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 responds to contextual novelty. Prior neuroimaging findings suggested that the amygdala responds to novel human faces (Schwartz et al., 2003
; Wright et al., 2003
), but the current results suggest that such responses are not specific to faces and extend to other types of visual stimuli. Second, and most important, the amygdala appears especially sensitive to unusual stimuli, resulting in preferential processing of uncommon stimuli beyond the increased awareness afforded to contextually novel stimuli. The preferential processing interpretation is consistent with recent reports that the amygdala is engaged by unknown or ambiguous stimuli, such as uncertain outcomes (Hsu et al., 2005
) and supports the view that the amygdala is involved in allocating resources to determine the attributes and potential impact of unknown stimuli (Whalen, 1998
Unlike the amygdala, the hippocampus did not show an increased response to the novel uncommon stimuli, but showed a similar response to both contextual and categorical novelty. The hippocampal response to contextual novelty is consistent with prior studies demonstrating a critical role for the hippocampus in detecting novel events (Knight and Nakada, 1998
) and in the contextual probability of an event occurring over time (Harrison et al., 2006
; Strange et al., 2005
). Our findings add to the literature by demonstrating that the hippocampal response to novel stimuli generalizes to unusual novel stimuli. However, unlike studies reporting a unique role for the anterior hippocampus in detecting contextually novel objects or events (Herry et al., 2007
; Pihlajamaki et al., 2004
; Strange et al., 1999
), we found activation in both the anterior and posterior hippocampus.
In the whole brain analyses, the strongest finding was the involvement of the primary and secondary visual areas in novelty detection for both common and unusual stimuli. This finding is not surprising given the amygdala’s efferent connections to the visual system (Amaral et al., 2003
). The enhanced activation of visual regions by novel stimuli parallels effects of emotional images (Lang et al., 1998
). To the extent that these visual cortical responses are directed by the amygdala, the present results suggest that the amygdala’s ability to direct attentional resources extends to novel images. However, we can not rule out the possibility that these findings are driven by other regions or reflect a primary sensory process in visual cortex. Effective connectivity analysis (Friston, 1994
) might further our understanding of the functional relationship between the amygdala and visual cortex.
We selected a block design for this initial study to provide both increased detection power (Liu et al., 2001
) using a paradigm previously used to demonstrate amygdala response to novel faces (Schwartz et al., 2003
). An assumption of the block design is that all stimuli within a block are similar. However, stimuli can differ along multiple dimensions—such as novelty, valence, arousal, salience, and impact—which may each contribute to the brain’s response to these stimuli. For example, in this study the novel uncommon images were also rated as slightly more arousing than the novel common images. Several studies indicate that arousing stimuli induce amygdala activation (Kensinger and Schacter, 2006
; Lewis et al., 2007
), although the extent to which these activations relate to arousal versus valence, salience or impact, remains a matter of debate in the literature (Anders et al., 2008
; Ewbank et al., 2009
; Posner et al., 2009
). An event-related design can control for these image-specific differences by including additional regressors in the model, although often at the cost of reduced detection power. This study used a block design to provide the initial evidence for the amygdala’s response unique response to categorical novelty. Future studies could use an event-related design to further explore the effect of other stimulus features (e.g., salience, impact) on the amygdala’s response to novelty.
The results from this study may have implications for research in temperament, personality and psychiatric illness. Individual differences in response to novelty are a core part of temperament and personality , and extreme responses, such as neophobia and sensation seeking, are characteristic of psychiatric illnesses including social anxiety, autism, schizophrenia and substance abuse. Examination of individual differences in the brain’s response to nonsocial novelty may provide new insights into both normal variation in personality and psychiatric illness.