Spatiotemporal integration of tactile information in human somatosensory cortex

BACKGROUND: Our goal was to examine the spatiotemporal integration of tactile information in the hand representation of human primary somatosensory cortex (anterior parietal somatosensory areas 3b and 1), secondary somatosensory cortex (S2), and the parietal ventral area (PV), using high-resolution whole-head magnetoencephalography (MEG). To examine representational overlap and adaptation in bilateral somatosensory cortices, we used an oddball paradigm to characterize the representation of the index finger (D2; deviant stimulus) as a function of the location of the standard stimulus in both right- and left-handed subjects. RESULTS: We found that responses to deviant stimuli presented in the context of standard stimuli with an interstimulus interval (ISI) of 0.33s were significantly and bilaterally attenuated compared to deviant stimulation alone in S2/PV, but not in anterior parietal cortex. This attenuation was dependent upon the distance between the deviant and standard stimuli: greater attenuation was found when the standard was immediately adjacent to the deviant (D3 and D2 respectively), with attenuation decreasing for non-adjacent fingers (D4 and opposite D2). We also found that cutaneous mechanical stimulation consistently elicited not only a strong early contralateral cortical response but also a weak ipsilateral response in anterior parietal cortex. This ipsilateral response appeared an average of 10.7 ± 6.1 ms later than the early contralateral response. In addition, no hemispheric differences either in response amplitude, response latencies or oddball responses were found, independent of handedness. CONCLUSION: Our findings are consistent with the large receptive fields and long neuronal recovery cycles that have been described in S2/PV, and suggest that this expression of spatiotemporal integration underlies the complex functions associated with this region. The early ipsilateral response suggests that anterior parietal fields also receive tactile input from the ipsilateral hand. The lack of a hemispheric difference in responses to digit stimulation supports a lack of any functional asymmetry in human somatosensory cortex

Brain Cortical Mapping by Simultaneous Recording of Functional Near Infrared Spectroscopy and Electroencephalograms from the Whole Brain During Right Median Nerve Stimulation

To investigate relationships between hemodynamic responses and neural activities in the somatosensory cortices, hemodynamic responses by near infrared spectroscopy (NIRS) and electroencephalograms (EEGs) were recorded simultaneously while subjects received electrical stimulation in the right median nerve. The statistical significance of the hemodynamic responses was evaluated by a general linear model (GLM) with the boxcar design matrix convoluted with Gaussian function. The resulting NIRS and EEGs data were stereotaxically superimposed on the reconstructed brain of each subject. The NIRS data indicated that changes in oxy-hemoglobin concentration increased at the contralateral primary somatosensory (SI) area; responses then spread to the more posterior and ipsilateral somatosensory areas. The EEG data indicated that positive somatosensory evoked potentials peaking at 22 ms latency (P22) were recorded from the contralateral SI area. Comparison of these two sets of data indicated that the distance between the dipoles of P22 and NIRS channels with maximum hemodynamic responses was less than 10 mm, and that the two topographical maps of hemodynamic responses and current source density of P22 were significantly correlated. Furthermore, when onset of the boxcar function was delayed 5–15 s (onset delay), hemodynamic responses in the bilateral parietal association cortices posterior to the SI were more strongly correlated to electrical stimulation. This suggests that GLM analysis with onset delay could reveal the temporal ordering of neural activation in the hierarchical somatosensory pathway, consistent with the neurophysiological data. The present results suggest that simultaneous NIRS and EEG recording is useful for correlating hemodynamic responses to neural activity

Early integration of bilateral touch in the primary somatosensory cortex

Animal, as well as behavioural and neuroimaging studies in humans have documented integration of bilateral tactile information at the level of primary somatosensory cortex (SI). However, it is still debated whether integration in SI occurs early or late during tactile processing, and whether it is somatotopically organized. To address both the spatial and temporal aspects of bilateral tactile processing we used magnetoencephalography in a tactile repetition-suppression paradigm. We examined somatosensory evoked-responses produced by probe stimuli preceded by an adaptor, as a function of the relative position of adaptor and probe (probe always at the left index finger; adaptor at the index or middle finger of the left or right hand) and as a function of the delay between adaptor and probe (0, 25 or 125 ms). Percentage of response-amplitude suppression was computed by comparing paired (adaptor+probe) with single stimulations of adaptor and probe. Results show that response suppression varies differentially in SI and SII as a function of both spatial and temporal features of the stimuli. Remarkably, repetition suppression of SI activity emerged early in time, regardless of whether the adaptor stimulus was presented on the same and the opposite body side with respect to the probe. These novel findings support the notion of an early and somatotopically organized interhemispheric integration of tactile information in SI

Bilateral representations of touch in the primary somatosensory cortex

According to current textbook knowledge, primary somatosensory cortex (SI) supports unilateral tactile representations, whereas structures beyond SI, in particular the secondary somatosensory cortices (SII), support bilateral tactile representations. However, dexterous and well-coordinated bimanual motor tasks require early integration of bilateral tactile information. Sequential processing, first of unilateral and subsequently of bilateral sensory information might not be sufficient to accomplish these tasks. This view of sequential processing in the somatosensory system might therefore be questioned, at least for demanding bimanual tasks. Evidence from the last fifteen years is forcing a revision of this textbook notion. Studies in animals and humans indicate that SI is more than a simple relay for unilateral sensory information and, together with SII, contributes to the integration of somatosensory inputs from both sides of the body. Here, we review a series of recent works from our own and other laboratories in favour of interactions between tactile stimuli on the two sides of the body at early stages of processing. We will focus on tactile processing, although a similar logic may also apply to other aspects of somatosensation. We begin by describing the basic anatomy and physiology of interhemispheric transfer, drawing on neurophysiological studies in animals and behavioural studies in humans that showed tactile interactions between body sides, both in healthy and brain-damaged individuals. Then we describe the neural substrates of bilateral interactions in somatosensation as revealed by neurophysiological work in animals and neuroimaging studies in humans (i.e., functional magnetic resonance imaging, magnetoencephalography, and transcranial magnetic stimulation). Finally, we conclude with considerations on the dilemma of how efficiently integrating bilateral sensory information at early processing stages can coexist with more lateralised representations of somatosensory input, in the context of motor control

A conceptual model of tactile processing across body features of size, shape, side, and spatial location

The processing of touch depends of multiple factors, such as the properties of the skin and type of receptors stimulated, as well as features related to the actual configuration and shape of the body itself. A large body of research has focused on the effect that the nature of the stimuli has on tactile processing. Less research, however, has focused on features beyond the nature of the touch. In this review, we focus on some features related to the body that have been investigated for less time and in a more fragmented way. These include the symmetrical quality of the two sides of the body, the postural configuration of the body, as well as the size and shape of different body parts. We will describe what we consider three key aspects: (a) how and at which stages tactile information is integrated between different parts and sides of the body; (b) how tactile signals are integrated with online and stored postural configurations of the body, regarded as priors; (c) and how tactile signals are integrated with representations of body size and shape. Here, we describe how these different body dimensions affect integration of tactile information as well as guide motor behaviour by integrating them in a single model of tactile processing. We review a wide range of neuropsychological, neuroimaging and neurophysiological data and suggest a revised model of tactile integration on the basis of the one proposed previously by Longo and colleagues (2010)

Neuromagnetic studies on cortical somatosensory functions in infants and children : Normal development and effect of early brain lesions

Until recently, objective investigation of the functional development of the human brain in vivo was challenged by the lack of noninvasive research methods. Consequently, fairly little is known about cortical processing of sensory information even in healthy infants and children. Furthermore, mechanisms by which early brain insults affect brain development and function are poorly understood. In this thesis, we used magnetoencephalography (MEG) to investigate development of cortical somatosensory functions in healthy infants, very premature infants at risk for neurological disorders, and adolescents with hemiplegic cerebral palsy (CP). In newborns, stimulation of the hand activated both the contralateral primary (SIc) and secondary somatosensory cortices (SIIc). The activation patterns differed from those of adults, however. Some of the earliest SIc responses, constantly present in adults, were completely lacking in newborns and the effect of sleep stage on SIIc responses differed. These discrepancies between newborns and adults reflect the still developmental stage of the newborns’ somatosensory system. Its further maturation was demonstrated by a systematic transformation of the SIc response pattern with age. The main early adult­like components were present by age two. In very preterm infants, at term age, the SIc and SIIc were activated at similar latencies as in healthy fullterm newborns, but the SIc activity was weaker in the preterm group. The SIIc response was absent in four out of the six infants with brain lesions of the underlying hemisphere. Determining the prognostic value of this finding remains a subject for future studies, however. In the CP adolescents with pure subcortical lesions, contrasting their unilateral symptoms, the SIc responses of both hemispheres differed from those of controls: For example the distance between SIc representation areas for digits II and V was shorter bilaterally. In four of the five CP patients with cortico­subcortical brain lesions, no normal early SIc responses were evoked by stimulation of the palsied hand. The varying differences in neuronal functions, underlying the common clinical symptoms, call for investigation of more precisely designed rehabilitation strategies resting on knowledge about individual functional alterations in the sensorimotor networks.Lääketieteellisen teknologian kehitys on vasta viime vuosina mahdollistanut lasten aivotoiminnan tarkan, objektiivisen tutkimuksen. Näin ollen esimerkiksi aistiärsykkeiden aivoprosessoinnista vastasyntyneillä tiedetään varsin vähän, samoin kuin monien aivotoimintojen kehittymisestä lapsen kasvaessa. Myös ymmärrys erilaisten aivovaurioiden vaikutuksesta kehittyviin aivoihin on puutteellista. Magnetoenkefalografialla (MEG) tutkitaan aivohermosolujen toimintaa mittaamalla niissä syntyvien sähkövirtojen tuottamia magneettikenttiä pään ulkopuolelta. Väitöskirjassa MEG:n avulla tutkittiin tuntoaivokuoren toimintaa vastasyntyneillä ja tämän toiminnan kehitystä ensimmäisten elinvuosien aikana. Lisäksi tuntoaivokuoren toimintaa tarkasteltiin pikkukeskosena syntyneillä vauvoilla sekä nuorilla, joilla on varhaisen aivovaurion aiheuttama toispuoleinen CP-vamma. Jo vastasyntyneellä useat aivoalueet aktivoituivat käden alueen kosketusärsykkeen jälkeen. Tuntoaivokuoren aktiivisuus poikkesi kuitenkin oleellisesti aikuisesta: tietyt aikuistyyppiset aivovasteet puuttuivat vastasyntyneiltä täysin heijastaen vastasyntyneen vauvan hermoston keskeneräistä kehitysvaihetta. Tuntoaivovasteet kehittyivät iän myötä järjestelmällisesti siten, että kaksivuotiailla ne alkoivat morfologisesti muistuttaa aikuisten vasteita. Pikkukeskosten primaarisen tuntoaivokuoren vaste oli lasketussa ajassa heikompi kuin terveillä täysaikaisilla vauvoilla, mikä voi johtua pienemmästä aktivoituneesta hermosolujoukosta tai aktivaation epäsynkroniasta. Sekundaarisen tuntoaivokuoren vasteen puuttuminen liittyi poikkeaviin ultraääni- ja magneettikuvauslöydöksiin. Tämän havainnon ennusteellista merkitystä selvitetään parhaillaan seurantatutkimuksella. CP-vammaisilla nuorilla tuntoaivovasteissa havaittiin verrokkeihin nähden useita poikkeavuuksia, jotka olivat osin laaja-alaisempia kuin oli pääteltävissä kliinisistä oireista tai aivojen rakenteellisesta vauriosta. Esimerkiksi potilailla, joiden sairauden taustalla oli subkortikaalinen aivovaurio, etu- ja pikkusormien edustusalueet tuntoaivokuorella olivat verrokkeihin nähden lähempänä toisiaan sekä vaurion puoleisessa että vastakkaisessa aivopuoliskossa. Aivojen erilaisten rakenteellisten vaurioiden aiheuttamien toiminnallisten muutosten tarkempi ymmärtäminen voi osoittautua merkittäväksi CP-potilaiden kuntoutuksen ja hoidon yksilöllisessä räätälöinnissä

Kosketuksen käsittely ihmisen tunto- ja kuuloaivokuorella

Tactile sensation plays an important role in everyday life. While the somatosensory system has been studied extensively, the majority of information has come from studies using animal models. Recent development of high-resolution anatomical and functional imaging techniques has enabled the non-invasive study of human somatosensory cortex and thalamus. This thesis provides new insights into the functional organization of the human brain areas involved in tactile processing using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). The thesis also demonstrates certain optimizations of MEG and fMRI methods. Tactile digit stimulation elicited stimulus-specific responses in a number of brain areas. Contralateral activation was observed in somatosensory thalamus (Study II), primary somatosensory cortex (SI; I, III, IV), and post-auditory belt area (III). Bilateral activation was observed in secondary somatosensory cortex (SII; II, III, IV). Ipsilateral activation was found in the post-central gyrus (area 2 of SI cortex; IV). In addition, phasic deactivation was observed within ipsilateral SI cortex and bilateral primary motor cortex (IV). Detailed investigation of the tactile responses demonstrated that the arrangement of distal-proximal finger representations in area 3b of SI in humans is similar to that found in monkeys (I). An optimized MEG approach was sufficient to resolve such fine detail in functional organization. The SII region appeared to contain double representations for fingers and toes (II). The detection of activations in the SII region and thalamus improved at the individual and group levels when cardiac-gated fMRI was used (II). Better detection of body part representations at the individual level is an important improvement, because identification of individual representations is crucial for studying brain plasticity in somatosensory areas. The posterior auditory belt area demonstrated responses to both auditory and tactile stimuli (III), implicating this area as a physiological substrate for the auditory-tactile interaction observed in earlier psychophysical studies. Comparison of different smoothing parameters (III) demonstrated that proper evaluation of co-activation should be based on individual subject analysis with minimal or no smoothing. Tactile input consistently influenced area 3b of the human ipsilateral SI cortex (IV). The observed phasic negative fMRI response is proposed to result from interhemispheric inhibition via trans-callosal connections. This thesis contributes to a growing body of human data suggesting that processing of tactile stimuli involves multiple brain areas, with different spatial patterns of cortical activation for different stimuli

Dynamic Oscillatory Interactions Between Neural Attention and Sensorimotor Systems

The adaptive and flexible ability of the human brain to preference the processing of salient environmental features in the visual space is essential to normative cognitive function, and various neurologically afflicted patient groups report negative impacts on visual attention. While the brain-bases of human attentional processing have begun to be unraveled, very little is known regarding the interactions between attention systems and systems supporting sensory and motor processing. This is essential, as these interactions are dynamic; evolving rapidly in time and across a wide range of functionally defined rhythmic frequencies. Using magnetoencephalography (MEG) and a range of novel cognitive paradigms and analytical techniques, this work attempts to fill critical gaps in this knowledge. Specifically, we unravel the role of dynamic oscillatory interactions between attention and three sensorimotor systems. First, we establish the importance of sub-second occipital alpha (8 – 14 Hz) oscillatory responses in visual distractor suppression during selective attention (Chapter 1) and their essential role in fronto-parietal attention networks during visual orienting (Chapter 2). Next, we examine the divergent effects of directed attention on multi-frequency primary somatosensory neural oscillations in the theta (4 – 8 Hz), alpha, and beta (18 – 26 Hz) bands (Chapter 3). Finally, we extend these findings to the motor system (Chapter 4), and find that the frontal and parietal beta-frequency oscillations known to support motor planning and execution are modulated equivalently by differing subtypes of attentional interference, whereas frontal gamma (64 – 84 Hz) oscillations specifically index the superadditive effect of this interference. These findings provide new insight into the dynamic nature of attention-sensorimotor interactions in the human brain, and will be the foundation for groundbreaking new studies of attentional deficits in patients with common neurological disorders (e.g., Alzheimer’s disease, HIV-associated neurocognitive disorders, Parkinson’s disease). With an enhanced knowledge of the temporal and spectral definitions of these impairments, new therapeutic interventions utilizing frequency-targeted neural stimulation can be developed

Störung der sensomotorischen Integration bei der Amyotrophen Lateralsklerose

Die Amyotrophe Lateralsklerose (ALS) ist durch die Degeneration des ersten und zweiten Motoneurons charakterisiert, jedoch existieren zunehmend Hinweise auf einen systemischen Charakter. So wurden kognitive Dysfunktion, Sensibilitätsstörungen und Veränderungen sensorischer Fasern beobachtet. Im Vordergrund stehen Untersuchungen zu somatosensorisch evozierten Potentialen (SEP), die bisherigen Ergebnisse sind kontrovers. Die Magnetenzephalographie (MEG) ist eine hochauflösende Untersuchungsmethode, die die durch zerebrale Aktivität generierten Felder aufzeichnet. Ziel der Arbeit ist die Darstellung der kortikalen Antwort nach elektrischer Medianus- und mechanischer Fingerbeerenstimulation und Erfassung von Störungen der sensomotorischen Integration bei ALS- Patienten. Hierzu wurden 31 ALS-Patienten und 29 Kontrollpersonen eingeschlossen und SEPs beider Körperhälften via MEG erfasst. Statistisch signifikant stellte sich eine größere Signalamplitude der Kontrollpersonen im Vergleich zu den Patienten nach Reizung des rechten Zeigefingers dar. Die kortikalen Antworten nach Medianusstimulation traten im kontralateralen S1 und S2 auf. Nach Medianusreizung links imponierte eine signifikant höhere Antwort der Patienten mit bulbärem Onset, ähnliche Ergebnisse wurden zuvor demonstriert. Zusammenfassend scheint das sensorische System bei ALS-Patienten auf Kortexebene nicht vollständig intakt zu sein; minimale Veränderungen können wertvolle Informationen für das Verständnis der Erkrankung liefern

Event-related potential studies of somatosensory detection and discrimination.

This thesis contains four studies, the first examining methodology issues and four subsequent ones examining somatosensory cortical processing using event-related potentials (ERPs). The methodology section consists of 2 experiments. The first compared the latency variability in stimulus presentation between 3 computers. The second monitored the applied force of the vibration stimuli under experimental conditions to ensure that the chosen method for somatosensory stimulus presentation was consistent and reliable. The next study involved 3 experiments that aimed to characterize the mid to long latency somatosensory event-related potentials to different duration vibratory stimuli using both intracranial and scalp recording. The results revealed differences in the waveform morphology of the responses to and on-off responses, which had not previously been noted in the somatosensory system. The third and fourth studies each consisted of 2 experiments. These examined the discrimination between vibratory stimuli using an odd-ball paradigm to try to obtain a possible 'mismatch' response, similar to that reported in the auditory system. The aim of this study was to clarify some of the discrepancies in the literature surrounding the somatosensory mismatch response and to further characterize this response. The results from intracranial and scalp ERP recordings showed a two-component, negative-positive mismatch response over the anterior parietal region and a negative component over the superior pre-frontal region in response to changes in both frequency and duration. The negative component over the frontal region had never before been described. The last study explored possible interactions between somatosensory and auditory cortical potentials in response to spatially and temporally synchronized auditory and vibratory stimuli. The results showed clear interactions in the cortical responses to combined auditory and somatosensory stimuli in both standard and mismatch conditions