Our findings provide evidence that scene representations in PPA depend on temporal context. In the main experiment, the magnitude of RA was more than 4× greater in the Repeated Context condition (0.41%) than in the Novel Context condition (0.09%). Because previous studies used randomized trial histories (e.g., Turk-Browne et al., 2006
), which mirrored our Novel Context condition, they may have underestimated the true magnitude of RA. These studies intended to repeat stimuli, but assumed that the brain’s definition of a repetition matched the experimenter’s: that a repetition occurred when a stimulus had been seen before, irrespective of whether it had appeared in the same temporal context. We demonstrate that the definition of a scene repetition should be broadened to include temporal context in PPA.
There are two potential explanations of how temporal context affects RA. First, PPA may exhibit hysteresis, a general property of many mechanical, biological, and economic systems in which output can only be predicted from input with knowledge about initial conditions (i.e., the starting state of the system). Recent visual experience may alter the state of PPA by inducing persistent activity, which may in turn provide scaffolding for the representation of a novel scene. When the scene is re-encountered, it may not fully benefit from this prior experience unless PPA has been returned to the same state by repeating the temporal context.
Second, temporal context may affect RA as a result of prediction
. TCM provides a potential mechanism for such predictions, whereby the current context—a recency-weighted running average of experience—cues the retrieval of information that was previously bound to that context. In our case, the context includes the preceding two items, which may cue the retrieval of the third item. TCM was developed based on word list recall and other episodic memory tasks, and linked to the hippocampus and medial temporal lobe more broadly (e.g., Kumaran and Maguire, 2006
; Jenkins and Ranganath, 2010
; Manning et al., 2011
; Morgan et al., 2011
; Tubridy and Davachi, 2011
). Our exploratory analyses of the hippocampus are consistent with the possibility that these mechanisms operate incidentally and may be responsible for context-dependent RA in PPA. Specifically, the hippocampus may spontaneously retrieve items associated with the current context and reinstate them in PPA (Turk-Browne et al., 2010
), such that greater RA occurs when a predicted scene appears.
Neural models of RA (see Grill-Spector et al., 2006
) often focus on local processes and interactions (i.e., fatigue and sharpening models). In contrast, the prediction account fits best with a facilitation model in which hippocampal or other feedback potentiates the representation of the predicted item, reducing processing latency/duration (or prediction error; Friston, 2005
). The fact that expectations about stimulus repetition enhance RA has been interpreted similarly (Summerfield et al., 2008
). Our findings represent a novel discovery because the general probability of item repetition was held constant throughout our study, with predictability depending only on the identities of the preceding context items and prior learning of specific item-item associations.
As an implicit measure, RA may provide a new way to answer fundamental questions about context. For example: How many preceding items need to be repeated to elicit maximal RA? Do they need to be repeated in the same order? How is the length of the context window affected by stimulus complexity? Are there stable individual differences in context window length and do they predict memory abilities? Answers to such questions have important implications for theoretical models of memory such as TCM, where a definition of temporal context has proven elusive.
The current findings only license conclusions about scenes and PPA. However, they are consistent with three broader interpretations: First, temporal context may be an important property of how all objects are represented in their preferred category-selective areas. Second, effects of temporal context may be limited to PPA and to scenes, possibly reflecting a greater importance of temporal context for that category. Third, effects may be limited to PPA but occur there for objects from any category (cf. debate about semantic context in PHC; Bar et al., 2008
; but see Epstein and Ward, 2010
). By establishing this novel phenomenon, we hope to stimulate future research to adjudicate between these possibilities. For instance, each account makes a different prediction about whether temporal context should influence RA for other objects (e.g., faces): in their preferred area (e.g., fusiform face area), at all, or in PPA, respectively.
By integrating past and present, PPA and PHC more generally may serve as a bridge between perception and memory. Given the importance of temporal context in episodic memory (Howard and Kahana, 2002
; Sederberg et al., 2008
), our findings suggest a parsimonious explanation for why this region is frequently implicated in both domains (e.g., Brewer et al., 1998
; Wagner et al., 1998
; Turk-Browne et al., 2006
). Ultimately, the context-dependence of scene representations in PHC may help us encode and navigate complex environments. Indeed, PHC has been implicated in spatial navigation beyond the processing of scenes (e.g., Aguirre et al., 1996
; Janzen and van Turennout, 2004
; Zhang and Ekstrom, 2012
). Temporal context may help PHC to encode the structure of the environment in the service of navigation, both by differentiating similar looking scenes that are located in different places and by stitching together different looking scenes that appear nearby in space.