Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex

Abstract

The ability to perceive and differentiate facial expressions is vital for social communication. Numerous functional MRI (fMRI) studies in humans have shown enhanced responses to faces with different emotional valence, in both the amygdala and the visual cortex. However, relatively few studies have examined how valence influences neural responses in monkeys, thereby limiting the ability to draw comparisons across species and thus understand the underlying neural mechanisms. Here we tested the effects of macaque facial expressions on neural activation within these two regions using fMRI in three awake, behaving monkeys. Monkeys maintained central fixation while blocks of different monkey facial expressions were presented. Four different facial expressions were tested: (i) neutral, (ii) aggressive (open-mouthed threat), (iii) fearful (fear grin), and (iv) submissive (lip smack). Our results confirmed that both the amygdala and the inferior temporal cortex in monkeys are modulated by facial expressions. As in human fMRI, fearful expressions evoked the greatest response in monkeys-even though fearful expressions are physically dissimilar in humans and macaques. Furthermore, we found that valence effects were not uniformly distributed over the inferior temporal cortex. Surprisingly, these valence maps were independent of two related functional maps: (i) the map of "face-selective" regions (faces versus non-face objects) and (ii) the map of "face-responsive" regions (faces versus scrambled images). Thus, the neural mechanisms underlying face perception and valence perception appear to be distinct.

Fig. 1.

Stimulus conditions and fMRI coverage. (A) Examples of the different facial expressions tested. (B) Within each block, each image was presented for 700 ms followed by a mask for 300 ms. Four facial expressions were presented from each of eight different monkeys. (C) Sagittal view of a monkey anatomical scan illustrating the typical location of the slices (in red).

Fig. 2.

Face-responsive versus face-selective regions. Lateral and ventral inflated views show face-responsive regions and face-selective regions in both hemispheres from monkeys E and R. Face-responsive regions were defined as those showing significantly greater activation for neutral faces relative to scrambled faces (shown in yellow/red), whereas face-selective regions were defined as those showing greater activation for neutral faces relative to non-face objects (outlined in black). The frontal lobe was imaged only in monkey E. as, arcuate sulcus; ios, inferior occipital sulcus; ls, lateral sulcus; los, lateral orbital sulcus; lus, lunate sulcus; pmts, posterior middle temporal sulcus; sts, superior temporal sulcus.

Fig. 3.

Amplitude of valence effect within face-responsive and face-selective regions of IT cortex. The percent signal change is shown for the different facial expressions within two face-selective and two face-responsive ROIs in the left hemispheres of monkeys E and R. The lateral view illustrates the approximate location of the selected ROIs. For both the face-selective and face-responsive regions, the histograms on the left indicate activations in the anterior ROIs, whereas the histograms on the right indicate activations in the posterior ROIs. All ROIs were equated in size. Asterisks indicate significant differences relative to the neutral condition for each ROI (P < 0.05; errors bars indicate the SEM). N, neutral; T, threat; F, fear grin; L, lip smack.

Fig. 4.

Map of valence effects throughout IT cortex. (A) Lateral inflated views of the left and right hemispheres of monkeys E and R, showing the magnitude of the valence effect within the face-selective regions (outlined in black) and the more extensive face-responsive regions. The significance of the valence effect reflects the difference in the fMRI signal of any facial expression relative to the neutral expression (i.e., threat versus neutral or fear grin versus neutral or lip smack versus neutral). (B) Correlation between valence effect and either face responsivity (Left) or face selectivity (Right) across monkeys E and R.

Fig. 5.

Valence effect within the amygdala. (A) Coronal section illustrating face-responsive regions within the amygdala for all three animals. (B) Magnified view of the amygdala activation and schematic representation of the amygdala nuclei. The face-responsive regions were found bilaterally in the basal and lateral nuclei of the amygdala in all animals. (C) Percent signal change within face-responsive regions in the amygdala in one hemisphere of one monkey, evoked by the perception of facial expressions. Asterisks indicate that fear grin elicited a greater response than the neutral expression. AB, accessory basal nucleus; B, basal nucleus; CE, central nucleus; L, lateral nucleus; M, medial nucleus; N, neutral; T, threat; F, fear grin; L, lip smack.