Multiple frequency steady-state evoked magnetic field mapping of digit representation in primary somatosensory cortex

Magnetic source imaging of multiple frequency steady-state somatosensory evoked responses was examined using a 151-channel magnetoencephalography (MEG) system and a dual-channel electrical stimulator. Somatotopy of digit representation was studied in healthy subjects and effects of injury-related cortical plasticity in patients with unilateral transections of the median or the ulnar nerve. Dipole source locations exhibited somatotopic order with overlap between neighboring digits. In two of three nerve injury patients evidence for cortical reorganization was found. The location of sources related to digits neighboring deafferented digits was changed and their dipole moments were enlarged by comparsion with the sources related to contralateral homologue control digits. As a basis for magnetic source imaging, the recording of multiple frequency somatosensory steady-state evoked responses may be a viable and time saving alternative to the recording of transient evoked responses.     

Multiple frequency steady-state evoked magnetic field mapping of digit representation in primary somatosensory cortex

Magnetic source imaging of multiple frequency steady-state somatosensory evoked responses was examined using a 151-channel magnetoencephalography (MEG) system and a dual-channel electrical stimulator. Somatotopy of digit representation was studied in healthy subjects and effects of injury-related cortical plasticity in patients with unilateral transections of the median or the ulnar nerve. Dipole source locations exhibited somatotopic order with overlap between neighboring digits. In two of three nerve injury patients evidence for cortical reorganization was found. The location of sources related to digits neighboring deafferented digits was changed and their dipole moments were enlarged by comparsion with the sources related to contralateral homologue control digits. As a basis for magnetic source imaging, the recording of multiple frequency somatosensory steady-state evoked responses may be a viable and time saving alternative to the recording of transient evoked responses.     

Functional imaging of perceptual learning in human primary and secondary somatosensory cortex

Cellular mechanisms underlying synaptic plasticity are in line with the Hebbian concept. In contrast, data linking Hebbian learning to altered perception are rare. Combining functional magnetic resonance imaging with psychophysical tests, we studied cortical reorganization in primary and secondary somatosensory cortex (SI and SII) and the resulting changes of tactile perception before and after tactile coactivation, a simple type of Hebbian learning. Coactivation on the right index finger (IF) for 3 hr lowered its spatial discrimination threshold. In parallel, blood-oxygen level-dependent (BOLD) signals from the right IF representation in SI and SII enlarged. The individual threshold reduction was linearly correlated with the enlargement in SI, implying a close relation between altered discrimination and cortical reorganization. Controls consisting of a single-site stimulation did not affect thresholds and cortical maps. Accordingly, changes within distributed cortical networks based on Hebbian mechanisms alter the individual percept.     

Theta-burst stimulation-induced plasticity over primary somatosensory cortex changes somatosensory temporal discrimination in healthy humans

Background

The somatosensory temporal discrimination threshold (STDT) measures the ability to perceive two stimuli as being sequential. Precisely how the single cerebral structures contribute in controlling the STDT is partially known and no information is available about whether STDT can be modulated by plasticity-inducing protocols.

Methodology/Principal Findings

To investigate how the cortical and cerebellar areas contribute to the STDT we used transcranial magnetic stimulation and a neuronavigation system. We enrolled 18 healthy volunteers and 10 of these completed all the experimental sessions, including the control experiments. STDT was measured on the left hand before and after applying continuous theta-burst stimulation (cTBS) on the right primary somatosensory area (S1), pre-supplementary motor area (pre-SMA), right dorsolateral prefrontal cortex (DLPFC) and left cerebellar hemisphere. We then investigated whether intermittent theta-burst stimulation (iTBS) on the right S1 improved the STDT. After right S1 cTBS, STDT values increased whereas after iTBS to the same cortical site they decreased. cTBS over the DLPFC and left lateral cerebellum left the STDT statistically unchanged. cTBS over the pre-SMA also left the STDT statistically unchanged, but it increased the number of errors subjects made in distinguishing trials testing a single stimulus and those testing paired stimuli.

Conclusions/Significance

Our findings obtained by applying TBS to the cortical areas involved in processing sensory discrimination show that the STDT is encoded in S1, possibly depends on intrinsic S1 neural circuit properties, and can be modulated by plasticity-inducing TBS protocols delivered over S1. Our findings, giving further insight into mechanisms involved in somatosensory temporal discrimination, help interpret STDT abnormalities in movement disorders including dystonia and Parkinson''s disease.     

Close to you: embodied simulation for peripersonal space in primary somatosensory cortex

Background

An increasing body of evidence has demonstrated that in contrast to the classic understanding the primary somatosensory cortex (SI) reflects merely seen touch (in the absence of any real touch on the own body). Based on these results it has been discussed that SI may play a role in understanding touch seen on other bodies. In order to further examine this understanding of observed touch, the current study aimed to test if mirror-like responses in SI are affected by the perspective of the seen touch. Thus, we presented touch on a hand and close to the hand either in first-person-perspective or in third-person-perspective.

Principal Findings

Results of functional magnetic resonance imaging (fMRI) revealed stronger vicarious brain responses in SI/BA2 for touch seen in first-person-perspective. Surprisingly, the third-person viewpoint revealed activation in SI both when subjects viewed a hand being stimulated as well as when the space close to the hand was being touched.

Conclusions/Significance

Based on these results we conclude that vicarious somatosensory responses in SI/BA2 are affected by the viewpoint of the seen hand. Furthermore, we argue that mirror-like responses in SI do not only reflect seen touch, but also the peripersonal space surrounding this body (in third-person-perspective). We discuss these findings with recent studies on mirror responses for action observation in peripersonal space.     

Responses of neurons in cat primary somatosensory cortex to repetitive stimulation of vibrissae

Extra- and intracellular responses of neurons in the primary somatosensory cortex to repetitive mechanical stimulation of the vibrissae at different frequencies were studied in unanesthetized curarized adult cats. Unlike responses to electrical stimulation of the combined afferent input (the infraorbital nerve) spike discharges of neurons in response to vibrissal stimulation can reproduce rather higher frequencies of stimulation and their initial character changes more often in the course of the repetitive series. Most cortical neurons were characterized by limitation of the area of their peripheral receptive fields with an increase in the frequency of adequate repetitive stimulation. A group of cortical neurons was distinguished by its ability to respond to high-frequency stimulation and to generate burst discharges. Comparison of the frequency characteristics of spike responses of these cells and of inhibitory synaptic action in other cortical neurons led to the conclusion that this group of cells thus distinguished may be inhibitory cortical neurons. The role of interaction between excitatory and inhibitory processes arising in cortical neurons during repetitive stimulation of different areas of their receptive fields is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 14, No. 2, pp. 164–171, March–April, 1982.     

Millisecond-timescale local network coding in the rat primary somatosensory cortex

Correlation among neocortical neurons is thought to play an indispensable role in mediating sensory processing of external stimuli. The role of temporal precision in this correlation has been hypothesized to enhance information flow along sensory pathways. Its role in mediating the integration of information at the output of these pathways, however, remains poorly understood. Here, we examined spike timing correlation between simultaneously recorded layer V neurons within and across columns of the primary somatosensory cortex of anesthetized rats during unilateral whisker stimulation. We used bayesian statistics and information theory to quantify the causal influence between the recorded cells with millisecond precision. For each stimulated whisker, we inferred stable, whisker-specific, dynamic bayesian networks over many repeated trials, with network similarity of 83.3±6% within whisker, compared to only 50.3±18% across whiskers. These networks further provided information about whisker identity that was approximately 6 times higher than what was provided by the latency to first spike and 13 times higher than what was provided by the spike count of individual neurons examined separately. Furthermore, prediction of individual neurons' precise firing conditioned on knowledge of putative pre-synaptic cell firing was 3 times higher than predictions conditioned on stimulus onset alone. Taken together, these results suggest the presence of a temporally precise network coding mechanism that integrates information across neighboring columns within layer V about vibrissa position and whisking kinetics to mediate whisker movement by motor areas innervated by layer V.     

Restoration of contralateral representation in the mouse somatosensory cortex after crossing nerve transfer

Avulsion of spinal nerve roots in the brachial plexus (BP) can be repaired by crossing nerve transfer via a nerve graft to connect injured nerve ends to the BP contralateral to the lesioned side. Sensory recovery in these patients suggests that the contralateral primary somatosensory cortex (S1) is activated by afferent inputs that bypassed to the contralateral BP. To confirm this hypothesis, the present study visualized cortical activity after crossing nerve transfer in mice through the use of transcranial flavoprotein fluorescence imaging. In naïve mice, vibratory stimuli applied to the forepaw elicited localized fluorescence responses in the S1 contralateral to the stimulated side, with almost no activity in the ipsilateral S1. Four weeks after crossing nerve transfer, forepaw stimulation in the injured and repaired side resulted in cortical responses only in the S1 ipsilateral to the stimulated side. At eight weeks after crossing nerve transfer, forepaw stimulation resulted in S1 cortical responses of both hemispheres. These cortical responses were abolished by cutting the nerve graft used for repair. Exposure of the ipsilateral S1 to blue laser light suppressed cortical responses in the ipsilateral S1, as well as in the contralateral S1, suggesting that ipsilateral responses propagated to the contralateral S1 via cortico-cortical pathways. Direct high-frequency stimulation of the ipsilateral S1 in combination with forepaw stimulation acutely induced S1 bilateral cortical representation of the forepaw area in naïve mice. Cortical responses in the contralateral S1 after crossing nerve transfer were reduced in cortex-restricted heterotypic GluN1 (NMDAR1) knockout mice. Functional bilateral cortical representation was not clearly observed in genetically manipulated mice with impaired cortico-cortical pathways between S1 of both hemispheres. Taken together, these findings strongly suggest that activity-dependent potentiation of cortico-cortical pathways has a critical role for sensory recovery in patients after crossing nerve transfer.     

C-fibres provide a source of masking inhibition to primary somatosensory cortex.

Capsaicin was applied to the exposed radial nerve of adult flying foxes (n = 5) and cats (n = 2) while recording in primary somatosensory cortex from a single neuron with a receptive field on digits 1 or 2. Within four minutes of application of capsaicin the borders of these receptive fields dramatically expanded. In a further four flying foxes it was shown, with subcutaneous delivery just proximal to the receptive fields, that capsaicin need affect only afferents from the region of a neuron's receptive field to induce expansion. Capsaicin applied directly to a nerve, or subcutaneously in high concentrations, is a selective neurotoxin that rapidly prevents the propagation of action potentials in most C-fibres. The result provides a partial explanation for experiments involving the specific and complete denervation of receptive fields of neurons in primary somatosensory cortex. Such denervation does not lead to unresponsiveness but to immediate sensitivity to stimulation of areas surrounding the original fields. Thus it appears that some subclass of capsaicin-sensitive C-fibres provides a primary source for the masking inhibition that normally limits the extent of the receptive fields of cortical neurons.     

An examination of somatosensory area SIII in ferret cortex

A somatotopically organized region on the suprasylvian gyrus of the ferret was examined using multiunit recordings and anatomical tracer injections. This area, which contains a representation of the face, was bordered by the primary somatosensory area (SI), anteriorly, and by the visually responsive rostral posterior parietal cortex (PPr), posteriorly. Anatomical tracers revealed connections to this region from cortical areas MI, SI, MRSS, PPr, and the thalamic posterior nucleus. These results are consistent with previous work in ferrets as well as with the location, physiology, and connectivity of area SIII in cats. Given its associations, functional properties, location, and homology, it is proposed that this region represents the third cortical somatosensory area (SIII) in ferrets.     

Optical imaging of nociception in primary somatosensory cortex of non-human primates

While the activation of primary somatosensory (SI) cortex during pain perception is consistently reported in functional imaging studies on normal subjects and chronic pain patients, the specific roles of SI, particularly the subregions within SI, in the processing of sensory aspects of pain are still largely unknown. Using optical imaging of intrinsic signal (OIS) and single unit electrophysiology, we studied cortical activation patterns within SI cortex (among Brodmann areas 3a, 3b and 1) and signal amplitude changes to various intensities of non-nociceptive, thermal nociceptive and mechanical nociceptive stimulation of individual distal finerpads in anesthetized squirrel monkeys. We have demonstrated that areas 3a and 1 are preferentially involved in the processing of nociceptive information while areas 3b and 1 are preferentially activated in the processing of non-nociceptive (touch) information. Nociceptive activations of individual fingerpad were organized topographically suggesting that nociceptive topographic map exits in areas 3a and 1. Signal amplitude was enhanced to increasing intensity of mechanical nociceptive stimuli in areas 3a, 3b and 1. Within area 1, nociceptive response co-localizes with the non-nociceptive response. Therefore, we hypothesize that nocicepitve information is area-specifically represented within SI cortex, in which nociceptive inputs are preferentially represented in areas 3a and 1 while non-nociceptive inputs are preferentially represented in areas 3b and 1.     

A supramodal number representation in human intraparietal cortex

The triple-code theory of numerical processing postulates an abstract-semantic "number sense." Neuropsychology points to intraparietal cortex as a potential substrate, but previous functional neuroimaging studies did not dissociate the representation of numerical magnitude from task-driven effects on intraparietal activation. In an event-related fMRI study, we presented numbers, letters, and colors in the visual and auditory modality, asking subjects to respond to target items within each category. In the absence of explicit magnitude processing, numbers compared with letters and colors across modalities activated a bilateral region in the horizontal intraparietal sulcus. This stimulus-driven number-specific intraparietal response supports the idea of a supramodal number representation that is automatically accessed by presentation of numbers and may code magnitude information.     

Horseradish peroxidase-positive neurons of nonspecific thalamic nuclei projecting to the primary somatosensory cortex in cats

The morphology and topography of neurons whose axons form the nonspecific thalamic input in the primary somatosensory area were studied in the cat forebrain by the retrograde axonal horseradish peroxidase transport method. Stained cells were found in the dorsolateral part of the nucleus ventralis anterior, and were diffusely distributed in the nucleus centralis, lateralis, the lateral part of the nucleus dorsalis medialis, and the dorsal part of the centrum medianum. In the nucleus paracentralis only solitary, palely stained neurons were detected. Cells stained with horse-radish peroxidase were multipolar, triangular, or fusiform. The results are evidence that besides the ventrobasal complex, the nonspecific nuclei of the diencephalon also project into the somatosensory cortex. This indicates the existence of multiple afferent thalamic inputs into the somatic cortex.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 11, No. 5, pp. 435–440, September–October, 1979.     

Predicting spike occurrence and neuronal responsiveness from LFPs in primary somatosensory cortex

Local Field Potentials (LFPs) integrate multiple neuronal events like synaptic inputs and intracellular potentials. LFP spatiotemporal features are particularly relevant in view of their applications both in research (e.g. for understanding brain rhythms, inter-areal neural communication and neuronal coding) and in the clinics (e.g. for improving invasive Brain-Machine Interface devices). However the relation between LFPs and spikes is complex and not fully understood. As spikes represent the fundamental currency of neuronal communication this gap in knowledge strongly limits our comprehension of neuronal phenomena underlying LFPs. We investigated the LFP-spike relation during tactile stimulation in primary somatosensory (S-I) cortex in the rat. First we quantified how reliably LFPs and spikes code for a stimulus occurrence. Then we used the information obtained from our analyses to design a predictive model for spike occurrence based on LFP inputs. The model was endowed with a flexible meta-structure whose exact form, both in parameters and structure, was estimated by using a multi-objective optimization strategy. Our method provided a set of nonlinear simple equations that maximized the match between models and true neurons in terms of spike timings and Peri Stimulus Time Histograms. We found that both LFPs and spikes can code for stimulus occurrence with millisecond precision, showing, however, high variability. Spike patterns were predicted significantly above chance for 75% of the neurons analysed. Crucially, the level of prediction accuracy depended on the reliability in coding for the stimulus occurrence. The best predictions were obtained when both spikes and LFPs were highly responsive to the stimuli. Spike reliability is known to depend on neuron intrinsic properties (i.e. on channel noise) and on spontaneous local network fluctuations. Our results suggest that the latter, measured through the LFP response variability, play a dominant role.     

Contrast adaptation and representation in human early visual cortex

The human visual system can distinguish variations in image contrast over a much larger range than measurements of the static relationship between contrast and response in visual cortex would suggest. This discrepancy may be explained if adaptation serves to re-center contrast response functions around the ambient contrast, yet experiments on humans have yet to report such an effect. By using event-related fMRI and a data-driven analysis approach, we found that contrast response functions in V1, V2, and V3 shift to approximately center on the adapting contrast. Furthermore, we discovered that, unlike earlier areas, human V4 (hV4) responds positively to contrast changes, whether increments or decrements, suggesting that hV4 does not faithfully represent contrast, but instead responds to salient changes. These findings suggest that the visual system discounts slow uninformative changes in contrast with adaptation, yet remains exquisitely sensitive to changes that may signal important events in the environment.     

The representation of erroneously perceived stimuli in the primary visual cortex

In order to attain a correct interpretation of an ambiguous visual stimulus, the brain may have to elaborate on the sensory evidence. Are the neurons that carry the sensory evidence also involved in generating an interpretation? To address this question, we studied the activity of neurons in the primary visual cortex of macaque monkeys involved in a task in which they have to trace a curve mentally, without moving their eyes. On a percentage of trials, the monkeys made errors and traced the wrong curve. Here, we show that these errors are predicted by activity in area V1. Thus, neurons in the primary visual cortex do not only represent sensory events, but also the way in which they are interpreted by the monkey.     

Population coding in somatosensory cortex

Computational analyses have begun to elucidate which components of somatosensory cortical population activity may encode basic stimulus features. Recent results from rat barrel cortex suggest that the essence of this code is not synergistic spike patterns, but rather the precise timing of single neuron's first post-stimulus spikes. This may form the basis for a fast, robust population code.     

Interhemispheric interactions between the human primary somatosensory cortices

In the somatosensory domain it is still unclear at which processing stage information reaches the opposite hemispheres. Due to dense transcallosal connections, the secondary somatosensory cortex (S2) has been proposed to be the key candidate for interhemispheric information transfer. However, recent animal studies showed that the primary somatosensory cortex (S1) might as well account for interhemispheric information transfer. Using paired median nerve somatosensory evoked potential recordings in humans we tested the hypothesis that interhemispheric inhibitory interactions in the somatosensory system occur already in an early cortical processing stage such as S1. Conditioning right S1 by electrical median nerve (MN) stimulation of the left MN (CS) resulted in a significant reduction of the N20 response in the target (left) S1 relative to a test stimulus (TS) to the right MN alone when the interstimulus interval between CS and TS was between 20 and 25 ms. No such changes were observed for later cortical components such as the N20/P25, N30, P40 and N60 amplitude. Additionally, the subcortically generated P14 response in left S1 was also not affected. These results document the existence of interhemispheric inhibitory interactions between S1 in human subjects in the critical time interval of 20-25 ms after median nerve stimulation.     

Cell-type-specific recruitment of GABAergic interneurons in the primary somatosensory cortex by long-range inputs

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