Human SII Research Articles

Action execution and action observation elicit mirror responses with the same temporal profile in human SII

The properties of the secondary somatosensory area (SII) have been described by many studies in monkeys and humans. Recent studies on monkeys, however, showed that beyond somatosensory stimuli, SII responds to a wider number of stimuli, a finding requiring a revision that human SII is purely sensorimotor. By recording cortical activity with stereotactic electroencephalography (stereo-EEG), we examined the properties of SI and SII in response to a motor task requiring reaching, grasping and manipulation, as well as the observation of the same actions. Furthermore, we functionally characterized this area with a set of clinical tests, including tactile, acoustical, and visual stimuli. The results showed that only SII activates both during execution and observation with a common temporal profile, whereas SI response were limited to execution. Together with their peculiar response to tactile stimuli, we conclude that the role of SII is pivotal also in the observation of actions involving haptic control.

The organization of the posterior parietal cortex devoted to upper limb actions: An fMRI study.

The present fMRI study examined whether upper‐limb action classes differing in their motor goal are encoded by different PPC sectors. Action observation was used as a proxy for action execution. Subjects viewed actors performing object‐related (e.g., grasping), skin‐displacing (e.g., rubbing the skin), and interpersonal upper limb actions (e.g., pushing someone). Observation of the three action classes activated a three‐level network including occipito‐temporal, parietal, and premotor cortex. The parietal region common to observing all three action classes was located dorsally to the left intraparietal sulcus (DIPSM/DIPSA border). Regions specific for observing an action class were obtained by combining the interaction between observing action classes and stimulus types with exclusive masking for observing the other classes, while for regions considered preferentially active for a class the interaction was exclusively masked with the regions common to all observed actions. Left putative human anterior intraparietal was specific for observing manipulative actions, and left parietal operculum including putative human SII region, specific for observing skin‐displacing actions. Control experiments demonstrated that this latter activation depended on seeing the skin being moved and not simply on seeing touch. Psychophysiological interactions showed that the two specific parietal regions had similar connectivities. Finally, observing interpersonal actions preferentially activated a dorsal sector of left DIPSA, possibly the homologue of ventral intraparietal coding the impingement of the target person's body into the peripersonal space of the actor. These results support the importance of segregation according to the action class as principle of posterior parietal cortex organization for action observation and by implication for action execution. Hum Brain Mapp 36:3845–3866, 2015. © 2015 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.

Visual Responsiveness of Neurons in the Secondary Somatosensory Area and its Surrounding Parietal Operculum Regions in Awake Macaque Monkeys.

Previous neurophysiological studies performed in macaque monkeys have shown that the secondary somatosensory cortex (SII) is essentially engaged in the processing of somatosensory information and no other sensory input has been reported. In contrast, recent human brain-imaging studies have revealed the effects of visual and auditory stimuli on SII activity, which suggest multisensory integration in the human SII. To determine whether multisensory responses of the SII also exist in nonhuman primates, we recorded single-unit activity in response to visual and auditory stimuli from the SII and surrounding regions in 8 hemispheres from 6 awake monkeys. Among 1157 recorded neurons, 306 neurons responded to visual stimuli. These visual neurons usually responded to rather complex stimuli, such as stimulation of the peripersonal space (40.5%), observation of human action (29.1%), and moving-object stimulation outside the monkey's reach (23.9%). We occasionally applied auditory stimuli to visual neurons and found 10 auditory-responsive neurons that exhibited somatosensory responses. The visual neurons were distributed continuously along the lateral sulcus covering the entire SII, along with other somatosensory neurons. These results highlight the need to investigate novel functional roles—other than somesthetic sensory processing—of the SII.

Adaptation in human somatosensory cortex as a model of sensory memory construction: a study using high-density EEG.

Adaptation in sensory cortices has been seen as a mechanism allowing the creation of transient memory representations. Here we tested the adapting properties of early responses in human somatosensory areas SI and SII by analysing somatosensory-evoked potentials over the very first repetitions of a stimulus. SI and SII generators were identified by well-defined scalp potentials and source localisation from high-density 128-channel EEG. Earliest responses (~20 ms) from area 3b in the depth of the post-central gyrus did not show significant adaptation to stimuli repeated at 300 ms intervals. In contrast, responses around 45 ms from the crown of the gyrus (areas 1 and 2) rapidly lessened to a plateau and abated at the 20th stimulation, and activities from SII in the parietal operculum at ~100 ms displayed strong adaptation with a steady amplitude decrease from the first repetition. Although responses in both SI (1-2) and SII areas showed adapting properties and hence sensory memory capacities, evidence of sensory mismatch detection has been demonstrated only for responses reflecting SII activation. This may index the passage from an early form of sensory storage in SI to more operational memory codes in SII, allowing the prediction of forthcoming input and the triggering of a specific signal when such input differs from the previous sequence. This is consistent with a model whereby the length of temporal receptive windows increases with progression in the cortical hierarchy, in parallel with the complexity and abstraction of neural representations.

Are There Nociceptive-Specific Brain Potentials?

to the editor: In their study on factor analysis of brain responses to different stimulus modalities, [Mouraux and Iannetti (2009)][1] claimed that laser-evoked brain potentials do not reflect nociceptive-specific neural activity, although laser radiant heat pulses provide a purely nociceptive input

The Somatotopic Organization of Cytoarchitectonic Areas on the Human Parietal Operculum

The secondary somatosensory cortex (SII) of nonhuman primates is located on the parietal operculum. In the monkey, electrophysiological and connectivity tracing studies as well as histological investigations provide converging evidence for 3 distinct cortical areas (SII, PV, and VS) within this region, each of which contains a complete somatotopic map. Although the equivalency of the parietal operculum as the location of SII between humans and nonhuman primates is undisputed, the internal organization of the human SII region is still largely unknown. Based on their topography, we have previously argued that the cytoarchitectonic areas OP 1, OP 4, and OP 3 may constitute the human homologues of areas SII, PV, and VS, respectively. To test this hypothesis, we here examined (using functional magnetic resonance imaging) the somatotopic organization of the human parietal operculum by applying tactile stimulation to the skin at 4 different locations on either side of the body (face, hands, trunk, and legs). The locations of the resulting activation foci were then compared with the cytoarchitectonic maps of this region. Data analysis revealed 2 somatotopic body representations on the lateral operculum in areas OP 1 and OP 4. The functional border between these 2 body maps was defined by a mirror reversal in the somatotopic arrangement and coincided with the cytoarchitectonically defined border between these 2 areas. This somatotopic arrangement closely matches that described for SII and PV in nonhuman primates. The data also suggested a third somatotopic map located deeper inside the Sylvian fissure in area OP 3. Based on the observed topographic arrangement and their functional response characteristics, we conclude that cytoarchitectonic areas OP1, OP 4, and OP 3 on the human parietal operculum constitute the human homologues of primate areas SII, PV, and VS, respectively.

Centrifugal regulation of human cortical responses to a task-relevant somatosensory signal triggering voluntary movement

Many studies have reported a movement-related modulation of response in the primary and secondary somatosensory cortices (SI and SII) to a task-irrelevant stimulation in primates. In the present study, magnetoencephalography (MEG) was used to examine the top–down centrifugal regulation of neural responses in the human SI and SII to a task-relevant somatosensory signal triggering a voluntary movement. Nine healthy adults participated in the study. A visual warning signal was followed 2 s later by a somatosensory imperative signal delivered to the right median nerve at the wrist. Three kinds of warning signal informed the participants of the reaction which should be executed on presentation of the imperative signal (rest or extension of the right index finger, extension of the left index finger). The somatosensory stimulation was used to both generate neural responses and trigger voluntary movement and therefore was regarded as a task-relevant signal. The responses were recorded using a whole-head MEG system. The P35m response around the SI was reduced in magnitude without alteration of the primary SI response, N20m, when the signal triggered a voluntary movement compared to the control condition, whereas bilateral SII responses peaking at 70–100 ms were enhanced and the peak latency was shortened. The peak latency of the responses in the SI and SII preceded the onset of the earliest voluntary muscle activation in each subject. Later bilateral perisylvian responses were also enhanced with movement. In conclusion, neural activities in the SI and SII evoked by task-relevant somatosensory signals are regulated differently by motor-related neural activities before the afferent inputs. The present findings indicate a difference in function between the SI and SII in somatosensory–motor regulation.

Neuromagnetic SII responses do not fully reflect pain scale

To elucidate the role of somatosensory cortices in coding pain magnitude, we recorded the neuromagnetic responses of ten subjects to mild, moderate, and severe pain stimulation by delivering thulium-laser pulses on the dorsum of the left hand. The stimulus intensities for producing different pain levels were determined individually, and the mean values across subjects were 255, 365, and 490 mJ for mild, moderate, and severe pain, respectively. We obtained 40 responses for each intensity condition, and analyzed the averaged cortical signals by multi-dipole modeling. All subjects showed consistent activation over the bilateral secondary somatosensory (SII) cortices for each intensity level, peaking around 150–230 ms, with 15-ms earlier on the contralateral hemisphere. The SII dipole strength was significantly larger for the moderate than for the mild pain stimulation, but lacked further increase as the pain magnitude elevated to the severe level. In contrast, the primary somatosensory cortical response was detected in only half of our subjects, and thus it seemed difficult to evaluate its role in pain intensity coding. Our results suggest that activation strength in human SII cortices reflects the magnitude of peripheral noxious inputs only up to the moderate level, and some other cerebral correlates may get involved in sensing a further increment of pain magnitude.

The Human Parietal Operculum. I. Cytoarchitectonic Mapping of Subdivisions

The human secondary somatosensory cortex (SII) is located on the parietal operculum, as shown by intraoperative stimulation and functional imaging studies. The position and extent of the anatomical correlates of this functionally defined region, however, are still unknown. We have therefore histologically mapped the putative anatomical correlates of the SII cortex in cell-body-stained histological sections of 10 human postmortem brains using quantitative cytoarchitectonic analysis. The gray level index (GLI), which is an indicator of the volume fraction of nerve cell bodies, was measured in the parietal operculum. GLI profiles as measures of the laminar pattern of the cortex were extracted perpendicular to cortical layers. Cytoarchitectonic borders were detected observer-independently by multivariate statistical analysis of the laminar profiles. Four cytoarchitectonic areas (termed OP 1-4) were identified. This cytoarchitectonic heterogeneity of the parietal operculum corresponds to results of functional imaging studies on the human SII cortex and data from non-human primates where multiple subregions within SII have been demonstrated by electrophysiological and connectivity studies.

The Human Parietal Operculum. II. Stereotaxic Maps and Correlation with Functional Imaging Results

In this study we describe the localization of the cytoarchitectonic subdivisions of the human parietal operculum in stereotaxic space and relate these anatomically defined cortical areas to the location of the functionally defined secondary somatosensory cortex (SII cortex) using a meta-analysis of functional imaging results. The human parietal operculum consists of four distinct cytoarchitectonic areas (OP 1-4) as shown in the preceding publication. The 10 cytoarchitectonically examined brains were 3-D-reconstructed and spatially normalized to the T1-weighted single-subject template of the Montreal Neurological Institute (MNI). A probabilistic map was calculated for each area in this standard stereotaxic space. A cytoarchitectonic summary map of the four cortical areas on the human parietal operculum which combines these probabilistic maps was subsequently computed for the comparison with a meta-analysis of functional locations of SII. The meta-analysis used the results from 57 fMRI and PET studies and allowed the comparison of the functionally defined SII region to the cytoarchitectonic map of the parietal operculum. The functional localization of SII showed a good match to the cytoarchitectonically defined region. Therefore the cytoarchitectonic maps of OP 1-4 of the human parietal operculum can be interpreted as an anatomical correlate of the (functionally defined) human SII region. Our results also suggest that the SII foci reported in functional imaging studies may actually reflect activations in either of its architectonic subregions.

Activation of human SII cortex during exploratory finger movement and hand clenching tasks

We used electric median nerve stimuli to elucidate the functional properties of neurons in the human secondary somatosensory cortex during exploration of small objects and muscle contraction. Somatosensory evoked fields were recorded from nine healthy subjects with a 204-channel neuromagnetometer. Electrical stimuli were applied once every 3 s to the left median nerve at the wrist. The conditions during the stimulation were rest (control session), exploration of small objects (exploration session) and clenching the hand while the wrist was being electrically stimulated (clench session). The strengths of equivalent current dipoles of evoked fields from the secondary somatosensory cortex were increased during the exploration session, but those of evoked fields were decreased by the clench session.

Functional topography of the secondary somatosensory cortex for nonpainful and painful stimulation of median and tibial nerve: an fMRI study

Functional magnetic resonance imaging (fMRI) was used to study the cortical activity of the bilateral secondary somatosensory cortex (SII) during nonpainful (motor threshold) and painful electrical stimulation of median and tibial nerves. fMRI recordings were performed in eight normal young adults. The aim was at evaluating the working hypothesis of a spatial segregation of nonpainful and painful populations not only in the "hand" representation of SII [Ferretti, A., Babiloni, C., Del Gratta, C., Caulo, M., Tartaro, A., Bonomo, L., Rossini, P.M., Romani, G.L., 2003. Functional topography of the secondary somatosensory cortex for nonpainful and painful stimuli: an fMRI study. NeuroImage 20, 1625-1638.] but also in its "foot" representation. Results showed that, in both "hand" and "foot" representations of bilateral SII, the activity elicited by the painful stimulation was localized more posteriorly with respect to that elicited by the nonpainful stimulation. A fine spatial analysis of the SII responses revealed a clear somatotopic organization in the bilateral SII subregion especially reactive to the nonpainful stimuli (i.e., segregation of the hand and foot representations). In contrast, it was not possible to disentangle the "hand" and "foot" representations of SII for painful stimuli. These results extended to the SII "foot" representation previous evidence of a spatial segregation in the SII "hand" representation of subregions for the painful and nonpainful stimuli. Furthermore, they suggest that noxious information is not somatotopically represented in human bilateral SII, at least as inferred from fMRI data at 1.5 T.

Temporal dynamics of alpha and beta rhythms in human SI and SII after galvanic median nerve stimulation. A MEG study

In this MEG study, we investigated cortical alpha/sigma and beta ERD/ERS induced by median nerve stimulation to extend previous evidence on different resonant and oscillatory behavior of SI and SII (NeuroImage 13 [2001] 662). Here, we tested whether simple somatosensory stimulation could induce a distinctive sequence of alpha/sigma and beta ERD/ERS over SII compared to SI. We found that for both alpha/sigma (around 10 Hz) and beta (around 20 Hz) rhythms, the latencies of ERD and ERS were larger in bilateral SII than in contralateral SI. In addition, the peak amplitude of alpha/sigma and beta ERS was smaller in bilateral SII than in contralateral SI. These results indicate a delayed and prolonged activation of SII responses, reflecting a protracted information elaboration possibly related to SII higher order role in the processing of somatosensory information. This temporal dynamics of alpha/sigma and beta rhythms may be related to a sequential activation scheme of SI and SII during the somatosensory information processes. Future studies should evaluate in SII the possible different functional significance of alpha/sigma with respect to beta rhythms during somatosensory processing.

Role of human SII cortices in sensorimotor integration.

To elucidate the functional properties of neurons in the human primary (SI) and ipsilateral and contralateral secondary (iSII or cSII) cortices in response to stimuli during finger movement. We measured somatosensory evoked fields (SEFs) produced by electric stimuli delivered to the median nerve at 0.2 Hz in 6 healthy subjects. The amplitudes of evoked fields from both iSII and cSII were gradually attenuated with time. Consecutive blocks of trials were obtained to assess the habituation of each evoked field. Complex finger movements with attention (gating session) increased the amplitude of evoked fields from the iSII cortices but reduced the amplitudes of evoked fields from the cSII cortices (P<0.01). In contrast, the amplitude of P30 m from the SI did not show habituation effects but decreased significantly in the gating session (P<0.01). The enhanced iSII as well as suppressed cSII cortices during complex finger movements with attention are not only considered to be result of gating effect but also attention.

Modulated Activation of the Human SI and SII Cortices during Observation of Hand Actions

Neurons in area F5 of the monkey premotor cortex are activated during both execution and observation of hand actions. A similar “mirror-neuron system” seems to exist also in the human brain, including at least the superior temporal sulcus region, Broca's area, and the primary motor cortex. We recorded somatosensory evoked fields in response to median nerve stimulation from nine healthy subjects during (i) rest, (ii) manipulation of a small object, and (iii) observation of the same action to find out to what extent the somatosensory cortices display behavior similar to the human mirror-neuron system. SI signals were enhanced and SII signals suppressed during both manipulation and observation, except when the right manipulating hand was stimulated. Our results suggest that the SI and SII cortices contribute to the human mirror-neuron system, possibly providing information necessary for preserving the sense of self during action observation.

Cortical Activation Associated with Passive Movements of the Human Index Finger: An MEG Study

We recorded somatosensory evoked fields to passive extensions of the left and right index fingers in eight healthy adults. A new nonmagnetic device was designed to produce calibrated extensions of 19°, with a mean angular velocity of 630°/s. The responses, recorded with a 306-channel neuromagnetometer, were modeled with current dipoles. The earliest activation was in the primary somatosensory cortex, with peaks at 36–58 and 30–82 ms for left and right index finger extensions, respectively. Later signals were observed in the left second somatosensory (SII) cortex in six of eight subjects at 75–175 and 75–155 ms for left- and right-sided extensions, respectively; three subjects showed bilateral SII activation in at least one condition. Our results suggest a predominant role for the human left SII cortex in proprioceptive processing.

Left-Hemisphere-Dominant SII Activation after Bilateral Median Nerve Stimulation

We used bilateral median nerve stimuli to find out possible hemispheric dominance in the activation of the second somatosensory cortex, SII. Somatosensory evoked fields (SEFs) were recorded from 14 healthy adults (7 right-handed, 7 left-handed) with a 306-channel neuromagnetometer. Electrical stimuli were applied once every 3 s simultaneously either to the left and right median nerves at the wrists or to the palmar skin of both thumbs. Sources of SEFs were modeled with four current dipoles, located in the SI and SII cortices of both hemispheres. The SI activation strengths did not differ between the hemispheres, whereas the SII responses were significantly stronger in the left than in the right hemisphere. In right-handers, the left/right SII ratios were 1.9 and 1.8 for wrist and thumb stimuli, respectively. The corresponding values were 1.5 and 1.7 in left-handers. The results indicate handedness-independent functional specialization of the human SII cortices.

Functional overlap of finger representations in human SI and SII cortices.

We aimed to find out to what extent functional representations of different fingers of the two hands overlap at the human primary and secondary somatosensory cortices SI and SII. Somatosensory evoked fields (SEFs) were recorded with a 306-channel neuromagnetometer from 8 subjects. Tactile stimuli, produced by diaphragms driven by compressed air, were delivered to the fingertips in three different conditions. First, the right index finger was stimulated once every 2 s. Then two other stimuli were interspersed, in different sessions, to right- or left-hand fingers (thumb, middle finger, or ring finger) between the successive right index finger stimuli. Strengths of the responses to right index finger stimuli were evaluated in each condition. Responses to right index finger stimuli were modeled by three current dipoles, located at the contralateral SI and the SII cortices of both hemispheres. The earliest SI responses, peaking around 65 ms, were suppressed by 18% (P < 0.05) when the intervening stimuli were presented to the same hand; intervening stimuli to the other hand had no effect. The SII responses were bilaterally suppressed by intervening stimuli presented to either hand: in the left SII, the suppression was 39 and 42% (P < 0.01) and in the right SII 67 and 72% (P < 0.001) during left- and right-sided intervening stimuli, respectively. Left- and right-sided intervening stimuli affected similarly the SII responses and had no effect on the response latencies. The results indicate a strong and symmetric overlap of finger representations for both hands in the human SII cortices, and a weaker functional overlap for fingers of the same hand in the SI cortex.

Evidence for a 7- to 9-Hz “Sigma” Rhythm in the Human SII Cortex

Electrical activity of the human brain features several rhythmical components which can be readily studied with whole-scalp neuromagnetometers. We describe a new 7- to 9-Hz “sigma” rhythm in the human second somatosensory cortex, distinct from both the mu rhythm of the primary sensorimotor cortex and the tau rhythm of the supratemporal auditory cortex. Sigma shows rate-selective responsiveness to rhythmical median nerve stimulation and is enhanced by stimulation at the rhythm's dominant frequency. Single stimuli may trigger several periods of the rhythm. The functional significance of the sigma rhythm remains to be investigated.

Sustained Activation of the Human SII Cortices by Stimulus Trains

To compare the functional properties of neurons in the human primary (SI) and secondary (SII) cortices, we recorded somatosensory-evoked fields (SEFs) from seven healthy subjects to single electric stimuli and stimulus trains delivered to the median nerve at 8–12 Hz. The SI and SII cortices responded strikingly differently to stimulus trains: whereas SI followed each stimulus with a sharp transient response up to at least 12 Hz, the transient responses were much less prominent at SII, which mainly responded with a sustained field that returned to baselevel at 800–1000 ms. The different response patterns of SI and SII suggest that the inhibition, following the early excitatory responses, is weaker at SII than SI, or that inhibitory responses of these two areas differ in their relative timing.