The fusiform response to faces: explicit versus implicit processing of emotion

Abstract

Regions of the fusiform gyrus (FG) respond preferentially to faces over other classes of visual stimuli. It remains unclear whether emotional face information modulates FG activity. In the present study, whole-head magnetoencephalography (MEG) was obtained from fifteen healthy adults who viewed emotionally expressive faces and made button responses based upon emotion (explicit condition) or age (implicit condition). Dipole source modeling produced source waveforms for left and right primary visual and left and right fusiform areas. Stronger left FG activity (M170) to fearful than happy or neutral faces was observed only in the explicit task, suggesting that directed attention to the emotional content of faces facilitates observation of M170 valence modulation. A strong association between M170 FG activity and reaction times in the explicit task provided additional evidence for a role of the fusiform gyrus in processing emotional information.

Figure 1

Examples of emotion face stimuli: upper and lower left = happy; upper right = neutral; lower right = fearful. Order of explicit (upper row) and implicit tasks (lower row) was counterbalanced across subjects. Stimuli were presented for 500 ms with a 2,300 ± 200 ms ISI.

Figure 2

Standard regional source model locations for visual and FG sources (Talairach coordinates). Average 3D distance from the mean values was 11.6 mm (s.d. = 4.5) and 9.8 mm (s.d. = 4.0) for visual and fusiform sources, respectively (left and right do not differ due to symmetry constraints).

Figure 3

Left and right hemisphere early visual source waveforms for the fearful, happy, and neutral conditions (explicit task). No early visual source strength main effects or interactions were observed.

Figure 4

Left and right hemisphere FG grand average source waveforms for the fearful, happy, and neutral conditions (explicit task), showing stronger early left fusiform source strength (∼ 150 ms) to fearful than happy or neutral faces (P < 0.05). Late FG activity (∼ 230 ms) can also be observed. It should be noted, however, that each individual's FG response was temporally shifted to the grand average M170 latency and, as such, activity before and after the M170 peak may be imprecise.

Figure 5

Pearson's r correlation between early fusiform source strength and RT, collapsed across hemisphere. The strong association (r = 0.70), accounting for nearly 50% of the RT variance, suggests involvement of the fusiform gyri in explicit emotion processing.