Oscillatory characteristics of face-evoked neuromagnetic responses

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Abstract

To study the oscillatory activities during face processing, we recorded magnetoencephalographic responses in 8 healthy subjects to upright and inverted human faces, and obtained the time-frequency representation by using wavelet transform. Delta to beta activities were clearly increased at 140–210 ms after stimulus onset in the bilateral occipitotemporal (OT) areas (t7 > 5.5; p < 0.001), with larger power for theta, alpha and beta over the right side. Notably, more increase alpha activity for inverted than upright face condition was observed in the right OT area. Our results suggest that 4–25 Hz oscillations are involved in face information processing, and the more activation over the right OT implies the right hemisphere advantage for face perception. Moreover, the alpha activity may reflect the differential cortical demands for processing inverted and upright face images.

Introduction

Event-related potential (ERP) studies (Allison et al., 1994, Bentin et al., 1996, Eimer, 2000, George et al., 1996, Goffaux et al., 2003, Itier and Taylor, 2002, McCarthy et al., 1999, Rossion et al., 2000, Sagiv and Bentin, 2001) show the face-evoked negative responses peaking around 170 ms (N170). The neuromagnetic ∼ 170 ms component (M170) has been further localized in the occipitotemporal (OT) cortex in some magnetoencephalography (MEG) studies with stronger activation in the right hemisphere (Halgren et al., 2000, Hsiao et al., 2005, Sams et al., 1997, Watanabe et al., 2003). Notably, image inversion impairs the recognition of faces more than other objects (Yin, 1969, Rhodes et al., 1993). In the right OT region, N170 or M170 responses show longer latencies and larger amplitudes for inverted than upright faces (Eimer, 2000, Goffaux et al., 2003, Hsiao et al., 2005, Itier and Taylor, 2002, Linkenkaer-Hansen et al., 1998, Liu et al., 2000, McCarthy et al., 1999, Rossion et al., 2000, Watanabe et al., 2003).

Both EEG and MEG reflect the activity of an ensemble of sources generating rhythmic activities in several frequency ranges. In response to external stimulation, these sources are coherently coupled and activated with subsequent alterations in brain rhythms (Basar, 1998, Basar, 1999). Recent studies have shown the involvement of delta to gamma oscillations in the auditory and visual evoked responses (Basar, 1998, Basar, 1999, Basar et al., 2000, Basar et al., 2004, Klopp et al., 1999, Quian Quiroga et al., 2001, Yordanova et al., 2000, Yordanova et al., 2002). Of those, Klopp et al. (1999) have reported a synchronous 5–45 Hz power increase at 150–210 ms after stimulus onset in the fusiform gyrus, suggesting the contribution of cerebral oscillations to face processing. However, we do not know the hemispheric difference of these rhythmic activities and their involvement in the processing of inverted faces.

Wavelet transform gives a time-frequency representation of brain activities and provides a good temporal resolution for rhythmic activities in comparison with conventional Fourier transform (Basar et al., 1999, Demiralp et al., 1999, Quian Quiroga et al., 2001, Samar, 1999, Schiff et al., 1994, Tzelepi et al., 2000, Yordanova et al., 2000, Yordanova et al., 2002). It has been used to explore the rhythmic patterns of cortical responses to checkerboard patterns (Quian Quiroga and Schurmann, 1999, Quian Quiroga et al., 2001), sinusoidal gratings (Tzelepi et al., 2000), or rectangular light-stimuli (Yordanova et al., 2002). However, the oscillatory features during face perception in the OT areas remain unclear.

In this study, using MEG recordings and wavelet transform, we explored the oscillatory dynamics of cortical responses elicited by upright and inverted faces.

Section snippets

Subjects

We studied eight healthy, right-handed volunteers (4 men and 4 women; age range 24 to 28 years), with normal or corrected-to-normal vision. None had neurological or psychiatric deficits. Informed consent was obtained from each participant.

Stimuli

Our stimuli consisted of upright and inverted grayscale pictures of 23 Chinese faces with neutral expressions and an average 12 cd/m2 in brightness. With a personal computer (Acer Veriton) and an LCD projector (Electrohome Electronics, 38-DMD001-EXP, Canada),

ECD analysis of face-evoked neuromagnetic responses

Fig. 1 shows the typical source waveforms and localizations of neuromagnetic responses to upright faces in Subject 1. The right panel shows the waveforms and amplitudes of 3 ECDs as a function of time. The early response at 121 ms in the MO area is followed by later activations in the right OT and left OT at ∼ 180 ms. The left panel shows ECDs locations superimposed on the subject's own brain MR images. The early face-evoked response is localized in the occipital area, presumably around the

Time-domain versus frequency-domain representation of face-evoked responses

We obtained typical time-domain face-evoked responses in each subject, in line with earlier reports from scalp ERP (Allison et al., 1994, Bentin et al., 1996, Eimer, 2000, George et al., 1996, Goffaux et al., 2003, Itier and Taylor, 2002, McCarthy et al., 1999, Rossion et al., 2000, Sagiv and Bentin, 2001) and MEG recordings (Halgren et al., 2000, Hsiao et al., 2005, Linkenkaer-Hansen et al., 1998, Sams et al., 1997, Watanabe et al., 2003). In this paper, we further demonstrated a clear

Conclusions

Face perception is an essential function for humans. Our results show that human faces evoke 4–25 Hz oscillations at 140–210 ms in the occipitotemporal cortex. Notably, the alpha activity may be the main frequency component reflecting the difference of neuronal demands for perceiving inverted and upright faces, with possible contribution from the attention-related synchronization. Our present study opens a new window for further exploration of face processing mechanisms in the human brains.

Acknowledgements

We thank Mr. Chih-Che Chou and Mr. Chou-Ming Cheng for technical assistance in the acquisition of MR images. This study was supported by research grants from National Science Council (NSC-93-2213-E010-016, Y Chang; NSC-93-2314-B-075-086, NSC-92-2314-B-075-080-, YY Lin; NSC-92-2314-B-075-095, NSC-932314-B-0750-84, JC Hsieh), National Health and Research Institute (NHRI-EX93-9332SI, JC Hsieh), and Taipei Veterans General Hospital (93323, 94323, YY Lin; 923721, 92348, 933561, 93322, JC Hsieh),

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