A magnetoencephalographic study of face processing: M170, gamma‐band oscillations and source localization

EEG studies suggested that the N170 ERP and Gamma‐band responses to faces reflect early and later stages of a multiple‐level face‐perception mechanism, respectively. However, these conclusions should be considered cautiously because EEG‐recorded Gamma may be contaminated by noncephalic activity such as microsaccades. Moreover, EEG studies of Gamma cannot easily reveal its intracranial sources. Here we recorded MEG rather than EEG, assessed the sources of the M170 and Gamma oscillations using beamformer, and explored the sensitivity of these neural manifestations to global, featural and configural information in faces. The M170 was larger in response to faces and face components than in response to watches. Scrambling the configuration of the inner components of the face even if presented without the face contour reduced and delayed the M170. The amplitude of MEG Gamma oscillations (30–70 Hz) was higher than baseline during an epoch between 230–570 ms from stimulus onset and was particularly sensitive to the configuration of the stimuli, regardless of their category. However, in the lower part of this frequency range (30–40 Hz) only physiognomic stimuli elevated the MEG above baseline. Both the M170 and Gamma were generated in a posterior‐ventral network including the fusiform, inferior‐occipital and lingual gyri, all in the right hemisphere. The generation of Gamma involved additional sources in the visual system, bilaterally. We suggest that the evoked M170 manifests a face‐perception mechanism based on the global characteristics of face, whereas the induced Gamma oscillations are associated with the integration of visual input into a pre‐existent coherent perceptual representation. Hum Brain Mapp, 2013. © 2012 Wiley Periodicals, Inc.     

Time course of gamma‐band oscillation associated with face processing in the inferior occipital gyrus and fusiform gyrus: A combined fMRI and MEG study

Debate continues over whether the inferior occipital gyrus (IOG) or the fusiform gyrus (FG) represents the first stage of face processing and what role these brain regions play. We investigated this issue by combining functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) in normal adults. Participants passively observed upright and inverted faces and houses. First, we identified the IOG and FG as face‐specific regions using fMRI. We applied beamforming source reconstruction and time–frequency analysis to MEG source signals to reveal the time course of gamma‐band activations in these regions. The results revealed that the right IOG showed higher gamma‐band activation in response to upright faces than to upright houses at 100 ms from the stimulus onset. Subsequently, the right FG showed greater gamma‐band response to upright faces versus upright houses at around 170 ms. The gamma‐band activation in the right IOG and right FG was larger in response to inverted faces than to upright faces at the later time window. These results suggest that (1) the gamma‐band activities occurs rapidly first in the IOG and next in the FG and (2) the gamma‐band activity in the right IOG at later time stages is involved in configuration processing for faces. Hum Brain Mapp 38:2067–2079, 2017. © 2017 Wiley Periodicals, Inc.     

Functional and structural correlates of the aging brain: Relating visual cortex (V1) gamma band responses to age‐related structural change

The gamma band response is thought to be a key neural signature of information processing in the mammalian brain, yet little is known about how age‐related maturation influences the γ‐band response. Recent MRI‐based studies have shown that brain maturation is accompanied by clear structural changes in both gray and white matter, yet the correspondence of these changes to brain function is unclear. The objective of this study was to relate visual cortex (V1) γ‐band responses to age‐related structural change. We evaluated MEG measured γ‐band responses to contrast gratings stimuli and structural MRIs from participants observed from two separate research centers (MEG lab at CUBRIC, Cardiff University, UK, and the Lurie Family Foundations MEG Imaging Center, (CHOP) at the Children's Hospital of Philadelphia). Pooled participant data (N = 59) ranged in age from 8.7 to 45.3 years. We assessed linear associations between age and MEG γ‐band frequency and amplitude, as well as between age and MRI volumetric parameters of the occipital lobe. Our MEG findings revealed a significant negative correlation for gamma band frequency versus age. Volumetric brain analysis from the occipital lobe also revealed significant negative correlations between age and the cortical thickness of pericalcarine and cuneus areas. Our functional MEG and structural MRI findings shows regionally specific changes due to maturation and may thus be informative for understanding physiological processes of neural development, maturation, and age‐related decline. In addition, this study represents (to our knowledge), the first published demonstration of multicenter data sharing across MEG centers. Hum Brain Mapp 33:2035–2046, 2012. © 2011 Wiley Periodicals, Inc.     

Neural responses to rigidly moving faces displaying shifts in social attention investigated with fMRI and MEG

A widely adopted neural model of face perception (Haxby, Hoffman, & Gobbini, 2000) proposes that the posterior superior temporal sulcus (STS) represents the changeable features of a face, while the face-responsive fusiform gyrus (FFA) encodes invariant aspects of facial structure. ‘Changeable features’ of a face can include rigid and non-rigid movements. The current study investigated neural responses to rigid, moving faces displaying shifts in social attention. Both functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) were used to investigate neural responses elicited when participants viewed video clips in which actors made a rigid shift of attention, signalled congruently from both the eyes and head. These responses were compared to those elicited by viewing static faces displaying stationary social attention information or a scrambled video displaying directional motion. Both the fMRI and MEG analyses demonstrated heightened responses along the STS to turning heads compared to static faces or scrambled movement conditions. The FFA responded to both turning heads and static faces, showing only a slight increase in response to the dynamic stimuli. These results establish the applicability of the Haxby model to the perception of rigid face motions expressing changes in social attention direction. Furthermore, the MEG beamforming analyses found an STS response in an upper frequency band (30-80 Hz) which peaked in the right anterior region. These findings, derived from two complementary neuroimaging techniques, clarify the contribution of the STS during the encoding of rigid facial action patterns of social attention, emphasising the role of anterior sulcal regions alongside previously observed posterior areas.     

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.     

Individual peak gamma frequency predicts switch rate in perceptual rivalry

Perceptual rivalry—the experience of alternation between two mutually exclusive interpretations of an ambiguous image—provides powerful opportunities to study conscious awareness. It is known that individual subjects experience perceptual alternations for various types of bistable stimuli at distinct rates, and this a stable, heritable trait. Also stable and heritable is the peak frequency of induced gamma‐band (30–100 Hz) oscillation of a population‐level response in occipital cortex to simple visual patterns, which has been established as a neural correlate of conscious processing. Interestingly, models for rivalry alternation rate and for the frequency of population‐level oscillation have both cited inhibitory connections in cortex as crucial determinants of individual differences, and yet the relationship between these two variables has not yet been investigated. Here, we used magnetoencephalography to compare differences in alternation rate for binocular and monocular types of perceptual rivalry to differences in evoked and induced gamma‐band frequency of neuromagnetic brain responses to simple nonrivalrous grating stimuli. For both types of bistable images, alternation rate was inversely correlated with the peak frequency of late evoked gamma activity in primary visual cortex (200–400 ms latency). Our results advance models of inhibition that account for subtle variation in normal visual cortex, and shed light on how small differences in anatomy and physiology relate to individual cognition and performance. Hum Brain Mapp 36:566–576, 2015. © 2014 Wiley Periodicals, Inc .     

Temporal dynamics of face repetition suppression

Single-unit recordings and functional brain imaging studies have shown reduced neural responses to repeated stimuli in the visual cortex. Using MEG, we compared responses evoked by repetitions of neutral faces to those evoked by fearful faces, which were either task relevant (targets) or irrelevant (distracters). Faces evoked a bi-phasic response in extrastriate cortex, peaking at 160–185 ms and at 220–250 ms, with stronger responses to neutral faces at the earlier interval and stronger responses to fearful faces at the later interval. At both latencies, repetitions of neutral and fearful targets resulted in reduced amplitude of the MEG signal. Additionally, we found that the context in which targets were presented affected their processing: fearful distracters increased the responses evoked by both neutral and fearful targets. Our data indicate that valence enhancement and context effects can be detected in extrastriate visual cortex within 250 ms and that these processes likely reflect feedback from other regions.     

It takes longer to recognize the eyes than the whole face in humans.

Brain responses to eyes and whole face were studied by magnetoencephalography (MEG). We used five different visual stimuli, face with opened eyes, face with closed eyes, eyes, scrambled face, and hand. 1M was evoked in response to all kinds of stimuli but 2M peaking at approximately 180 ms was recorded only for face and eyes. The peak latencies of 1M and 2M and the interpeak latency 1M-2M to eyes were significantly longer than those to face, and there was no significant difference of latency between face with opened eyes and face with closed eyes. The 2M both for face and eyes was generated in the same area, the inferior temporal cortex, around the fusiform gyrus.     

Endogenously generated gamma‐band oscillations in early visual cortex: A neurofeedback study

Human subjects were trained with neurofeedback (NFB) to enhance the power of narrow‐band gamma oscillations in circumscribed regions of early visual cortex. To select the region and the oscillation frequency for NFB training, gamma oscillations were induced with locally presented drifting gratings. The source and frequency of these induced oscillations were determined using beamforming methods. During NFB training the power of narrow band gamma oscillations was continuously extracted from this source with online beamforming and converted into the pitch of a tone signal. We found that seven out of ten subjects were able to selectively increase the amplitude of gamma oscillations in the absence of visual stimulation. One subject however failed completely and two subjects succeeded to manipulate the feedback signal by contraction of muscles. In all subjects the attempts to enhance visual gamma oscillations were associated with an increase of beta oscillations over precentral/frontal regions. Only successful subjects exhibited an additional marked increase of theta oscillations over precentral/prefrontal and temporal regions whereas unsuccessful subjects showed an increase of alpha band oscillations over occipital regions. We argue that spatially confined networks in early visual cortex can be entrained to engage in narrow band gamma oscillations not only by visual stimuli but also by top down signals. We interpret the concomitant increase in beta oscillations as indication for an engagement of the fronto‐parietal attention network and the increase of theta oscillations as a correlate of imagery. Our finding support the application of NFB in disease conditions associated with impaired gamma synchronization.     

Seeing sounds and hearing sights: the influence of prior learning on current perception

It is well known that previous perceptual experiences alter subsequent perception, but the details of the neural underpinnings of this general phenomenon are still sketchy. Here, we ask whether previous experiences with an item (such as seeing a person's face) leads to the alteration of the neural correlates related to processing of the item as such, or whether it creates additional associative connections between such substrates and those activated during prior experience. To address this question, we used magnetoencephalography (MEG) to identify neural changes accompanying subjects' viewing of unfamiliar versus famous faces and hearing the names of unfamiliar versus famous names. We were interested in the nature of the involvement of auditory brain regions in the viewing of faces, and in the involvement of visual regions in the hearing of names. Evoked responses from MEG recordings for the names and faces conditions were localized to auditory and visual cortices, respectively. Unsurprisingly, peak activation strength of evoked responses was larger for famous versus nonfamous names within the superior temporal gyrus (STG), and was similar for famous and nonfamous faces in the occipital cortex. More relevant to the issue of experience on perception, peak activation strength in the STG was larger for viewed famous versus nonfamous faces, and peak activation within the occipital cortex was larger for heard famous versus nonfamous names. Critically, these experience-related responses were present within 150-250 msec of stimulus onset. These findings support the hypothesis that prior experiences may influence processing of faces and names such that perception encompasses more than what is imparted on the senses.     

Spatiotemporal dynamics in human visual cortex rapidly encode the emotional content of faces

Recognizing emotion in faces is important in human interaction and survival, yet existing studies do not paint a consistent picture of the neural representation supporting this task. To address this, we collected magnetoencephalography (MEG) data while participants passively viewed happy, angry and neutral faces. Using time‐resolved decoding of sensor‐level data, we show that responses to angry faces can be discriminated from happy and neutral faces as early as 90 ms after stimulus onset and only 10 ms later than faces can be discriminated from scrambled stimuli, even in the absence of differences in evoked responses. Time‐resolved relevance patterns in source space track expression‐related information from the visual cortex (100 ms) to higher‐level temporal and frontal areas (200–500 ms). Together, our results point to a system optimised for rapid processing of emotional faces and preferentially tuned to threat, consistent with the important evolutionary role that such a system must have played in the development of human social interactions.     

The selectivity of the occipitotemporal M170 for faces

Evidence from fMRI, ERPs and intracranial recordings suggests the existence of face-specific mechanisms in the primate occipitotemporal cortex. The present study used a 64-channel MEG system to monitor neural activity while normal subjects viewed a sequence of grayscale photographs of a variety of unfamiliar faces and non-face stimuli. In 14 of 15 subjects, face stimuli evoked a larger response than non-face stimuli at a latency of 160 ms after stimulus onset at bilateral occipitotemporal sensors. Inverted face stimuli elicited responses that were no different in amplitude but 13 ms later in latency than upright faces. The profile of this M170 response across stimulus conditions is largely consistent with prior results using scalp and subdural ERPs.     

Repetition suppression of face‐selective evoked and induced EEG recorded from human cortex

In functional MRI studies, repetition suppression refers to the reduction of hemodynamic activation to repeated stimulus presentation. For example, the repeated presentation of a face reduces the hemodynamic response evoked by faces in the fusiform gyrus. The neural events that underlie repetition suppression are not well understood. Indeed, in contrast to the hemodynamic response, the face‐specific N200 recorded from subdural electrodes on the ventral occipitotemporal cortex, primarily along the fusiform gyrus, has been reported to be insensitive to face‐identity repetition. We have previously described a face‐specific broadband gamma (30–100 Hz) response at ventral face‐specific N200 sites that is functionally dissociable from the N200. In this study, we investigate whether gamma and other components of the electroencephalogram spectrum are affected by face‐identity repetition independently of the N200. Participants viewed sequentially presented identical faces. At sites on and around the fusiform gyrus, we found that face repetition modulated alpha (8–12 Hz), low‐gamma (30–60 Hz), and high‐gamma (60–100 Hz) synchrony, but not the N200. These findings provide evidence of a spatially co‐localized progression of face processing. Whereas the N200 reflects an initial obligatory response that is less sensitive to face‐identity repetition, the subsequent spectral fluctuations reflect more elaborative face processing and are thus sensitive to face novelty. It is notable that the observed modulations were different for different frequency bands. We observed repetition suppression of broadband gamma, but repetition enhancement of alpha synchrony. This difference is discussed with regard to an existing model of repetition suppression and behavioral repetition priming. Hum Brain Mapp 35:4155–4162, 2014. © 2014 Wiley Periodicals, Inc .     

Identifying spatially overlapping local cortical networks with MEG

Recent modelling studies (Hadjipapas et al. [2009]: Neuroimage 44:1290‐1303) have shown that it may be possible to distinguish between different neuronal populations on the basis of their macroscopically measured (EEG/MEG) mean field. We set out to test whether the different orientation columns contributing to a signal at a specific cortical location could be identified based on the measured MEG signal. We used 1.5deg square, static, obliquely oriented grating stimuli to generate sustained gamma oscillations in a focal region of primary visual cortex. We then used multivariate classifier methods to predict the orientation (left or right oblique) of the stimuli based purely on the time‐series data from this one location. Both the single trial evoked response (0–300 ms) and induced post‐transient power spectra (300–2,300 ms, 20–70 Hz band) due to the different stimuli were classifiable significantly above chance in 11/12 and 10/12 datasets respectively. Interestingly, stimulus‐specific information is preserved in the sustained part of the gamma oscillation, long after perception has occurred and all neuronal transients have decayed. Importantly, the classification of this induced oscillation was still possible even when the power spectra were rank‐transformed showing that the different underlying networks give rise to different characteristic temporal signatures. Hum Brain Mapp, 2010. © 2009 Wiley‐Liss, Inc.     

Altered automatic face processing in individuals with high-functioning autism spectrum disorders: Evidence from visual evoked potentials

Individuals with autism spectrum disorders (ASDs) have different automatic responses to faces than typically developing (TD) individuals. We recorded visual evoked potentials (VEPs) in 10 individuals with high-functioning ASD (HFASD) and 10 TD individuals. Visual stimuli consisted of upright and inverted faces (fearful and neutral) and objects presented subliminally in a backward-masking paradigm. In all participants, the occipital N1 (about 100 ms) and P1 (about 120 ms) peaks were major components of the evoked response. We calculated “subliminal face effect (SFE)” scores by subtracting the N1/P1 amplitudes and latencies of the object stimuli from those of the face stimuli. In the TD group, the SFE score for the N1 amplitude was significantly higher for upright fearful faces but not neutral faces, and this score was insignificant when the stimuli were inverted. In contrast, the N1 amplitude of the HFASD subjects did not show this SFE in the upright orientation. There were no significant group differences in SFE scores for P1 amplitude, latency, or N1 latency. Our findings suggest that individuals with HFASD have altered automatic visual processing for emotional faces within the lower level of the visual cortex. This impairment could be a neural component of the disrupted social cognition observed in individuals with HFASD.     

High freuquency oscillatory activity in the human brain

Synchronized neural activity in animal visual cortex in the frequency range above 20 Hz, the gamma band, has been proposed as a signature of temporal feature binding. More and more research in humans by means of noninvasive electrophysiological recordings was stimulated by these studies. Here, research on evoked and induced gamma band activity in human EEG and MEG mainly in the auditory and visual modality is reviewed and their role in perceptual processes, feature integration and language processing is discussed. In addition, research on the attentional modulation of gamma band activity is reviewed. In contrast to evoked gamma band activity, which occurs right after stimulus onset, induced gamma band activity can be recorded with a latency of 200 to 400 ms and a frequency range of 30 to 95 Hz. Cumulative consistent experimental evidence allows us to conclude that gamma band activity in the human cortex is related to neuronal information processing and cognitive functions, e.g. memory processes. The findings are discussed in the light of different functional theories of induced gamma band activity.     

Human face perception traced by magneto- and electro-encephalography.

The temporal and spatial processing of face perception in normal subjects was traced by magnetoencephalography (MEG) and electroencephalography (EEG). We used 5 different visual stimuli: (1) face with opened eyes, (2) face with closed eyes, (3) eyes, (4) scrambled face, and (5) hand, and they were shown in random order. Subjects were asked to count the number of hand stimuli. To analyze the complicated brain responses to visual stimuli, we used brain electric source analysis (BESA) as the spatio-temporal multiple source model. In MEG recording, the 1M and 2M components were identified in all subjects. The 1M component was recorded to all kinds of stimuli. The 2M component was clearly identified only to face stimulation in all subjects, but to eyes stimulation in only 3 subjects with a small amplitude. The 2M component was not identified to scrambled face nor hand stimulation. The 2M component was recorded from the right hemisphere in all subjects, but in only 5 of 10 subjects from the left hemisphere. The mean peak latencies of the 1M and 2M components were approximately 132 and 179 ms, respectively. The interpeak latency between 1M and 2M was approximately 47 ms on average but the interindividual difference was large. There was no significant difference of the 2M latency between face with opened eyes and face with closed eyes. The 1M component was generated in the primary visual cortex in the bilateral hemispheres, and the 2M component was generated in the inferior temporal cortex, around the fusiform gyrus. In the EEG recording, face-specific components, positive at the vertex, P200 (Cz), and the negative at the temporal areas, N190 (T5') and N190 (T6'), were clearly recorded. The EEG results were fundamentally compatible with the MEG results. The amplitude of the component recorded from the right hemisphere was significantly larger than that from the left hemisphere. These findings suggest that the fusiform gyrus is considered to play an important role in face perception in humans, and that the right hemisphere is more dominant. Face perception takes place approximately 47 ms after the primary response to visual stimulation in the primary visual cortex, but the period of information transfer to the fusiform gyrus is variable among subjects. Detailed temporal and spatial analyses of the processing of face perception can be achieved with MEG.     

Distinct contrast response functions in striate and extra-striate regions of visual cortex revealed with magnetoencephalography (MEG).

OBJECTIVE: To spatially and temporally characterise the cortical contrast response function to pattern onset stimuli in humans. METHODS: Magnetoencephalography (MEG) was used to investigate the human cortical contrast response function to pattern onset stimuli with high temporal and spatial resolution. A beamformer source reconstruction approach was used to spatially localise and identify the time courses of activity at various visual cortical loci. RESULTS: Consistent with the findings of previous studies, MEG beamformer analysis revealed two simultaneous generators of the pattern onset evoked response. These generators arose from anatomically discrete locations in striate and extra-striate visual cortex. Furthermore, these loci demonstrated notably distinct contrast response functions, with striate cortex increasing approximately linearly with contrast, whilst extra-striate visual cortex followed a saturating function. CONCLUSIONS: The generators that underlie the pattern onset visual evoked response arise from two distinct regions in striate and extra-striate visual cortex. SIGNIFICANCE: The spatially, temporally and functionally distinct mechanisms of contrast processing within the visual cortex may account for the disparate results observed across earlier studies and assist in elucidating causal mechanisms of aberrant contrast processing in neurological disorders.     

The effects of cross‐orientation masking on the visual gamma response in humans

Electrophysiological recordings in primates indicate that visual gamma contains distinct broad‐ and narrowband components that reflect different neuronal processes. Evidence suggests that cross‐orientation masking of luminance‐defined gratings should differentially modulate these two components. To test this we measured the effect of cross‐orientation masking on the gamma response in 12 human participants using magentoencephalography (MEG). Although both the amplitude and the frequency of gamma were modulated by the presence of a cross‐orientation mask, we failed to find evidence for distinguishable components: both broadband gamma at stimulus onset and sustained narrowband gamma were similarly modulated by mask contrast. However, we could not confirm the presence of masking effects due to mask contrast being confounded with the contrast of the stimulus as a whole. We therefore tested a further 12 participants in a second experiment in which the stimuli were: a plaid stimulus, the two component gratings which formed the plaid and the same two gratings but with Michelson contrast matched to the plaid. We found that gamma amplitude was reduced and gamma frequency increased to the plaid stimulus when compared with the contrast‐matched gratings or with the sum of the two component gratings, indicating that visual gamma was indeed modulated by cross‐orientation masking. Surprisingly, masking did not affect the pattern‐onset evoked response, challenging previous hypotheses that cross‐orientation suppression – the phenomenon by which the response to an orientated grating is suppressed by a cross‐orientation mask – is driven by feedforward inputs to V1.     

Social perception in the infant brain: gamma oscillatory activity in response to eye gaze

Gamma band oscillatory brain activity was measured to examinethe neural basis of 4-month-old infants’ perception ofeye gaze direction. Infants were presented with photographicimages of upright and inverted female faces directing theirgaze towards them or to the side. Direct gaze compared to avertedgaze in upright faces elicited increased early evoked gammaactivity at occipital channels indicating enhanced neural processingduring the earliest steps of face encoding. Direct gaze alsoelicited a later induced gamma burst over right prefrontal channels,suggesting that eye contact detection might recruit very similarcortical regions as in adults. An induced gamma burst in responseto averted gaze was observed over right posterior regions, whichmight reflect neural processes associated with shifting spatialattention. Inverted faces did not produce such effects, confirmingthat the gamma band oscillations observed in response to gazedirection are specific to upright faces. These data demonstratethe use of gamma band oscillations in examining the developmentof social perception and suggest an early specialization ofbrain regions known to process eye gaze.