/or consent of anatomical tracing and electrophysiological studies. Ana- each subject. tomical tracer studies of nonhuman primates demonstrate the existence of direct pathways between primary sensory fMRI Paradigms areas [Cappe and Barone, 2005; Clavagnier et al., 2004; Falchier et al., 2002; Rockland and Ojima, 2003; Rockland During a resting state scan participants were instructed and Van Hoesen, 1994]. For example, neurons in nonhu- to lay quietly with their eyes closed. The length of the man primate auditory cortex have projections that termi- scan was 4 min. The visual processing task consisted of nate in the anterior but not posterior regions of primary the presentation of a static black-and-white radial checker- visual cortex [Falchier et al., 2002; Rockland and Ojima, board pattern and a ‘‘flashing’’ checkerboard, in which the 2003]. In addition, electrophysiological studies demonstrate white and black patterns were inverted with an 8 Hz fre- cross-modal processing in low-level sensory cortex at time quency. The visual stimulus angle subtended by the periods well before association cortex could possibly checkerboard was 18.98. Presentation of the static and respond to a stimulus and drive the response [Giard and flashing stimuli alternated every 20 s for six cycles. In Peronnet, 1999]. both conditions, subjects were instructed to passively r 849 r r Eckert et al. r view the checkerboard. The total length of the task was 4 a second-level, single-sample t-test analysis (height thresh- min. old of FDR P < 0.05 and an extent threshold of P < 0.01) to determine the brain areas that showed significant func- Image Acquisition tional connectivity across subjects. Functional images of the adults were acquired on a 3T General Electric Signa scanner by using a standard General Anatomical Regions of Interest Electric whole-head coil. The scanner runs on an LX plat- form, with gradients in ‘‘miniCRM’’ configuration
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