Electrophysiological Studies of Face Perception in Humans

Abstract

Event-related potentials (ERPs) associated with face perception were recorded with scalp electrodes from normal volunteers. Subjects performed a visual target detection task in which they mentally counted the number of occurrences of pictorial stimuli from a designated category such us butterflies. In separate experiments, target stimuli were embedded within a series of other stimuli including unfamiliar human faces and isolated face components, inverted faces, distorted faces, animal faces, and other nonface stimuli. Unman faces evoked a negative potential at 172 msec (N170), which was absent from the ERPs elicited by other animate and inanimate nonface stimuli. N170 was largest over the posterior temporal scalp and was larger over the right than the left hemisphere. N170 was delayed when faces were presented upside-down, but its amplitude did not change. When presented in isolation, eyes elicited an N170 that was significantly larger than that elicited by whole faces, while noses and lips elicited small negative ERPs about 50 msec later than N170. Distorted human faces, in which the locations of inner face components were altered, elicited an N170 similar in amplitude to that elicited by normal faces. However, faces of animals, human hands, cars, and items of furniture did not evoke N170. N170 may reflect the operation of a neural mechanism tuned to detect (as opposed to identify) human faces, similar to the "structural encoder" suggested by Bruce and Young (1986). A similar function has been proposed for the face-selective N200 ERP recorded from the middle fusiform and posterior inferior temporal gyri using subdural electrodes in humans (Allison, McCarthy, Nobre, Puce, & Belger, 1994c). However, the differential sensitivity of N170 to eyes in isolation suggests that N170 may reflect the activation of an eye-sensitive region of cortex. The voltage distribution of N170 over the scalp is consistent with a neural generator located in the occipitotemporal sulcus lateral to the fusiform/inferior temporal region that generates N200.

Figure 1

(A) ERPs elicited by faces and scrambled faces at 14 scalp locations. Note Nl70 at Locations T₅ and T₆. (B) ERPs elicited al T₅ and T₆, by the four nontarget stimulus categories. (C) P300 (largest at P_z) elicited by target butterflies. In this and the following figures, waveforms are grand averages across all subjects of each experiment.

Figure 2

ERPs elicited by human faces, animal faces, human hands, and furniture at T₅ and T₆.

Figure 3

Voltage distribution of ERPs clicited by upright human faces at 28 scalp locations at 88 (A), 128 (B), 172 (C), and 230 (D) msec from stimulus onset. Blue-purple hues represent negative voltages, yellow-red huts represent positive voltages.

Figure 4

ERPs elicited by upright faces and inverted faces at T₅ and T₆.

Figure 5

ERPs elicited by whole faces, isolated eyes, lips, and noses at T₅ and T₆.

Figure 6

Voltage distribution of ERPs elicited by faces and face components, based on 28 scalp locations and calculated at the peak of the negative potentials: (A) faces (at 172 msec). (B) eyes (at 172 msec), (C) lips (at 212 msec), (D) noses (at 232 msec).

Figure 7

ERPs elicited by distorted faces, eyes, lips, and noses at T₅ and T₆.

Figure 8

Schematic illustration of a working hypothesis of regions of extrastriate cortex involved in face perception. A face-sensitive region, located mainly in the fusiform gyrus and maximally responsive to human faces, generates an N200 potential as recorded from the cortical surface (Allison et al., l994a,b,c). The dipole generator is approximately vertical. An eye-sensitive region, located mainly in the medial wall of the occipitotemporal sulcus and maximally responsive to human eyes (Fig. 5), generates an N170 potential as recorded from the temporal scalp. The dipole generator is oblique and points approximately to the middle temporal gyrus, where scalp electrodes T₅ and T₆ are typically located (Homan et al., 1988). In the anterior-posterior dimension the eye-sensitive region is hypothesized to be located in the mid-fusiform region anterior to the region of inferior temporal gyrus that responds to faces. Drawing adapted from Figure 198 of Damasio (1995). The right hemisphere is illustrated, but both hemispheres are activated by faces and eyes. Abbreviations: CS, collateral sulcus; FG, fusiform gyrus; ITG, inferior temporal gyrus; MTG middle temporal gyrus; OTS, occipitotemporal sulcus.

Figure 9

Examples of stimuli used in Experiment 1.

Figure 10

Examples of stimuli used in Experiment 2.

Figure 11

Examples of stimuli used in Experiment 4.

Figure 12

Examples of stimuli used in Experiment 5. The normal version of the distorted face on the left is shown in Figure 11, upper left.