Haptic contents of a movie dynamically engage the spectator's sensorimotor cortex.

Observation of another person's actions and feelings activates brain areas that support similar functions in the observer, thereby facilitating inferences about the other's mental and bodily states. In real life, events eliciting this kind of vicarious brain activations are intermingled with other complex, ever-changing stimuli in the environment. One practical approach to study the neural underpinnings of real-life vicarious perception is to image brain activity during movie viewing. Here the goal was to find out how observed haptic events in a silent movie would affect the spectator's sensorimotor cortex. The functional state of the sensorimotor cortex was monitored by analyzing, in 16 healthy subjects, magnetoencephalographic (MEG) responses to tactile finger stimuli that were presented once per second throughout the session. Using canonical correlation analysis and spatial filtering, consistent single-trial responses across subjects were uncovered, and their waveform changes throughout the movie were quantified. The long-latency (85-175 ms) parts of the responses were modulated in concordance with the participants' average moment-by-moment ratings of own engagement in the haptic content of the movie (correlation r = 0.49; ratings collected after the MEG session). The results, obtained by using novel signal-analysis approaches, demonstrate that the functional state of the human sensorimotor cortex fluctuates in a fine-grained manner even during passive observation of temporally varying haptic events. Hum Brain Mapp 37:4061-4068, 2016. © 2016 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.

Brain responds to another person's eye blinks in a natural setting-the more empathetic the viewer the stronger the responses.

An observer's brain is known to respond to another person's small nonverbal signals, such as gaze shifts and eye blinks. Here we aimed to find out how an observer's brain reacts to a speaker's eye blinks in the presence of other audiovisual information. Magnetoencephalographic brain responses along with eye gaze were recorded from 13 adults who watched a video of a person telling a story. The video was presented first without sound (visual), then with sound (audiovisual), and finally the audio story was presented with a still-frame picture on the screen (audio control). The viewers mainly gazed at the eye region of the speaker. Their saccades were suppressed at about 180 ms after the start of the speaker's blinks, a subsequent increase of saccade occurence to the base level, or higher, at around 340 ms. The suppression occurred in visual and audiovisual conditions but not during the control audio presentation. Prominent brain responses to blinks peaked in the viewer's occipital cortex at about 250 ms, with no differences in mean peak amplitudes or latencies between visual and audiovisual conditions. During the audiovisual, but not visual-only, presentation, the responses were the stronger the more empathetic the subject was according to the Empathic Concern score of the Interpersonal Reactivity Index questionnaire (Spearman's rank correlation, 0.73). The other person's eye blinks, nonverbal signs that often go unnoticed, thus elicited clear brain responses even in the presence of attention-attracting audiovisual information from the narrative, with stronger responses in people with higher empathy scores.

Neuromagnetic brain responses to other person's eye blinks seen on video.

Eye blinks, typically occurring 15-20 times per minute, rarely capture attention during face-to-face interaction. To determine the extent to which eye blinks affect the viewer's brain activity, we recorded magnetoencephalographic brain responses to natural blinks, and to the same blinks slowed down to 38% of the original speed. The stimuli were presented on video once every 2.3-6.2 s. As a control, we presented two horizontal black bars moving with the same time courses and the same extent as the eyelids in the blink video. Both types of blinks and bars elicited clear responses peaking at about 200 ms in the occipital areas, with no systematic differences between hemispheres. For the bars, these main responses were (as expected) weaker (by 24%) and later (by 33 ms) to slow-motion than normal-speed stimuli. For blinks, however, the responses to both normal-speed and slow-motion stimuli were of the same amplitude and latency. Our results demonstrate that the brain not only responds to other persons' eye blinks, but that the responses are as fast and of equal size even when the blinks are considerably slowed down. We interpret this finding to reflect the increased social salience of the slowed-down blinks that counteracted the general tendency of the brain to react more weakly and more slowly to slowly- vs. quickly-changing stimuli. This finding may relate to the social importance of facial gestures, including eye blinks.

Reactivity of sensorimotor oscillations is altered in children with hemiplegic cerebral palsy: A magnetoencephalographic study.

Cerebral palsy (CP) is characterized by difficulty in control of movement and posture due to brain damage during early development. In addition, tactile discrimination deficits are prevalent in CP. To study the function of somatosensory and motor systems in CP, we compared the reactivity of sensorimotor cortical oscillations to median nerve stimulation in 12 hemiplegic CP children vs. 12 typically developing children using magnetoencephalography. We also determined the primary cortical somatosensory and motor representation areas of the affected hand in the CP children using somatosensory-evoked magnetic fields and navigated transcranial magnetic stimulation, respectively. We hypothesized that the reactivity of the sensorimotor oscillations in alpha (10 Hz) and beta (20 Hz) bands would be altered in CP and that the beta-band reactivity would depend on the individual pattern of motor representation. Accordingly, in children with CP, suppression and rebound of both oscillations after stimulation of the contralateral hand were smaller in the lesioned than intact hemisphere. Furthermore, in two of the three children with CP having ipsilateral motor representation, the beta- but not alpha-band modulations were absent in both hemispheres after affected hand stimulation suggesting abnormal sensorimotor network interactions in these individuals. The results are consistent with widespread alterations in information processing in the sensorimotor system and complement current understanding of sensorimotor network development after early brain insults. Precise knowledge of the functional sensorimotor network organization may be useful in tailoring individual rehabilitation for people with CP.

Cortical somatosensory processing measured by magnetoencephalography predicts neurodevelopment in extremely low-gestational-age infants.

BACKGROUND: Higher cortical function during sensory processing can be examined by recording specific somatosensory-evoked magnetic fields (SEFs) with magnetoencephalography (MEG). We evaluated whether, in extremely low-gestational-age (ELGA) infants, abnormalities in MEG-recorded SEFs at term age are associated with adverse neurodevelopment at 2 y of corrected age. METHODS: SEFs to tactile stimulation of the index finger were recorded at term age in 30 ELGA infants (26.5 ± 1.2 wk, birth weight: 884 g ± 181 g). Neurodevelopment was evaluated at 2 y of corrected age. Controls were 11 healthy term infants. RESULTS: In nine of the ELGA infants (30.0%), SEFs were categorized as abnormal on the basis of lack of response from secondary somatosensory cortex (SII). At 2 y, these infants had a significantly worse mean developmental quotient and locomotor subscale on the Griffiths Mental Development Scales than the ELGA infants with normal responses. Mild white matter abnormalities in magnetic resonance imaging at term age were detected in 21% of infants, but these abnormalities were not associated with adverse neurodevelopment. CONCLUSION: Abnormal SII responses at term predict adverse neuromotor development at 2 y of corrected age. This adverse development may not be foreseen with conventional neuroimaging methods, suggesting a role for evaluating SII responses in the developmental risk assessment of ELGA infants.

Bilateral alterations in somatosensory cortical processing in hemiplegic cerebral palsy.

AIM: In individuals with cerebral palsy (CP), cerebral insults during early development may induce profound reorganization of the motor representation. This study determined the extent of alterations in cortical somatosensory functions in adolescents with hemiplegic CP with subcortical brain lesions. METHOD: We recorded somatosensory evoked magnetic fields in response to hand area stimulation from eight adolescents with hemiplegic CP (five females and three males; mean age 14y 6mo, SD 2y 3mo) and eight age- and sex-matched healthy comparison adolescents (mean age 15y 4mo, SD 2y 4mo). All participants in the CP group had purely subcortical brain lesions in magnetic resonance images. RESULTS: The somatosensory representation of the affected limb was contralateral (i.e. ipsilesional), but detailed inspection of the evoked responses showed alterations bilaterally. In the primary somatosensory cortex, the representation areas of digits II and V were in both hemispheres closer to each other in participants with CP than in comparison participants [ANOVA main effect group F(1,14) =5.58; p=0.03]. In addition, the morphology of median nerve evoked fields was altered in the participants with CP. INTERPRETATION: In hemiplegic CP, modification of the somatosensory cortical network extends beyond what would be expected based on the unilateral symptoms and the anatomical lesion. Further understanding of the functional alterations in the sensorimotor networks may aid in developing more precisely designed rehabilitation strategies.

Importance of the left auditory areas in chord discrimination in music experts as demonstrated by MEG.

The brain basis behind musical competence in its various forms is not yet known. To determine the pattern of hemispheric lateralization during sound-change discrimination, we recorded the magnetic counterpart of the electrical mismatch negativity (MMNm) responses in professional musicians, musical participants (with high scores in the musicality tests but without professional training in music) and non-musicians. While watching a silenced video, they were presented with short sounds with frequency and duration deviants and C major chords with C minor chords as deviants. MMNm to chord deviants was stronger in both musicians and musical participants than in non-musicians, particularly in their left hemisphere. No group differences were obtained in the MMNm strength in the right hemisphere in any of the conditions or in the left hemisphere in the case of frequency or duration deviants. Thus, in addition to professional training in music, musical aptitude (combined with lower-level musical training) is also reflected in brain functioning related to sound discrimination. The present magnetoencephalographic evidence therefore indicates that the sound discrimination abilities may be differentially distributed in the brain in musically competent and naïve participants, especially in a musical context established by chord stimuli: the higher forms of musical competence engage both auditory cortices in an integrative manner.

Secondary somatosensory cortex evoked responses and 6-year neurodevelopmental outcome in extremely preterm children.

OBJECTIVE: We assessed in extremely preterm born (EPB) children whether secondary somatosensory cortex (SII) responses recorded with magnetoencephalography (MEG) at term-equivalent age (TEA) correlate with neurodevelopmental outcome at age 6 years. Secondly, we assessed whether SII responses differ between 6-year-old EPB and term-born (TB) children. METHODS: 39 EPB children underwent MEG with tactile stimulation at TEA. At age 6 years, 32 EPB and 26 TB children underwent MEG including a sensorimotor task requiring attention and motor inhibition. SII responses to tactile stimulation were modeled with equivalent current dipoles. Neurological outcome, motor competence, and general cognitive ability were prospectively evaluated at age 6 years. RESULTS: Unilaterally absent SII response at TEA was associated with abnormal motor competence in 6-year-old EPB children (p = 0.03). At age 6 years, SII responses were bilaterally detectable in most EPB (88%) and TB (92%) children (group comparison, p = 0.69). Motor inhibition was associated with decreased SII peak latencies in TB children, but EPB children lacked this effect (p = 0.02). CONCLUSIONS: Unilateral absence of an SII response at TEA predicted poorer motor outcome in EPB children. SIGNIFICANCE: Neurophysiological methods may provide new means for outcome prognostication in EPB children.

Music and speech listening enhance the recovery of early sensory processing after stroke.

Our surrounding auditory environment has a dramatic influence on the development of basic auditory and cognitive skills, but little is known about how it influences the recovery of these skills after neural damage. Here, we studied the long-term effects of daily music and speech listening on auditory sensory memory after middle cerebral artery (MCA) stroke. In the acute recovery phase, 60 patients who had middle cerebral artery stroke were randomly assigned to a music listening group, an audio book listening group, or a control group. Auditory sensory memory, as indexed by the magnetic MMN (MMNm) response to changes in sound frequency and duration, was measured 1 week (baseline), 3 months, and 6 months after the stroke with whole-head magnetoencephalography recordings. Fifty-four patients completed the study. Results showed that the amplitude of the frequency MMNm increased significantly more in both music and audio book groups than in the control group during the 6-month poststroke period. In contrast, the duration MMNm amplitude increased more in the audio book group than in the other groups. Moreover, changes in the frequency MMNm amplitude correlated significantly with the behavioral improvement of verbal memory and focused attention induced by music listening. These findings demonstrate that merely listening to music and speech after neural damage can induce long-term plastic changes in early sensory processing, which, in turn, may facilitate the recovery of higher cognitive functions. The neural mechanisms potentially underlying this effect are discussed.

Observing touch activates human primary somatosensory cortex.

We used magnetoencephalography to show that the human primary somatosensory (SI) cortex is activated by mere observation of touch. Somatosensory evoked fields were measured from adult human subjects in two conditions. First, the experimenter touched the subject's right hand with her index finger (Experienced touch). In the second condition, the experimenter touched her own hand in a similar manner (Observed touch). Minimum current estimates were computed across three consecutive 300-ms time windows (0-300, 300-600 and 600-900 ms) with respect to touch onset. During 'Experienced touch', as expected, the contralateral (left) SI cortex was strongly activated in the 0-300 ms time window. In the same time window, statistically significant activity also occurred in the ipsilateral SI, although it was only 2.5% of the strength of the contralateral activation; the ipsilateral activation continued in the 300-600 ms time window. During 'Observed touch', the left SI cortex was activated during the 300-600 ms interval; the activation strength was 7.5% of that during the significantly activated period (0-300 ms) of 'Experienced touch'. The results suggest that when people observe somebody else being touched, activation of their own somatosensory circuitry may contribute to understanding of the other person's somatosensory experience.

Early dissociation of face and object processing: a magnetoencephalographic study.

The early dissociation in cortical responses to faces and objects was explored with magnetoencephalographic (MEG) recordings and source localization. To control for differences in the low-level stimulus features, which are known to modulate early brain responses, we created a novel set of stimuli so that their combinations did not have any differences in the visual-field location, spatial frequency, or luminance contrast. Differing responses to face and object (flower) stimuli were found at about 100 ms after stimulus onset in the occipital cortex. Our data also confirm that the brain response to a complex visual stimulus is not merely a sum of the responses to its constituent parts; the nonlinearity in the response was largest for meaningful stimuli.

Does very premature birth affect the functioning of the somatosensory cortex?--A magnetoencephalography study.

Increased survival of extremely low birth weight infants has led to a need for new prognostic methods to predict possible future neurological impairment. We investigated the early development of the somatosensory system by recording the somatosensory evoked magnetic fields (SEFs) during natural sleep at fullterm age in 16 very prematurely born infants and 16 healthy newborns born at term. The purpose was to determine possible changes in the function of the somatosensory cortex in the prematurely born infants by comparing the latency, strength, location and morphology of the SEFs with those of healthy fullterm newborns. We recorded reliable SEFs in all patients and controls. The equivalent current dipole (ECD) strength of the first cortical response, M60, was significantly lower in the patients. Otherwise, the general morphology and latency of the SEFs were similar in the two groups of babies. The similar response latencies in the two groups indicate normally developed conduction in the somatosensory system of the prematurely born infants. The attenuated ECD strength may reflect weaker synchrony in firing or a smaller number of the cortical neurons activated by the somatosensory stimulation. At the individual level, in four of the preterm infants, a later M200 response was not present or could not be modeled: all of them had lesions of the underlying hemisphere depicted by ultrasound and magnetic resonance imaging.

Language impairment is reflected in auditory evoked fields.

Specific language impairment (SLI) is diagnosed when a child has problems in producing or understanding language despite having a normal IQ and there being no other obvious explanation. There can be several associated problems, and no single underlying cause has yet been identified. Some theories propose problems in auditory processing, specifically in the discrimination of sound frequency or rapid temporal frequency changes. We compared automatic cortical speech-sound processing and discrimination between a group of children with SLI and control children with normal language development (mean age: 6.6 years; range: 5-7 years). We measured auditory evoked magnetic fields using two sets of CV syllables, one with a changing consonant /da/ba/ga/ and another one with a changing vowel /su/so/sy/ in an oddball paradigm. The P1m responses for onsets of repetitive stimuli were weaker in the SLI group whereas no significant group differences were found in the mismatch responses. The results indicate that the SLI group, having weaker responses to the onsets of sounds, might have slightly depressed sensory encoding.

Newborns discriminate novel from harmonic sounds: a study using magnetoencephalography.

OBJECTIVE: We investigated whether newborns respond differently to novel and deviant sounds during quiet sleep. METHODS: Twelve healthy neonates were presented with a three-stimulus oddball paradigm, consisting of frequent standard (76%), infrequent deviant (12%), and infrequent novel stimuli (12%). The standards and deviants were counterbalanced between the newborns and consisted of 500 and 750 Hz tones with two upper harmonics. The novel stimuli contained animal, human, and mechanical sounds. All stimuli had a duration of 300 ms and the stimulus onset asynchrony was 1s. Evoked magnetic responses during quiet sleep were recorded and averaged offline. RESULTS: Two deflections peaking at 345 and 615 ms after stimulus onset were observed in the evoked responses of most of the newborns. The first deflection was larger to novel and deviant stimuli than to the standard and, furthermore, larger to novel than to deviant stimuli. The second deflection was larger to novel and deviant stimuli than to standards, but did not differ between the novels and deviants. CONCLUSIONS: The two deflections found in the present study reflect different mechanisms of auditory change detection and discriminative processes. SIGNIFICANCE: The early brain indicators of novelty detection may be crucial in assessing the normal and abnormal cortical function in newborns. Further, studying evoked magnetic fields to complex auditory stimulation in healthy newborns is needed for studying the newborns at-risk for cognitive or language problems.

Lack of Cortical Correlates of Response Inhibition in 6-Year-Olds Born Extremely Preterm - Evidence from a Go/NoGo Task in Magnetoencephalographic Recordings.

Children born extremely preterm (EPT) may have difficulties in response inhibition, but the neural basis of such problems is unknown. We recorded magnetoencephalography (MEG) during a somatosensory Go/NoGo task in 6-year-old children born EPT (n = 22) and in children born full term (FT; n = 21). The children received tactile stimuli randomly to their left little (target) and index (non-target) finger and were instructed to squeeze a soft toy with the opposite hand every time they felt a stimulus on the little finger. Behaviorally, the EPT children performed worse than the FT children, both in responding to the target finger stimulation and in refraining from responding to the non-target finger stimulation. In MEG, after the non-target finger stimulation (i.e., during the response inhibition), the sensorimotor alpha oscillation levels in the contralateral-to-squeeze hemisphere were elevated in the FT children when compared with a condition with corresponding stimulation but no task (instead the children were listening to a story and not attending to the fingers). This NoGo task effect was absent in the EPT children. Further, in the sensorimotor cortex contralateral to the tactile stimulation, the post-stimulus suppression was less pronounced in the EPT than FT children. We suggest that the missing NoGo task effect and lower suppression of sensorimotor oscillations are markers of deficient functioning of the sensorimotor networks in the EPT children.

Magnetic fields evoked by speech sounds in preschool children.

OBJECTIVE: Our objective was to study how well the auditory evoked magnetic fields (EF) reflect the behavioral discrimination of speech sounds in preschool children, and if they reveal the same information as simultaneously recorded evoked potentials (EP). METHODS: EFs and EPs were recorded in 11 preschool children (mean age 6 years 9 months) using an oddball paradigm with two sets of speech stimuli consisting both of one standard and two deviants. After the brain activity recording, children were tested on behavioural discrimination of the same stimuli presented in pairs. RESULTS: There was a mismatch negativity (MMN) calculated from difference curves and its magnetic counterpart MMNm measured from the original responses only to those deviants, which were behaviourally easiest to discriminate from the standards. In addition, EF revealed significant differences between the locations of the activation depending on the hemisphere and stimulus properties. CONCLUSIONS: EF, in addition to reflecting the sound-discrimination accuracy in a similar manner as EP, also reflected the spatial differences in activation of the temporal lobes. SIGNIFICANCE: These results suggest that both EPs and EFs are feasible for investigating the neural basis of sound discrimination in young children. The recording of EFs with its high spatial resolution reveals information on the location of the activated neural sources.

Evaluation of somatosensory cortical processing in extremely preterm infants at term with MEG and EEG.

OBJECTIVE: Prior studies on extremely preterm infants have reported long-term prognostic value of absent secondary somatosensory cortex (SII) responses in magnetoencephalography (MEG) at term. The present work (i) further examines the potential added value of SII responses in neonatal neurological evaluation of preterm infants, and (ii) tests whether SII responses are detectable in routine neonatal electroencephalogram complemented with median nerve stimulation (EEG-SEP). METHODS: Altogether 29 infants born <28 gestational weeks underwent MEG, MRI, and neonatal neurological examination at term age, and Hempel neurological examination at 2-years corrected age. Term-age EEG-SEP was available for seven infants. RESULTS: While in neonatal neurological examination severely abnormal finding predicted unfavorable outcome in 2/2 infants, outcome was unfavorable also in 3/9 (33%) moderately abnormal and in 5/18 (28%) mildly abnormal/normal infants. Of these eight infants four had unilaterally absent SII responses in MEG, compared with only two of the 24 infants with favorable outcome. Furthermore, SII responses (when present in MEG) were also usually detectable in EEG-SEP. CONCLUSIONS: Complementing clinical EEG recording with SEP holds promise for valuable extension of neonatal neurophysiological assessment. SIGNIFICANCE: Multimodal study of EEG and sensory evoked responses is informative, safe, and cheap, and it can be readily performed at bedside.

Somatosensory evoked potentials and magnetic fields elicited by tactile stimulation of the hand during active and quiet sleep in newborns.

OBJECTIVE: Our objective was to characterize the effects of sleep stages on tactile somatosensory evoked responses in full-term newborns. METHODS: Somatosensory evoked potentials (SEPs) and magnetic fields (SEFs) to tactile stimulation of the tip of the index finger and/or thenar eminence were measured from 14 healthy newborns. The stimulus was a gentle tap produced by a moving membrane driven by an air-pressure pulse. RESULTS: SEPs and SEFs to tactile stimulation of the skin were similar in waveform and latency to SEPs known to be produced by electrical stimulation of the fingertip of neonates. The two most distinguishable positive deflections of SEPs, P1 and P2, within 300 ms of the stimulation, and their magnetic counterparts were clearly smaller in active compared to quiet sleep. CONCLUSIONS: Our study demonstrates for the first time that it is possible to record SEFs in neonates, and that clear late cortical somatosensory responses are produced by tactile stimulation. In addition, the effect of sleep stage on these responses indicates differences in the processing of the incoming information, at least in the somatosensory modality, in active and quiet sleep. SIGNIFICANCE: Tactile stimulation may be useful as a completely non-invasive technique for studying the physiology of the somatosensory system in neonates. Methodologically, since the effect of sleep stage is profound, one must carefully monitor the sleep stages in studies of event-related responses in newborns, or else this effect may confound the phenomena being studied.

Brain responses to changes in speech sound durations differ between infants with and without familial risk for dyslexia.

A specific learning disability, developmental dyslexia, is a language-based disorder that is shown to be strongly familial. Therefore, infants born to families with a history of the disorder are at an elevated risk for the disorder. However, little is known of the potential early markers of dyslexia. Here we report differences between 6-month-old infants with and without high risk of familial dyslexia in brain electrical activation generated by changes in the temporal structure of speech sounds, a critical cueing feature in speech. We measured event-related brain responses to consonant duration changes embedded in ata pseudowords applying an oddball paradigm, in which pseudoword tokens with varying /t/ duration were presented as frequent standard (80%) or as rare deviant stimuli (each 10%) with an interval of 610 msec between the stimuli. The infants at risk differ from control infants in both their initial responsiveness to sounds per se and in their change-detection responses dependent on the stimulus context. These results show that infants at risk due to a familial background of reading problems process auditory temporal cues of speech sounds differently from infants without such a risk even before they learn to speak.

Development of Human Somatosensory Cortical Functions - What have We Learned from Magnetoencephalography: A Review.

The mysteries of early development of cortical processing in humans have started to unravel with the help of new non-invasive brain research tools like multichannel magnetoencephalography (MEG). In this review, we evaluate, within a wider neuroscientific and clinical context, the value of MEG in studying normal and disturbed functional development of the human somatosensory system. The combination of excellent temporal resolution and good localization accuracy provided by MEG has, in the case of somatosensory studies, enabled the differentiation of activation patterns from the newborn's primary (SI) and secondary somatosensory (SII) areas. Furthermore, MEG has shown that the functioning of both SI and SII in newborns has particular immature features in comparison with adults. In extremely preterm infants, the neonatal MEG response from SII also seems to potentially predict developmental outcome: those lacking SII responses at term show worse motor performance at age 2 years than those with normal SII responses at term. In older children with unilateral early brain lesions, bilateral alterations in somatosensory cortical activation detected in MEG imply that the impact of a localized insult may have an unexpectedly wide effect on cortical somatosensory networks. The achievements over the last decade show that MEG provides a unique approach for studying the development of the somatosensory system and its disturbances in childhood. MEG well complements other neuroimaging methods in studies of cortical processes in the developing brain.