Human Primary Somatosensory Cortex Research Articles

Metaplasticity in human primary somatosensory cortex: effects on physiology and tactile perception

Metaplasticity in human primary somatosensory cortex: effects on physiology and tactile perception

Individual left-hand and right-hand intra-digit representations in human primary somatosensory cortex.

Individual intra-digit somatotopy of all phalanges of the middle and little finger of the right and left hand was studied by functional magnetic resonance imaging in 12 healthy subjects. Phalanges were tactilely stimulated and activation in BA 3b of the human primary somatosensory cortex could be observed for each individual phalanx. Activation peaks were further analysed using the Direction/Order (DiOr) method, which identifies somatotopy, if a significantly high number of subjects exhibit ordered distal-to-proximal phalanx representions along a similar direction. Based on DiOr, ordered and similar-direction-aligned intra-digit maps across subjects were found at the left hand for the little and middle finger and at the right hand for the little finger. In these digits the proximal phalanges were represented more medially along the course of the central sulcus than the distal phalanges. This is contrasted by the intra-digit maps for the middle finger of the right hand, which showed larger inter-subject variations of phalanx alignments without a similar within-digit representation across subjects. As all subjects were right-handed and as the middle finger of the dominant hand probably plays a more individual role in everyday tactile performance than the little finger of the right hand and all left-hand digits, the observed variation might reflect a functional somatotopy based on individual use of that particular digit at the dominant hand.

Image-guided transcranial focused ultrasound stimulates human primary somatosensory cortex.

Focused ultrasound (FUS) has recently been investigated as a new mode of non-invasive brain stimulation, which offers exquisite spatial resolution and depth control. We report on the elicitation of explicit somatosensory sensations as well as accompanying evoked electroencephalographic (EEG) potentials induced by FUS stimulation of the human somatosensory cortex. As guided by individual-specific neuroimage data, FUS was transcranially delivered to the hand somatosensory cortex among healthy volunteers. The sonication elicited transient tactile sensations on the hand area contralateral to the sonicated hemisphere, with anatomical specificity of up to a finger, while EEG recordings revealed the elicitation of sonication-specific evoked potentials. Retrospective numerical simulation of the acoustic propagation through the skull showed that a threshold of acoustic intensity may exist for successful cortical stimulation. The neurological and neuroradiological assessment before and after the sonication, along with strict safety considerations through the individual-specific estimation of effective acoustic intensity in situ and thermal effects, showed promising initial safety profile; however, equal/more rigorous precautionary procedures are advised for future studies. The transient and localized stimulation of the brain using image-guided transcranial FUS may serve as a novel tool for the non-invasive assessment and modification of region-specific brain function.

Seeing is not feeling: posterior parietal but not somatosensory cortex engagement during touch observation.

Observing touch has been reported to elicit activation in human primary and secondary somatosensory cortices and is suggested to underlie our ability to interpret other's behavior and potentially empathy. However, despite these reports, there are a large number of inconsistencies in terms of the precise topography of activation, the extent of hemispheric lateralization, and what aspects of the stimulus are necessary to drive responses. To address these issues, we investigated the localization and functional properties of regions responsive to observed touch in a large group of participants (n = 40). Surprisingly, even with a lenient contrast of hand brushing versus brushing alone, we did not find any selective activation for observed touch in the hand regions of somatosensory cortex but rather in superior and inferior portions of neighboring posterior parietal cortex, predominantly in the left hemisphere. These regions in the posterior parietal cortex required the presence of both brush and hand to elicit strong responses and showed some selectivity for the form of the object or agent of touch. Furthermore, the inferior parietal region showed nonspecific tactile and motor responses, suggesting some similarity to area PFG in the monkey. Collectively, our findings challenge the automatic engagement of somatosensory cortex when observing touch, suggest mislocalization in previous studies, and instead highlight the role of posterior parietal cortex.

Individual fMRI maps of all phalanges and digit bases of all fingers in human primary somatosensory cortex.

This study determined the individual maps of all fingers in Brodmann area 3b of the human primary somatosensory cortex in a single fMRI session by tactile stimulation at 19 sites across all phalanges and digit bases of the 5 right-hand digits. To quantify basic features of the digit maps within and across subjects, we applied standard descriptive measures, but also implemented a novel quantitative analysis. This so-called Direction/Order (DiOr) method tested whether subjects exhibited an ordering of peak fMRI representations along their individual direction of alignment through the set of analyzed phalanges and whether these individual directions were similar across subjects. Across-digit analysis demonstrated that for each set of homologous phalanges, the D5-to-D1 representations were successively represented along a common direction of alignment. Hence, the well-known mediolateral D5-to-D1 somatotopy was not only confirmed for the distal phalanges (p1), but could also be shown for the medial (p2) and proximal phalanges (p3). In contrast, the peak activation for the digit bases (p4) only partly elicited that digit succession. Complementary, intra-digit analysis revealed a divergent picture of map topography for the different digits. Within D5 (and in a trend: D4), an ordered p1-to-p3 succession was found across subjects, pointing to a consistent intra-digit somatotopy for D5, with p3 generally found medial-posterior to p1. In contrast, for D1, D2, and D3, most subjects did not present with ordered p1-to-p3 maps nor were directions of alignment similarly oriented between subjects. These digits therefore exhibited highly diverse representation patterns across subjects.

Depicting the inner and outer nose: The representation of the nose and the nasal mucosa on the human primary somatosensory cortex (SI)

The nose is important not only for breathing, filtering air, and perceiving olfactory stimuli. Although the face and hands have been mapped, the representation of the internal and external surface of the nose on the primary somatosensory cortex (SI) is still poorly understood. To fill this gap functional magnetic resonance imaging (fMRI) was used to localize the nose and the nasal mucosa in the Brodman areas (BAs) 3b, 1, and 2 of the human postcentral gyrus (PG). Tactile stimulation during fMRI was applied via a customized pneumatically driven device to six stimulation sites: the alar wing of the nose, the lateral nasal mucosa, and the hand (serving as a reference area) on the left and right side of the body. Individual representations could be discriminated for the left and right hand, for the left nasal mucosa and left alar wing of the nose in BA 3b and BA 1 by comparing mean activation maxima and Euclidean distances. Right-sided nasal conditions and conditions in BA 2 could further be separated by different Euclidean distances. Regarding the alar wing of the nose, the results concurred with the classic sensory homunculus proposed by Penfield and colleagues. The nasal mucosa was not only determined an individual and bilateral representation, its position on the somatosensory cortex is also situated closer to the caudal end of the PG compared to that of the alar wing of the nose and the hand. As SI is commonly activated during the perception of odors, these findings underscore the importance of the knowledge of the representation of the nasal mucosa on the primary somatosensory cortex, especially for interpretation of results of functional imaging studies about the sense of smell.

Functional parcellation of the human primary somatosensory cortex to natural touch

Despite the significance of human touch, brain responses to interpersonal manual touch have been rarely investigated. We used functional magnetic resonance imaging to study brain activity in eight healthy adults whose left hand was touched by two individuals, in separate runs and in 20-s blocks, either by holding, smoothing, or poking. Acceleration was measured from both the subject's and the touching person's hands for postimaging control of the stimuli. Independent component analysis of the functional magnetic resonance imaging data unraveled three functional networks involving the primary somatosensory cortex (SI). One network comprised the contralateral and another the ipsilateral Brodmann area 3. The third network included area 2 bilaterally, left-hemisphere middle temporal gyrus and dorsolateral prefrontal regions, ventral prefrontal cortices bilaterally, and middle cingulate cortex. The response shapes and polarities varied between the three networks. The contralateral area 3 differentiated the responses between the three types of touch stimuli, and the response magnitudes depended on the variability of the touch within each block. However, the responses of the other two networks were strikingly similar to all stimuli. The subjects' reports on the pleasantness of the touch did not correlate with the characteristics of the SI responses. These findings imply area-specific processing of the natural human touch in three networks including the SI cortex, with only area 2 connected to a functional network of brain areas that may support social interaction.

Transcranial focused ultrasound modulates the activity of primary somatosensory cortex in humans

Improved methods of noninvasively modulating human brain function are needed. Here we probed the influence of transcranial focused ultrasound (tFUS) targeted to the human primary somatosensory cortex (S1) on sensory-evoked brain activity and sensory discrimination abilities. The lateral and axial spatial resolution of the tFUS beam implemented were 4.9 mm and 18 mm, respectively. Electroencephalographic recordings showed that tFUS significantly attenuated the amplitudes of somatosensory evoked potentials elicited by median nerve stimulation. We also found that tFUS significantly modulated the spectral content of sensory-evoked brain oscillations. The changes produced by tFUS on sensory-evoked brain activity were abolished when the acoustic beam was focused 1 cm anterior or posterior to S1. Behavioral investigations showed that tFUS targeted to S1 enhanced performance on sensory discrimination tasks without affecting task attention or response bias. We conclude that tFUS can be used to focally modulate human cortical function.

Event‐related fMRI at 7T reveals overlapping cortical representations for adjacent fingertips in S1 of individual subjects

Recent fMRI studies of the human primary somatosensory cortex have been able to differentiate the cortical representations of different fingertips at a single‐subject level. These studies did not, however, investigate the expected overlap in cortical activation due to the stimulation of different fingers. Here, we used an event‐related design in six subjects at 7 Tesla to explore the overlap in cortical responses elicited in S1 by vibrotactile stimulation of the five fingertips. We found that all parts of S1 show some degree of spatial overlap between the cortical representations of adjacent or even nonadjacent fingertips. In S1, the posterior bank of the central sulcus showed less overlap than regions in the post‐central gyrus, which responded to up to five fingertips. The functional properties of these two areas are consistent with the known layout of cytoarchitectonically defined subareas, and we speculate that they correspond to subarea 3b (S1 proper) and subarea 1, respectively. In contrast with previous fMRI studies, however, we did not observe discrete activation clusters that could unequivocally be attributed to different subareas of S1. Venous maps based on T2*‐weighted structural images suggest that the observed overlap is not driven by extra‐vascular contributions from large veins. Hum Brain Mapp 35:2027–2043, 2014. © 2013 The Authors Human Brain Mapping published by Wiley Periodicals, Inc.

Regional structural differences across functionally parcellated Brodmann areas of human primary somatosensory cortex

Ultra-high-field (UHF) MRI is ideally suited for structural and functional imaging of the brain. High-resolution structural MRI can be used to map the anatomical boundaries between functional domains of the brain by identifying changes related to the pattern of myelination within cortical gray matter, opening up the possibility to study the relationship between functional domains and underlying structure in vivo. In a recent study, we demonstrated the correspondence between functional (based on retinotopic mapping) and structural (based on changes in T2⁎-weighted images linked to myelination) parcellations of the primary visual cortex (V1) in vivo at 7T (Sanchez-Panchuelo et al., 2012b). Here, we take advantage of the improved BOLD CNR and high spatial resolution achievable at 7T to study regional structural variations across the functionally defined areas within the primary somatosensory cortex (S1) in individual subjects. Using a traveling wave fMRI paradigm to map the internal somatotopic representation of the index, middle, and ring fingers in S1, we were able to identify multiple map reversals at the tip and base, corresponding to the boundaries between Brodmann areas 3a, 3b, 1 and 2. Based on high resolution structural MRI data acquired in the same subjects, we inspected these functionally-parcellated Brodmann areas for differences in cortical thickness and MR contrast measures (magnetization transfer ratio (MTR) and signal intensity in phase sensitive inversion recovery (PSIR) images) that are sensitive to myelination. Consistent area-related differences in cortical thickness and MTR/PSIR measurements were found across subjects. However these measures did not have sufficient sensitivity to allow definition of areal boundaries.

Somatotopic finger mapping using MEG: Toward an optimal stimulation paradigm

ObjectiveIn non-invasive somatotopic mapping based on neuromagnetic source analysis, the recording time can be shortened and accuracy improved by applying simultaneously vibrotactile stimuli at different frequencies to multiple body sites and recording multiple steady-state responses. This study compared the reliability of sensory evoked responses, source localization performance, and reproducibility of digit maps for three different stimulation paradigms. MethodsVibrotactile stimuli were applied to the fingertip and neuromagnetic steady-state responses were recorded. Index and middle fingers were stimulated either sequentially in separate blocks, simultaneously at different frequencies, or in alternating temporal order within a block. ResultsResponse amplitudes were largest and source localization was most accurate between 21 and 23Hz. Separation of adjacent digits was significant for all paradigms in all participants. Suppressive interactions occurred between simultaneously applied stimuli. However, when frequently alternating between stimulus sites, the higher stimulus novelty resulted in increased amplitudes and superior localization performance. ConclusionsWhen receptive fields are strongly overlapping, the alternating stimulation is preferable over recording multiple steady state responses. SignificanceThe new paradigm improved the measurement of the distance of somatotopic finger representation in human primary somatosensory cortex, which is an important metric for neuroplastic reorganization after learning and rehabilitation training.

A Fovea for Pain at the Fingertips

SummaryThe spatial resolution of sensory systems is not homogeneous across their receptive surfaces. For example, tactile acuity is greatest on the fingertips, reflecting the high innervation density and small mechanoreceptive fields in this area [1, 2]. In contrast, pain is considered to lack any equivalent to the tactile fovea on the fingertips, where the density of nociceptive fibers is remarkably low [3]. Here, by combining psychophysics with histology, we show that this established notion is incorrect. By delivering small-diameter nociceptive-specific laser pulses to human volunteers, we discovered that (1) the spatial acuity for pain is higher on the fingertips than on proximal skin regions such as the hand dorsum, and (2) this distal-proximal gradient for pain is comparable to that for touch. In contrast, skin biopsies in the same participants showed that the intraepidermal nerve fiber density is lower in the fingertips than in the hand dorsum. The increased spatial acuity for pain on the fingertips therefore cannot be explained simply by peripheral innervation density. This finding is, however, consistent with the existence of fine-grained maps of nociceptive input to individual digits in the human primary somatosensory cortex [4].Video

Single-subject fMRI mapping at 7 T of the representation of fingertips in S1: a comparison of event-related and phase-encoding designs

A desirable goal of functional MRI (fMRI), both clinically and for basic research, is to produce detailed maps of cortical function in individual subjects. Single-subject mapping of the somatotopic hand representation in the human primary somatosensory cortex (S1) has been performed using both phase-encoding and block/event-related designs. Here, we review the theoretical strengths and limits of each method and empirically compare high-resolution (1.5 mm isotropic) somatotopic maps obtained using fMRI at ultrahigh magnetic field (7 T) with phase-encoding and event-related designs in six subjects in response to vibrotactile stimulation of the five fingertips. Results show that the phase-encoding design is more efficient than the event-related design for mapping fingertip-specific responses and in particular allows us to describe a new additional somatotopic representation of fingertips on the precentral gyrus. However, with sufficient data, both designs yield very similar fingertip-specific maps in S1, which confirms that the assumption of local representational continuity underlying phase-encoding designs is largely valid at the level of the fingertips in S1. In addition, it is shown that the event-related design allows the mapping of overlapping cortical representations that are difficult to estimate using the phase-encoding design. The event-related data show a complex pattern of overlapping cortical representations for different fingertips within S1 and demonstrate that regions of S1 responding to several adjacent fingertips can incorrectly be identified as responding preferentially to one fingertip in the phase-encoding data.

Fine-Grained Nociceptive Maps in Primary Somatosensory Cortex

Topographic maps of the receptive surface are a fundamental feature of neural organization in many sensory systems. While touch is finely mapped in the cerebral cortex, it remains controversial how precise any cortical nociceptive map may be. Given that nociceptive innervation density is relatively low on distal skin regions such as the digits, one might conclude that the nociceptive system lacks fine representation of these regions. Indeed, only gross spatial organization of nociceptive maps has been reported so far. However, here we reveal the existence of fine-grained somatotopy for nociceptive inputs to the digits in human primary somatosensory cortex (SI). Using painful nociceptive-selective laser stimuli to the hand, and phase-encoded functional magnetic resonance imaging analysis methods, we observed somatotopic maps of the digits in contralateral SI. These nociceptive maps were highly aligned with maps of non-painful tactile stimuli, suggesting comparable cortical representations for, and possible interactions between, mechanoreceptive and nociceptive signals. Our findings may also be valuable for future studies tracking the time course and the spatial pattern of plastic changes in cortical organization involved in chronic pain.

Within-Digit Functional Parcellation of Brodmann Areas of the Human Primary Somatosensory Cortex Using Functional Magnetic Resonance Imaging at 7 Tesla

The primary somatosensory cortex (S1) can be subdivided cytoarchitectonically into four distinct Brodmann areas (3a, 3b, 1, and 2), but these areas have never been successfully delineated in vivo in single human subjects. Here, we demonstrate the functional parcellation of four areas of S1 in individual human subjects based on high-resolution functional MRI measurements made at 7 T using vibrotactile stimulation. By stimulating four sites along the length of the index finger, we were able to identify and locate map reversals of the base to tip representation of the index finger in S1. We suggest that these reversals correspond to the areal borders between the mirrored representations in the four Brodmann areas, as predicted from electrophysiology measurements in nonhuman primates. In all subjects, maps were highly reproducible across scanning sessions and stable over weeks. In four of the six subjects scanned, four, mirrored, within-finger somatotopic maps defining the extent of the Brodmann areas could be directly observed on the cortical surface. In addition, by using multivariate classification analysis, the location of stimulation on the index finger (four distinct sites) could be decoded with a mean accuracy of 65% across subjects. Our measurements thus show that within-finger topography is present at the millimeter scale in the cortex and is highly reproducible. The ability to identify functional areas of S1 in vivo in individual subjects will provide a framework for investigating more complex aspects of tactile representation in S1.

Human finger somatotopy in areas 3b, 1, and 2: A 7T fMRI study using a natural stimulus

To study the properties of human primary somatosensory (S1) cortex as well as its role in cognitive and social processes, it is necessary to noninvasively localize the cortical representations of the body. Being arguably the most relevant body parts for tactile exploration, cortical representations of fingers are of particular interest. The aim of the present study was to investigate the cortical representation of individual fingers (D1-D5), using human touch as a stimulus. Utilizing the high BOLD sensitivity and spatial resolution at 7T, we found that each finger is represented within three subregions of S1 in the postcentral gyrus. Within each of these three areas, the fingers are sequentially organized (from D1 to D5) in a somatotopic manner. Therefore, these finger representations likely reflect distinct activations of BAs 3b, 1, and 2, similar to those described in electrophysiological work in non-human primates. Quantitative analysis of the local BOLD responses revealed that within BA3b, each finger representation is specific to its own stimulation without any cross-finger responsiveness. This finger response selectivity was less prominent in BA 1 and in BA 2. A test-retest procedure highlighted the reproducibility of the results and the robustness of the method for BA 3b. Finally, the representation of the thumb was enlarged compared to the other fingers within BAs 1 and 2. These findings extend previous human electrophysiological and neuroimaging data but also reveal differences in the functional organization of S1 in human and nonhuman primates.

An Approach to Localizing Corneal Pain Representation in Human Primary Somatosensory Cortex

The cornea has been a focus of animal electrophysiological research for decades, but little is known regarding its cortical representation in the human brain. This study attempts to localize the somatotopic representation of the cornea to painful stimuli in human primary somatosensory cortex using functional magnetic resonance imaging (fMRI). In this case study, a subject was imaged at 3T while bright light was presented in a block-design, which either produced pain and blinking (during photophobia) or blinking alone (after recovery from photophobia). Pain and blinking produced precisely localized activations in primary somatosensory cortex and primary motor cortex. These results indicate that noxious stimulation of the cornea can produce somatotopic activation in primary somatosensory cortex. This finding opens future avenues of research to evaluate the relationship between corneal pain and central brain mechanisms relating to the development of chronic pain conditions, such as dry eye-like symptoms.

Gamma-Band Oscillations in the Primary Somatosensory Cortex—A Direct and Obligatory Correlate of Subjective Pain Intensity

Electroencephalographic gamma band oscillations (GBOs) induced over the human primary somatosensory cortex (SI) by nociceptive stimuli have been hypothesized to reflect cortical processing involved directly in pain perception, because their magnitude correlates with pain intensity. However, as stimuli perceived as more painful are also more salient, an alternative interpretation of this correlation is that GBOs reflect unspecific stimulus-triggered attentional processing. In fact, this is suggested by recent observations that other features of the electroencephalographic (EEG) response correlate with pain perception when stimuli are presented in isolation, but not when their saliency is reduced by repetition. Here, by delivering trains of three nociceptive stimuli at a constant 1 s interval, and using different energies to elicit graded pain intensities, we demonstrate that GBOs recorded over SI always predict the subjective pain intensity, even when saliency is reduced by repetition. These results provide evidence for a close relationship between GBOs and the cortical activity subserving pain perception.

Modulation of somatosensory evoked magnetic fields by intensity of interfering stimuli in human somatosensory cortex: An MEG study

Somatosensory evoked responses are known to be modulated by previous interfering stimuli. Here, we first investigated the modulatory effects of interfering stimuli with different intensities on somatosensory evoked magnetic field in human primary (S1) and secondary (S2) somatosensory cortices. In the control condition of the study, test stimulus, set to strong intensity, was delivered to the left median nerve. Interfering stimuli with three different levels of intensity from weak (WI) through moderate (MI) and finally to strong (SI) were interspersed to the left median nerve between the test stimuli in each interfering condition. The cortical responses to the test stimulus were modeled with equivalent current dipoles in the contralateral S1 and bilateral S2 cortices from 17 subjects. The amplitude of the N20m deflection from the S1 was not changed by any interfering stimuli, whereas the amplitude of later P35m deflection was reduced by MI stimulus. The amplitude of P60m deflection was reduced by MI and SI stimuli. The extent of amplitude reduction of the bilateral S2 response was markedly increased as intensity of interfering stimuli increased from weak to moderate, but further reduction by the SI stimuli compared to MI stimuli was not observed. Those results indicated that somatosensory cortical activation in the S1 (P35m and P60m) and S2 were modulated by intensity of interfering stimuli. Our findings of a greater gating effect on the bilateral S2 compared to the contralateral S1 indicate that S2 may play an important role in temporal integration of different intensity levels of somatosensory inputs.

Reappraisal of the Somatosensory Homunculus and Its Discontinuities

Neuroscience folklore has it that somatotopy in human primary somatosensory cortex (SI) has two significant discontinuities: the hands and face map onto adjacent regions in SI, as do the feet and genitalia. It has been proposed that these conjunctions in SI result from coincident sources of stimulation in the fetal position, where the hands frequently touch the face, and the feet the genitalia. Computer modeling using a Hebbian variant of the self-organizing Kohonen net is consistent with this proposal. However, recent work reveals that the genital representation in SI for cutaneous sensations (as opposed to tumescence) is continuous with that of the lower trunk and thigh. This result, in conjunction with reports of separate face innervation and its earlier onset of sensory function, compared to that of the rest of the body, allows a reappraisal of homuncular organization. It is proposed that the somatosensory homunculus comprises two distinct somatotopic regions: the face representation and that of the rest of the body. Principles of self-organization do not account satisfactorily for the overall homuncular map. These results may serve to alert computational modelers that intrinsic developmental factors can override simple rules of plasticity.