Effects of Parietal TMS on Visual and Auditory Processing at the Primary Cortical Level – A Concurrent TMS-fMRI Study
Joana Leita o
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Axel Thielscher
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Sebastian Werner
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Rolf Pohmann
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Uta Noppeney
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Computational Neuroscience and Cognitive Robotics Centre, University of Birmingham
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Birmingham
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UK
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High-field Magnetic Resonance Centre, Max Planck Institute for Biological Cybernetics
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72076 Tu bingen
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Germany
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The Author 2012. Published by Oxford University Press. All rights reserved. For permissions
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please
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Cognitive Neuroimaging Group
Accumulating evidence suggests that multisensory interactions emerge already at the primary cortical level. Specifically, auditory inputs were shown to suppress activations in visual cortices when presented alone but amplify the blood oxygen level--dependent (BOLD) responses to concurrent visual inputs (and vice versa). This concurrent transcranial magnetic stimulation--functional magnetic resonance imaging (TMS-fMRI) study applied repetitive TMS trains at no, low, and high intensity over right intraparietal sulcus (IPS) and vertex to investigate top-down influences on visual and auditory cortices under 3 sensory contexts: visual, auditory, and no stimulation. IPS-TMS increased activations in auditory cortices irrespective of sensory context as a result of direct and nonspecific auditory TMS side effects. In contrast, IPS-TMS modulated activations in the visual cortex in a state-dependent fashion: it deactivated the visual cortex under no and auditory stimulation but amplified the BOLD response to visual stimulation. However, only the response amplification to visual stimulation was selective for IPS-TMS, while the deactivations observed for IPS- and VertexTMS resulted from crossmodal deactivations induced by auditory activity to TMS sounds. TMS to IPS may increase the responses in visual (or auditory) cortices to visual (or auditory) stimulation via a gain control mechanism or crossmodal interactions. Collectively, our results demonstrate that understanding TMS effects on (uni)sensory processing requires a multisensory perspective.
Introduction
Multisensory integration was traditionally thought to be deferred
until later processing stages in higher order association cortices.
Recent evidence from neuroanatomy, electrophysiology and
functional imaging in humans, nonhuman primates, and other
species suggests that sensory inputs interact already at the
primary, putatively unisensory, cortical level (Macaluso and Driver
2005; Schroeder and Foxe 2005; Ghazanfar and Schroeder 2006).
Specifically, in human functional imaging studies, the effect of
inputs from the nonpreferred sensory modality on activations in
primary sensory cortices depends on the presence or absence of
concurrent sensory inputs from the preferred modality (Laurienti
et al. 2002; Johnson and Zatorre 2005). For instance, auditory
inputs suppressed activations in visual cortices when presented
alone but amplified the blood oxygen level--dependent (BOLD)
response to concurrent visual inputs (and vice versa). In other
words, competitive interactions (=crossmodal deactivations)
between sensory cortices for unisensory stimulation mutated
into cooperative interactions (=superadditive response
enhancement) for multisensory stimulation (Werner and Noppeney
2010a, 2011).
The neural mechanisms that mediate these inhibitory and
excitatory audiovisual interactions at the primary cortical
level are currently unclear. Several functional architectures
have been proposed such as feedforward thalamocortical,
direct connectivity between sensory areas, and feedback from
higher order association areas such as the intraparietal sulcus
(IPS) or the superior temporal sulcus (Calvert 2001; Schroeder
et al. 2003; Beauchamp et al. 2004; Hackett et al. 2007; Driver
and Noesselt 2008; Sadaghiani et al. 2009). Recent
electroencephalography and transcranial magnetic stimulation (TMS)
studies have supported thalamocortical and direct mechanisms
by demonstrating multisensory interactions at less than 100 ms
poststimulus (Foxe et al. 2000; Molholm et al. 2002; Murray
et al. 2005; Romei et al. 2007; Cappe et al. 2010; Raij et al.
2010). Yet, given the sluggishness of the BOLD response,
functional magnetic resonance imaging (fMRI) activations in
primary sensory cortices may reflect a compound of early and
late interactions. Indeed, a recent study combining fMRI and
effective connectivity analyses (i.e., dynamic causal modeling)
suggested that low-level audiovisual interactions may be
mediated by both direct/thalamocortical influences and
top-down effects from higher order association areas (Werner
and Noppeney 2010a). From a cognitive perspective, these
top-down effects may also reflect crossmodal modulation of
attentional resources (Shomstein and Yantis 2004; Johnson
and Zatorre 2005, 2006; Werner and Noppeney 2011). Thus,
the IPS with its connectivity to visual or auditory cortices
(Hyvarinen 1982; Maunsell and van Essen 1983; Boussaoud
et al. 1990; Lewis and Van Essen 2000a) has been implicated
in crossmodal attentional s (...truncated)