A unique role for the human amygdala in novelty detection
Introduction
Humans must continually process vast amounts of incoming sensory information, requiring the brain to efficiently determine which stimuli require attention or memory encoding. Given limited resources, the ability to detect and direct attention to novel stimuli has substantial adaptive value. Novelty detection is supported by a coordinated network of brain regions in the medial temporal lobe, visual, parietal and prefrontal cortices, and the dopamine midbrain (Hughes, 2007, Kiehl et al., 2001, Ranganath and Rainer, 2003, Squire et al., 2004). Of these brain regions, the medial temporal lobe has received substantial attention. Converging support for medial temporal lobe involvement in novelty detection comes from single-cell recording (Fried et al., 1997, Rutishauser et al., 2006), lesion (Knight, 1996, Stark and Squire, 2003), and functional neuroimaging (Gonsalves et al., 2005, Kirwan et al., 2009) studies.
Within the medial temporal lobe, the hippocampus has long been recognized as an important brain structure for the detection of and subsequent memory for novel events (Knight, 1996, Kumaran and Maguire, 2009, Ranganath and Rainer, 2003). This function is usually interpreted within the context of the hippocampus's pivotal role in declarative memory, as the recognition of a new stimulus depends upon the ability to contrast it with stored memories (Hughes, 2007), and because new stimuli particularly warrant encoding.
Anterior to the hippocampus, the amygdala has also been identified as part of a neural novelty detection circuit (Kiehl et al., 2005). Recent studies indicate that the amygdala responds to novel stimuli, such as novel human faces (Schwartz et al., 2003, Wright et al., 2003) or novel sounds (Kiehl et al., 2005). The exact function of this response is uncertain, but it may be interpreted within the context of the amygdala's critical role in evaluating the emotional significance (Breiter et al., 1996, Whalen et al., 1998), arousal (Kensinger and Schacter, 2006, Lewis et al., 2007), or salience (Ewbank et al., 2009) of stimuli (for a review, see Zald, 2003). In animal studies, the amygdala response to novelty appears critical in mediating neophobic responses (Hughes, 2007), consistent with the amygdala's role in fear and avoidance behaviors (Davis and Whalen, 2001) .
While it is clear that novel stimuli engage both the amygdala and hippocampus, it is unclear whether novelty responses in the hippocampus and amygdala reflect a common underlying process since the type of novel stimulus used often differs across studies. For instance, in studies of memory, a novel stimulus is typically defined as a stimulus not previously presented in the study (e.g., Tulving et al., 1996). These stimuli (such as a picture of a house, landscape or person) are not conceptually novel, or unusual—indeed the person may have experienced the particular type of stimulus many times before. Rather, the stimuli are only novel to the current context. In contrast, in research on motivation and emotion, a novel stimulus is often categorically unique and represents an object or situation with which the person has no previous experience (Hamann et al., 2002), for example, a leafy sea dragon or rendering of a futuristic skyscraper. Detection of these two types of novelty may have different functional consequences: detection of novel common stimuli may increase awareness of the stimulus in the current context, and detection of novel uncommon stimuli may allocate processing resources to determine what the stimulus is and whether it will have a positive or negative impact on the individual.
Prior studies have experimentally manipulated type of novelty to examine functional differences within the hippocampus (Strange et al., 1999) and between the hippocampus and parahippocampal cortex (Duzel et al., 2003, Pihlajamaki et al., 2004). To our knowledge, no neuroimaging studies have contrasted contextual and categorical novelty nor compared the novelty responses of the amygdala and hippocampus.
To examine the role of the amygdala and hippocampus in detecting different types of novelty, we used functional magnetic resonance imaging (fMRI) to measure the blood oxygen level dependent (BOLD) response to three types of stimuli—familiar common, novel common, and novel uncommon—in 29 healthy adults. The novel common images represented contextual novelty because they had not been seen before in the context of this study and the novel uncommon stimuli represented categorical novelty because they were unusual and unlikely to have been seen before in real life. The results demonstrate that the amygdala and hippocampus have different response profiles to the two distinct types of novelty.
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Participants
Thirty-two healthy adults (19 females, 13 males) with an average age of 22 years (SD = 3.1) participated in the study. Participants were mainly right-handed (91%) and represented multiple ethnic groups: 71% Caucasian, 16% Asian, and 13% African-American. Data from three participants were later removed from analysis due to excessive motion during the scan (see fMRI data below) for an analytic sample size of 29 participants. The study was approved by the Vanderbilt Institutional Review Board.
Regions of interest: Amygdala and hippocampus
To examine the effect of contextual novelty on the amygdala and hippocampus, we compared BOLD responses between the familiar and novel images of common objects and scenes. In the amygdala, novel common images increased BOLD response by 50% in the left amygdala and 47% in the right amygdala (Fig. 1, Fig. 2). Consistent with the amygdala results, both left and right hippocampi showed an increased response (63% and 91%, respectively) to the novel common compared to the familiar images (Fig. 1,
Discussion
The present study illustrates the importance of distinguishing between different types of novelty. The amygdala and hippocampus demonstrated unique patterns of responses to two distinct types of novelty. Whereas the hippocampus showed a similar response to both contextual and categorical novelty, the amygdala was differentially sensitive to these two aspects of novelty. The results regarding the amygdala have two implications. First, the findings provide strong evidence that the amygdala
Acknowledgments
We thank Buddy Creech, Rebecca Ray, and Richard Shelton for their comments on this manuscript, and Jerome Kagan for helpful discussion. This work was supported in part by the National Institute of Mental Health (K01-MH083052 to J.U.B.; R01-MH074567 to D.H.Z.), the National Center for Research Resources (Vanderbilt CTSA grant 1-UL1-RR024975), and the Vanderbilt Institute of Imaging Science.
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