Upright face-preferential high-gamma responses in lower-order visual areas: Evidence from intracranial recordings in children

Abstract

Behavioral studies demonstrate that a face presented in the upright orientation attracts attention more rapidly than an inverted face. Saccades toward an upright face take place in 100-140 ms following presentation. The present study using electrocorticography determined whether upright face-preferential neural activation, as reflected by augmentation of high-gamma activity at 80-150 Hz, involved the lower-order visual cortex within the first 100 ms post-stimulus presentation. Sampled lower-order visual areas were verified by the induction of phosphenes upon electrical stimulation. These areas resided in the lateral-occipital, lingual, and cuneus gyri along the calcarine sulcus, roughly corresponding to V1 and V2. Measurement of high-gamma augmentation during central (circular) and peripheral (annular) checkerboard reversal pattern stimulation indicated that central-field stimuli were processed by the more polar surface whereas peripheral-field stimuli by the more anterior medial surface. Upright face stimuli, compared to inverted ones, elicited up to 23% larger augmentation of high-gamma activity in the lower-order visual regions at 40-90 ms. Upright face-preferential high-gamma augmentation was more highly correlated with high-gamma augmentation for central than peripheral stimuli. Our observations are consistent with the hypothesis that lower-order visual regions, especially those for the central field, are involved in visual cues for rapid detection of upright face stimuli.

Spatio-temporal dynamics of working memory maintenance and scanning of verbal information

“…Subdural platinum grid electrode (10 mm center-to-center distance; 4 mm diameter) placement was as described previously by our team (Matsuzaki et al, 2015; Nonoda et al, 2016). Extraoperative video–ECoG recordings were obtained for three to five days, using a 192-channel Nihon Kohden Neurofax 1100A Digital System (Nihon Kohden America Inc., Foothill Ranch, CA, USA) at a sampling frequency of 1,000 Hz as previously described.…”

“…Lateral and anterior–posterior X-rays were acquired following placement of intracranial electrodes; thereby, three metallic fiducial markers were placed at anatomically well-defined locations on the patient’s head for co-registration of the X-ray with the MRI. A 3D MRI brain surface image was created with electrodes delineated (Alkonyi et al, 2009; Matsuzaki et al, 2015; Muzik et al, 2007). Accuracy was confirmed by intraoperative digital photographs of in situ electrodes in each patient (Nonoda et al, 2016; Pieters et al, 2013; Wellmer et al, 2002).…”

“…The mean registration error was reported to be 1.56 mm in those ranging in age from 4 to 11 years old (Ghosh et al, 2010). Automatic parcellation of cortical gyri was performed at both individual and spatially normalized brain surfaces (Desikan et al, 2006; Matsuzaki et al, 2015), and all electrode sites were assigned anatomical labels (Fig. 2A).…”

Spatial–temporal patterns of electrocorticographic spectral changes during midazolam sedation

“…A three-dimensional MRI was created for each patient with the location of electrodes directly defined on the brain surface (Alkonyi et al, 2009; Matsuzaki et al, 2015). Using automatic parcellation of cortical gyri on FreeSurfer software (Desikan et al, 2006), subdural electrodes were assigned anatomical labels (Pieters et al, 2013; Matsuzaki et al, 2015; Supplementary Figure S2). …”

“…At each channel, we measured the percent change in amplitude at a given frequency band, in steps of 0.5 Hz and 100 milliseconds, relative to the mean amplitude in a control period for 20 seconds prior to the administration of midazolam (Nagasawa et al, 2012; Matsuzaki et al, 2015). We subsequently superimposed ECoG amplitude measures to each individual three-dimensional MRI (Brown et al, 2008; Nariai et al, 2011; Toyoda et al, 2014), yielding animation movies of amplitude changes at eight frequency bands (Figures 1 and 2; Video S1 and S2).…”