Integrated neural representations of odor intensity and affective valence in human amygdala

Abstract

Arousal and valence are proposed to represent fundamental dimensions of emotion. The neural substrates for processing these aspects of stimuli are studied widely, with recent studies of chemosensory processing suggesting the amygdala processes intensity (a surrogate for arousal) rather than valence. However, these investigations have assumed that a valence effect in the amygdala is linear such that testing valence extremes is sufficient to infer responses across valence space. In this study, we tested an alternative hypothesis, namely that valence responses in the amygdala are nonlinear. Using event-related functional magnetic resonance imaging, we measured amygdala responses to high- and low-concentration variants of pleasant, neutral, and unpleasant odors. Our results demonstrate that the amygdala exhibits an intensity-by-valence interaction in olfactory processing. In other words, the effect of intensity on amygdala activity is not the same at all levels of valence. Specifically, the amygdala responds differentially to high (vs low)-intensity odor for pleasant and unpleasant smells but not for neutral smells. This implies that the amygdala codes neither intensity nor valence per se, but a combination that we suggest reflects the overall emotional value of a stimulus.

Figure 1.

Rationale and experimental hypotheses. a, Previous experiments using pleasant and unpleasant stimuli (Anderson et al., 2003; Small et al., 2003) have shown a main effect of intensity in chemosensory processing, suggesting that the amygdala is preferentially tuned to intensity. However, because these studies did not use valence-neutral stimuli, it remains unclear how the amygdala would respond to the neutral mid-range of valence space (dashed box), which has important implications for interpretation of amygdala coding. In the current study, odors of pleasant, neutral, and unpleasant valence were each presented at high and low intensity, permitting a test of two competing hypotheses. b, Hypothesis I: main effect of intensity. Here, the amygdala responses are enhanced to high (vs low)-intensity odors, independent of valence, which would fit with previous findings suggesting the amygdala operates as an intensity detector across the entire valence spectrum. c, Hypothesis II: interaction of intensity and valence. Here, amygdala responses are enhanced only to high-intensity versions of pleasant and unpleasant, but not neutral, odor, implying a greater complexity to amygdala coding involving combined sensitivity to both intensity and valence. Thus, although the diagrams in b and c show equivalent response profiles at the extremes of valence, the inclusion of neutral odor allows the two hypotheses to be distinguished.

Figure 2.

Experimental design and behavioral data. The experiment corresponded to a three-by-two factorial design. The factors were odor type with three valence levels (pleasant, neutral, or unpleasant) and concentration with two levels (high or low). The plot shows the psychophysical odor space: valence on the abscissa, intensity on the ordinate. Ratings were collected using modified Labeled Magnitude Scales (see Materials and Methods). Both scales are truncated for display. Sl., Slightly; Mod., moderately; Str., strongly. Dark symbols, High-concentration odors; light symbols, low-concentration odors. Error bars show SEM; vertical bars represent error in intensity dimension; horizontal bars represent error in valence ratings.

Figure 3.

Differential effects of odor valence on intensity coding in the amygdala. Response time courses of amygdala activation for each level of odor concentration and odor type are shown. Data are taken from an unconstrained FIR model and highlight the selective effects of intensity on amygdala activity only at the extremes of odor valence.