Elsevier

NeuroImage

Volume 55, Issue 4, 15 April 2011, Pages 1889-1898
NeuroImage

The human amygdala plays a stimulus specific role in the detection of novelty

https://doi.org/10.1016/j.neuroimage.2011.01.034Get rights and content

Abstract

The primary focus of research on the amygdala has been on the detection of and response to emotion but the amygdala also sometimes responds to new or unexpected stimuli without specific emotional content. Very little is currently known about why the amygdala responds to some new stimuli but not to others. Here we investigated the conditions that are necessary and sufficient for the expression of novelty specific amygdala responses by presenting novel and repeated images to human participants and varying the content of these images while measuring blood-oxygenation level dependent (BOLD) responses. In Experiment 1 we presented novel and repeated emotional and neutral images. Both emotional and neutral images of humans evoked more amygdala activity when novel than when repeated. In Experiment 2 we presented novel and repeated images of humans and scenes. Images of humans but not scenes evoked more amygdala activity when novel than when repeated. Our results suggest that the amygdala plays a stimulus-specific role in the brain's novelty detection network. Surprisingly, emotion was not necessary for amygdalar novelty responses, but the presence of a human representation was important. Amygdala responses evoked by novel faces may reflect our need to use others' faces as clues for important events in the environment.

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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