The multisensory attentional consequences of tool use : a functional magnetic resonance imaging study

Background: Tool use in humans requires that multisensory information is integrated across different locations, from objects seen to be distant from the hand, but felt indirectly at the hand via the tool. We tested the hypothesis that using a simple tool to perceive vibrotactile stimuli results in the enhanced processing of visual stimuli presented at the distal, functional part of the tool. Such a finding would be consistent with a shift of spatial attention to the location where the tool is used. Methodology/Principal Findings: We tested this hypothesis by scanning healthy human participants’ brains using functional magnetic resonance imaging, while they used a simple tool to discriminate between target vibrations, accompanied by congruent or incongruent visual distractors, on the same or opposite side to the tool. The attentional hypothesis was supported: BOLD response in occipital cortex, particularly in the right hemisphere lingual gyrus, varied significantly as a function of tool position, increasing contralaterally, and decreasing ipsilaterally to the tool. Furthermore, these modulations occurred despite the fact that participants were repeatedly instructed to ignore the visual stimuli, to respond only to the vibrotactile stimuli, and to maintain visual fixation centrally. In addition, the magnitude of multisensory (visual-vibrotactile) interactions in participants’ behavioural responses significantly predicted the BOLD response in occipital cortical areas that were also modulated as a function of both visual stimulus position and tool position. Conclusions/Significance: These results show that using a simple tool to locate and to perceive vibrotactile stimuli is accompanied by a shift of spatial attention to the location where the functional part of the tool is used, resulting in enhanced processing of visual stimuli at that location, and decreased processing at other locations. This was most clearly observed in the right hemisphere lingual gyrus. Such modulations of visual processing may reflect the functional importance of visuospatial information during human tool use

The in vivo functional neuroanatomy and neurochemistry of vibrotactile processing

Touch is a sense with which humans are able to actively explore the world around them. Primary somatosensory cortex (S1) processing has been studied to differing degrees at both the macroscopic and microscopic levels in both humans and animals. Both levels of enquiry have their advantages, but attempts to combine the two approaches are still in their infancy. One mechanism that is possibly involved in determining the reponse properties of neurons that are involved in sensory discrimination is inhibition by γ-aminobutyric acid (GABA). Several studies have shown that inhibition is an important mechanism to “tune” the response of neurons. Recently it has become possible to measure the concentration of GABA in vivo using edited Magnetic Resonance Spectroscopy (MRS), whereas magnetoencephalography (MEG) offers the possibility to look at changes in neuromagnetic activation with millisecond accuracy. With these methods we aimed to establish whether in vivo non-invasive neuroimaging can elucidate the underlying neuronal mechanisms of human tactile behaviour and to determine how such findings can be integrated with what is currently known from invasive methods. Edited GABA-MRS has shown that individual GABA concentration in S1 correlates strongly with tactile frequency discrimination. MEG was used to investigate the neuromagnetic correlates of a frequency discrimination paradigm in which we induced adaptation to a 25 Hz frequency. We showed that S1 is driven by the adapting stimulus and shows that neural rhythms are modulated as a result of adaptation. This is the first time that behavioural psychophysics of tactile adaptation has been investigated using complimentary neuroimaging methods. We combined different methods to complement both physiological and behavioural studies of tactile processing in S1 to investigate the factors involved in the neural dynamics of tactile processing and we show that non-invasive studies on humans can be used to understand physiological underpinnings of somatosensory processing.EThOS - Electronic Theses Online ServiceGBUnited Kingdo

The in vivo functional neuroanatomy and neurochemistry of vibrotactile processing

Touch is a sense with which humans are able to actively explore the world around them. Primary somatosensory cortex (S1) processing has been studied to differing degrees at both the macroscopic and microscopic levels in both humans and animals. Both levels of enquiry have their advantages, but attempts to combine the two approaches are still in their infancy. One mechanism that is possibly involved in determining the reponse properties of neurons that are involved in sensory discrimination is inhibition by γ-aminobutyric acid (GABA). Several studies have shown that inhibition is an important mechanism to “tune” the response of neurons. Recently it has become possible to measure the concentration of GABA in vivo using edited Magnetic Resonance Spectroscopy (MRS), whereas magnetoencephalography (MEG) offers the possibility to look at changes in neuromagnetic activation with millisecond accuracy. With these methods we aimed to establish whether in vivo non-invasive neuroimaging can elucidate the underlying neuronal mechanisms of human tactile behaviour and to determine how such findings can be integrated with what is currently known from invasive methods. Edited GABA-MRS has shown that individual GABA concentration in S1 correlates strongly with tactile frequency discrimination. MEG was used to investigate the neuromagnetic correlates of a frequency discrimination paradigm in which we induced adaptation to a 25 Hz frequency. We showed that S1 is driven by the adapting stimulus and shows that neural rhythms are modulated as a result of adaptation. This is the first time that behavioural psychophysics of tactile adaptation has been investigated using complimentary neuroimaging methods. We combined different methods to complement both physiological and behavioural studies of tactile processing in S1 to investigate the factors involved in the neural dynamics of tactile processing and we show that non-invasive studies on humans can be used to understand physiological underpinnings of somatosensory processing

Synaptic Plasticity by Afferent Electrical Stimulation

The effect of afferent electrical stimulation on synaptic plasticity within the sensorimotor cortex will be discussed. Afferent electrical stimulation induces a down regulation of inhibitory neural circuits and plays a critical role in strengthening excitatory synapses. Synaptic modifications such as long-term potentiation (LTP) mechanisms could be a crucial mechanism underlying this stimulation-induced cortical plasticity. LTP and long-term depression (LTD) of synaptic transmission are crucial factors for activity-dependent changes in the strength of synaptic connections. Many studies demonstrated that these pathways play an important role in cortical synaptic plasticity. Repeated activation of excitatory synapses induces both short-term potentiation (STP) and LTP. Both types of synaptic potentiation affect N-methyl-D-aspartate glutamate receptors leading to the formation of new synapses or the unmasking of excitatory amino acid receptors on motor neurons. This increased excitability localized within the sensorimotor cortex may reflect an increase in neuronal activity as a result of a dynamic interaction of various synaptic and cellular mechanisms due to the local processing of afferent electrical input to the sensorimotor cortex. The chapter reviews also the large number of studies using fMRI and TMS to examine the effects of afferent electrical input from the hand on the excitability of human sensorimotor cortex

Functional Connectivity Evoked by Orofacial Tactile Perception of Velocity

The cortical representations of orofacial pneumotactile stimulation involve complex neuronal networks, which are still unknown. This study aims to identify the characteristics of functional connectivity (FC) evoked by three different saltatory velocities over the perioral and buccal surface of the lower face using functional magnetic resonance imaging in twenty neurotypical adults. Our results showed a velocity of 25 cm/s evoked stronger connection strength between the right dorsolateral prefrontal cortex and the right thalamus than a velocity of 5 cm/s. The decreased FC between the right secondary somatosensory cortex and right posterior parietal cortex for 5-cm/s velocity versus all three velocities delivered simultaneously (“All ON”) and the increased FC between the right thalamus and bilateral secondary somatosensory cortex for 65 cm/s vs “All ON” indicated that the right secondary somatosensory cortex might play a role in the orofacial tactile perception of velocity. Our results have also shown different patterns of FC for each seed (bilateral primary and secondary somatosensory cortex) at various velocity contrasts (5 vs 25 cm/s, 5 vs 65 cm/s, and 25 vs 65 cm/s). The similarities and differences of FC among three velocities shed light on the neuronal networks encoding the orofacial tactile perception of velocity

Cortical cross-modal plasticity following deafness measured using functional near-infrared spectroscopy

Evidence from functional neuroimaging studies suggests that the auditory cortex can become more responsive to visual and somatosensory stimulation following deafness, and that this occurs predominately in the right hemisphere. Extensive cross-modal plasticity in prospective cochlear implant recipients is correlated with poor speech outcomes following implantation, highlighting the potential impact of central auditory plasticity on subsequent aural rehabilitation. Conversely, the effects of hearing restoration with a cochlear implant on cortical plasticity are less well understood, since the use of most neuroimaging techniques in CI recipients is either unsafe or problematic due to the electromagnetic artefacts generated by CI stimulation. Additionally, techniques such as functional magnetic resonance imaging (fMRI) are confounded by acoustic noise produced by the scanner that will be perceived more by hearing than by deaf individuals. Subsequently it is conceivable that auditory responses to acoustic noise produced by the MR scanner may mask auditory cortical responses to non-auditory stimulation, and render inter-group comparisons less significant. Uniquely, functional near-infrared spectroscopy (fNIRS) is a silent neuroimaging technique that is non-invasive and completely unaffected by the presence of a CI. Here, we used fNIRS to study temporal-lobe responses to auditory, visual and somatosensory stimuli in thirty profoundly-deaf participants and thirty normally-hearing controls. Compared with silence, acoustic noise stimuli elicited a significant group fNIRS response in the temporal region of normally-hearing individuals, which was not seen in profoundly-deaf participants. Visual motion elicited a larger group response within the right temporal lobe of profoundly-deaf participants, compared with normally-hearing controls. However, bilateral temporal lobe fNIRS activation to somatosensory stimulation was comparable in both groups. Using fNIRS these results confirm that auditory deprivation is associated with cross-modal plasticity of visual inputs to auditory cortex. Although we found no evidence for plasticity of somatosensory inputs, it is possible that our recordings may have included activation of somatosensory cortex that masked any group differences in auditory cortical responses due to the limited spatial resolution associated with fNIRS

Functional deficits in carpal tunnel syndrome reflect reorganization of primary somatosensory cortex

Carpal tunnel syndrome, a median nerve entrapment neuropathy, is characterized by sensorimotor deficits. Recent reports have shown that this syndrome is also characterized by functional and structural neuroplasticity in the primary somatosensory cortex of the brain. However, the linkage between this neuroplasticity and the functional deficits in carpal tunnel syndrome is unknown. Sixty-three subjects with carpal tunnel syndrome aged 20–60 years and 28 age- and sex-matched healthy control subjects were evaluated with event-related functional magnetic resonance imaging at 3 T while vibrotactile stimulation was delivered to median nerve innervated (second and third) and ulnar nerve innervated (fifth) digits. For each subject, the interdigit cortical separation distance for each digit’s contralateral primary somatosensory cortex representation was assessed. We also evaluated fine motor skill performance using a previously validated psychomotor performance test (maximum voluntary contraction and visuomotor pinch/release testing) and tactile discrimination capacity using a four-finger forced choice response test. These biobehavioural and clinical metrics were evaluated and correlated with the second/third interdigit cortical separation distance. Compared with healthy control subjects, subjects with carpal tunnel syndrome demonstrated reduced second/third interdigit cortical separation distance (P < 0.05) in contralateral primary somatosensory cortex, corroborating our previous preliminary multi-modal neuroimaging findings. For psychomotor performance testing, subjects with carpal tunnel syndrome demonstrated reduced maximum voluntary contraction pinch strength (P < 0.01) and a reduced number of pinch/release cycles per second (P < 0.05). Additionally, for four-finger forced-choice testing, subjects with carpal tunnel syndrome demonstrated greater response time (P < 0.05), and reduced sensory discrimination accuracy (P < 0.001) for median nerve, but not ulnar nerve, innervated digits. Moreover, the second/third interdigit cortical separation distance was negatively correlated with paraesthesia severity (r = −0.31, P < 0.05), and number of pinch/release cycles (r = −0.31, P < 0.05), and positively correlated with the second and third digit sensory discrimination accuracy (r = 0.50, P < 0.05). Therefore, reduced second/third interdigit cortical separation distance in contralateral primary somatosensory cortex was associated with worse symptomatology (particularly paraesthesia), reduced fine motor skill performance, and worse sensory discrimination accuracy for median nerve innervated digits. In conclusion, primary somatosensory cortex neuroplasticity for median nerve innervated digits in carpal tunnel syndrome is indeed maladaptive and underlies the functional deficits seen in these patients