Early category-specific cortical activation revealed by visual stimulus inversion

Abstract

Visual categorization may already start within the first 100-ms after stimulus onset, in contrast with the long-held view that during this early stage all complex stimuli are processed equally and that category-specific cortical activation occurs only at later stages. The neural basis of this proposed early stage of high-level analysis is however poorly understood. To address this question we used magnetoencephalography and anatomically-constrained distributed source modeling to monitor brain activity with millisecond-resolution while subjects performed an orientation task on the upright and upside-down presented images of three different stimulus categories: faces, houses and bodies. Significant inversion effects were found for all three stimulus categories between 70-100-ms after picture onset with a highly category-specific cortical distribution. Differential responses between upright and inverted faces were found in well-established face-selective areas of the inferior occipital cortex and right fusiform gyrus. In addition, early category-specific inversion effects were found well beyond visual areas. Our results provide the first direct evidence that category-specific processing in high-level category-sensitive cortical areas already takes place within the first 100-ms of visual processing, significantly earlier than previously thought, and suggests the existence of fast category-specific neocortical routes in the human brain.

Figure 1. Examples of Stimuli and Experimental Trial.

A. Examples of the nine stimulus conditions. Photographs of Faces, Bodies and Houses were presented in three different ways: Upright, Inverted, and after phase-Scrambling. B. Example of an experimental trial. Stimuli were presented for 250-ms in random order, and after a delay of 500-ms subjects had to judge by button press whether the pictures were Upright, Inverted, or Scrambled.

Figure 2. Visually evoked magnetic fields to Upright and Inverted Stimuli.

Visually evoked magnetic fields to Upright (blue) and Inverted (red) Faces, Bodies, and Houses recorded at a typical posterior planar gradiometer (MEG2123) in a representative individual. The early response peaked around ∼100-ms after picture onset, and is clearly smaller for Upright Faces as compared to Inverted Faces. Note the different vertical scale for Bodies as compared to Faces and Houses. Displayed on the right are the corresponding topographic distributions of the evoked fields at 85-ms latency for the Upright and Inverted conditions and for the Upright-Inverted difference-wave, as seen from the back and the right side of the helmet.

Figure 3. Global measures of MEG activity.

A, B. The grand average (n = 9 subjects) of the Mean Global Field Power (MGFP) of the magnetometers (A) and gradiometers (B) showed a significant Inversion Effect for Faces only, i.e. around 170 ms. C. Source analysis (anatomically constrained MNE) revealed an early global Inversion Effect around 85-ms latency for all three stimulus categories with a larger mean overall ( = whole cortex) dipole strength for the Inverted stimuli than for the Upright stimuli. The time samples at which significant Inversion Effects occur (p<0.05; paired t-tests, n = 9, df = 8) are indicated by horizontal bars with color corresponding to category (Faces = yellow; Bodies = red; Houses = blue).

Figure 4. Source distribution of the M100 Stimulus Inversion Effect.

A. Anatomically constrained source analysis (average dSPM values across subjects; n = 9) for Upright (top trace) and Inverted Faces (bottom trace) from 70–100-ms after stimulus onset visualized on the inflated cortical surface (gyri appear in light grey, sulci in dark grey). For each time-instant, four different views are presented to depict the whole cortical surface, with left hemisphere on the left and right hemisphere on the right of each quadruplet. The two top images of each quadruplet show the lateral aspects of the brain and a little strip of the ventral aspect (lateral view, 11° tilted towards the bottom view); the two bottom images show the medial and ventral aspects of the brain (medial view, 45° tilted towards bottom view). Only values of dSPM>2.5 are visualized. A grey opaque mask was placed over the midbrain. B. Differential activation related to the Inversion Effects, i.e. the contrast between the Upright and Inverted condition of Faces, Bodies and Houses. Displayed are the largest positive or negative t-values (two-tailed paired t-tests; n = 9; df = 8) at each dipole location occurring within the 70–100-ms time-window. Significant t-values at the level of p<0.01 are thresholded with respect to baseline noise and visualized only if the dipole strength exceeds a signal-to-noise ratio of 2.5 (i.e. dSPM>2.5) in at least one of the single stimulus conditions. The red and yellow colors denote locations at which the dipole strength is stronger for Upright than for Inverted stimuli. Blue colors denote locations in which the dipole strength is stronger for the Inverted stimuli. Absolute t-values of 3.35 and larger (red/dark-blue) correspond to p<0.01, absolute t-values of 4.8 and larger (yellow/light blue) to p<0.001. Abbreviations: mFG = middle Fusiform Gyrus; IOG = Inferior Occipital Gyrus; LOC = Lateral Occipital Cortex; pIFG = posterior Inferior Frontal Gyrus; mOFC = medial OrbitoFrontal Cortex.

Figure 5. Category-specific cortical distribution of the M100 Inversion Effect.

A. Overview of the cortical distribution of the Inversion Effect for the M100 component for the three different stimulus categories. The three t-maps of figure 4 were combined into a single map. Dipole positions at which the Inverted stimuli induced significantly (p<0.01) larger currents than their canonical Upright presentation within the 70–100-ms time-window are color-coded according to stimulus category and their spatial overlap as displayed in panel C. B. Bar graph displaying the number of dipoles showing a significant Inversion Effect for Faces, Bodies and Houses. Within each stimulus category the color (color coding as in C) indicates the degree of category-specificity, i.e. the amount of spatial (non-)overlap with the other categories. The amount of spatial overlap between categories is small (see also panel C for the exact number of dipoles). C. Color coding of stimulus category and their spatial overlap as used in panels A and B, with the exact number of dipoles showing a significant Inversion Effect.

Figure 6. Time courses of current strength from selected regions.

Grand average (n = 9 subjects) time courses of estimated currents extracted from six regions that showed significant Inversion Effects indicated on the inflated brains in the top panel, i.e. the Calcarine Sulcus (1), IOG (2), LOC (3), mFG (4), pIFG/Insula (5), and the Precuneus/posterior Cingulate (6) for Upright and Inverted Faces (yellow), Bodies (red) and Houses (blue). The time instants at which significant differences occur between Upright and Inverted conditions are indicated at the level of p<0.01 (paired t-tests, n = 9, df = 8) by horizontal bars with color corresponding to category. Abbreviations: Calcarine S. = Calcarine Sulcus; IOG = Inferior Occipital Gyrus; LOC = Lateral Occipital Cortex; mFG = mid-Fusiform Gyrus; pIFG = posterior Inferior Frontal Gyrus; Precun = Precuneus; pCing = posterior Cingulate Gyrus.