Vision of the Body Modulates Somatosensory Intracortical Inhibition
Flavia Cardini
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1
Matthew R. Longo
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Patrick Haggard
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0
Institute of Cognitive Neuroscience, University College London
,
London WC1N 3AR
,
UK
1
Centro Studi e Ricerche in Neuroscienze Cognitive, University of Bologna
,
Cesena 47023
,
Italy
The magnitude of somatosensory evoked potentials (SEPs) elicited by simultaneous electrical stimulation of adjacent digits is generally less than the sum of potentials evoked by stimulation of each digit individually. This under-additivity suggests suppression between representations of adjacent skin regions and may reflect a process of lateral inhibition by interneurons in somatosensory cortex. Given that simply viewing the body enhances tactile acuity and that tactile acuity depends on cortical lateral inhibition, we investigated how viewing the body modulates suppressive interactions between simultaneous afferent volleys from adjacent fingers. We recorded SEPs evoked by electrical stimulation of the right index and middle fingers, either individually or simultaneously, while participants viewed either their own hand or an object. In between trains of electrical stimuli, participants discriminated the orientation of tactile gratings applied to either finger. Consistent with previous findings, viewing the hand enhanced tactile acuity. Furthermore, viewing the hand increased the suppression of the P50 potential due to simultaneous electrical stimulation of both fingers. Moreover, the visual enhancement of tactile performance correlated across participants with the visual modulation of suppression. These results demonstrate that vision enhances somatosensation by modulating activity of inhibitory interneuronal circuits in the somatosensory cortex.
Introduction
The different senses do not work in isolation but interact in
several ways. Most research on multisensory perception has
focused on cases of convergence between inputs from
different sensory modalities, such as individual neurons that
respond to inputs from multiple modalities (Meredith and Stein
1983). A second, less investigated, form of multisensory
interaction occurs when activity from one sensory modality
modulates activity in another. Multisensory convergence can
be considered as a largely feedforward process in which
information from different sensory modalities is increasingly
pooled to generate supramodal representations. In contrast,
multisensory modulation involves either horizontal interactions
between different sensory pathways or top-down influences on
predominantly unimodal functions. Multisensory convergence
and multisensory interaction co-occur in many perceptual
situations. Here, we investigate the neural basis of a particular
form of multisensory modulation, in a case where the
contribution of feedforward convergence of multisensory input
can be excluded.
Simply viewing the body improves tactile perception,
relative to viewing an object in the same location, an effect
known as visual enhancement of touch (Kennett et al. 2001).
This effect does not result simply from feedforward
convergence of visual and tactile information since it occurs even
when vision is entirely noninformative about touch.
Explanations based on multisensory spatial attention are also
insufficient since the touched body part and the object were
made to appear at the same spatial location using an
arrangement of mirrors. Since vision provides no information
about the tactile stimulus, but only a multisensory context in
which tactile information occurs, such effects cannot simply be
explained as integration of tactile and visual information.
Rather, viewing the body seems to provide a visual cntext or
set that enhances tactile processing. This contextual
interpretation is further supported by the finding that visual
enhancement of touch (VET) persists for some seconds of
darkness after viewing the hand (Taylor-Clarke et al. 2004).
The neuronal mechanisms underlying contextual
multisensory enhancement remain unclear. Two previous studies
investigated the possible locus of the VET effect. Taylor-Clarke
et al. (2002) measured mechanical somatosensory evoked
potentials (SEPs) in a 2-point discrimination task while viewing
the arm or an object. They found that the N80 component was
enhanced while viewing the arm. This component has been
identified with a second wave of recurrent processing within
primary somatosensory cortex (SI; Allison et al. 1992). A similar
conclusion was reached by Fiorio and Haggard (2005), who
found that a single transcranial magnetic stimulation (TMS) pulse
over primary somatosensory cortex, during a brief dark interval
between vision and touch, abolished the visual enhancement of
touch. TMS over another area in the somatosensory pathway, SII,
was ineffective. These neurophysiological results receive further
support from the finding of Serino et al. (2009) that viewing the
hand also improves tactile discrimination not only on the hand
but also on the cheek. Since the overlap of hand and face
representa (...truncated)