The human amygdala plays a stimulus specific role in the detection of novelty
Research Highlights
► We investigated the conditions that are important for amygdalar novelty responses. ► Novel emotional and neutral images of humans evoke amygdala responses. ► Novel neutral scenes do not evoke amygdala responses. ► Our results suggest that amygdalar novelty responses are stimulus-specific.
Introduction
Activity in the brain's novelty detection network is thought to represent an early stage in memory encoding, focusing attention on unexpected stimuli or events (Tulving et al., 1996). The amygdala plays an important role in the formation of new memories for emotional events (Canli et al., 2000). Although often overlooked in novelty detection studies (Daselaar et al., 2006, Menon et al., 2000, Tulving et al., 1996, Yamaguchi et al., 2004), the amygdala sometimes responds to novel stimuli much like other regions (i.e. hippocampus, parahippocampal gyrus). For example, Schwartz and colleagues presented blocks of faces and found that the amygdala responded maximally when the faces in a given block were presented only once (Schwartz et al., 2003). In contrast, Yamaguchi and colleagues showed that the hippocampus but not the amygdala was activated by novel presentations of animals, buildings and landscapes, suggesting that novelty per se does not drive amygdala responses (Yamaguchi et al., 2004).
Although larger blood-oxygenation level dependent (BOLD) responses have been observed in the human amygdala for stimuli that are novel to the observer, we still lack a basic understanding of the conditions that are necessary and sufficient for such responses. We hypothesized that novelty-specific amygdala responses are not evoked by all stimuli, but are dependent on characteristics of the novel stimulus.
We used functional magnetic resonance imaging (fMRI) to determine which stimulus characteristics are most important for novelty-specific amygdala responses. We presented novel and repeated images and systematically varied the content of these images based on the previously established framework of amygdala functions. In Experiment 1 we sought to determine if emotional content played an important role in amygdalar novelty responding. In Experiment 2 we sought to determine if human representations were necessary for novelty-specific amygdala responses. Finally, we investigated the temporal properties of novelty-specific amygdalar responses by comparing the responses evoked by novel and repeated stimuli across trials.
Section snippets
Participants
Fifty-three neurologically healthy undergraduate students (Age: M = 20.78, SD = 2.90) at the University of Wisconsin-Milwaukee participated in this experiment and received $20 for participation, as well as extra credit in their psychology classes and a picture of their brain. Thirty-three were female. Three participants were excluded from the study because of computer/recording failures. Ten participants were excluded because of excessive head motion. Of the remaining participants, 20 individuals
Novelty-specific BOLD responses in the amygdala and hippocampus are not dependent on emotion
We began by investigating emotion as a potential mediating factor for two reasons. First, the amygdala is important for the perception of and response to emotional stimuli (Adolphs et al., 1994, Cheng et al., 2003, Williams et al., 2001). Second, amygdala activity at encoding correlates with subsequent memory for emotional scenes, suggesting that amygdala activity may help facilitate memory for emotional events (Canli et al., 2000). Amygdalar novelty responses may facilitate the encoding of
Discussion — the amygdala plays a stimulus specific role in the detection of novel stimuli
We show that the amygdala is sensitive to stimulus novelty, but only when certain types of stimuli are used. Surprisingly, these findings do not depend on the emotional content of the images. Novel emotional and neutral images of humans each evoke robust amygdala responses. Our findings are original because we show that neutral scenes do not evoke a novelty response in the amygdala. Remarkably, amygdala activity does not seem to gradually habituate with repeated stimulus presentations. Instead,
Acknowledgments
This study was supported by the National Institute of Mental Health (MH060668 and MH069558).
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