The effect of scene context on episodic object recognition: parahippocampal cortex mediates memory encoding and retrieval success

Abstract

Previous research has investigated intentional retrieval of contextual information and contextual influences on object identification and word recognition, yet few studies have investigated context effects in episodic memory for objects. To address this issue, unique objects embedded in a visually rich scene or on a white background were presented to participants. At test, objects were presented either in the original scene or on a white background. A series of behavioral studies with young adults demonstrated a context shift decrement (CSD)-decreased recognition performance when context is changed between encoding and retrieval. The CSD was not attenuated by encoding or retrieval manipulations, suggesting that binding of object and context may be automatic. A final experiment explored the neural correlates of the CSD, using functional Magnetic Resonance Imaging. Parahippocampal cortex (PHC) activation (right greater than left) during incidental encoding was associated with subsequent memory of objects in the context shift condition. Greater activity in right PHC was also observed during successful recognition of objects previously presented in a scene. Finally, a subset of regions activated during scene encoding, such as bilateral PHC, was reactivated when the object was presented on a white background at retrieval. Although participants were not required to intentionally retrieve contextual information, the results suggest that PHC may reinstate visual context to mediate successful episodic memory retrieval. The CSD is attributed to automatic and obligatory binding of object and context. The results suggest that PHC is important not only for processing of scene information, but also plays a role in successful episodic memory encoding and retrieval. These findings are consistent with the view that spatial information is stored in the hippocampal complex, one of the central tenets of Multiple Trace Theory.

Figure 1

Examples of study and test probe by condition. The test phase also included schema-consistent lure objects and lure scenes.

Figure 2

Average d-prime scores by experiment and condition (* indicates a significant difference between conditions within the experiment). Experiment 4 represents a reversal of the SCENE.OBJECT condition; that is, OBJECT.SCENE.

Figure 3

Context Shift Decrement (percent decrease in hit rate when context changed between study and test) by Experiment. Error bars represent the standard error of the mean.

Figure 4

The mean response time (std. err. mean) for correct and incorrect trials for each condition. There were no differences in response times across conditions for incorrect trials. For correct trials, response time for OOC

Figure 5

A. Activation observed when contrasting encoding of scenes (object in scene) versus objects [image coordinates: MNI: 30 −48 −8; Tal: 29 −47 4]. Massive bilateral activation was observed in posterior brain regions including the following regions: PHC, fusiform and lingual gyri, inferior, middle and superior occipital gyri, cuneus, precuneus, and inferior portions of the superior parietal lobule. B. Subsequent memory effects in PHC, right [MNI: 28 −42 −6; Tal: 28 −41 −3] greater than left [MNI: −32 −51 −3; Tal: −32 −50 0]. Increased PHC activation during encoding of SCENE.OBJECT trials was associated with subsequent memory for the object when it was later presented on a white background. C. Retrieval success activity in SCENE.OBJECT condition. Preferential activation of right PHC [MNI: 30 −41 −9; Tal: 30 −41 −5] was observed in SCENE.OBJECT hits > SCENE.OBJECT misses. D. Bilateral PHC activation during recognition hits of SCENE.OBJECT relative to OBJECT.OBJECT [right PHC: MNI: 28 −36 −14; Tal:28 −35 −10; ;left PHC: MNI: −28 −40 −10; Tal:−28 −40 −7]. The only difference between the conditions was that SCENE.OBJECT trials had been encoded in a naturalistic scene, whereas OBJECT.OBJECT trials had been encoded on a white background.

Figure 6

Subsequent memory effect in right PHC. Activation plotted from the peak voxel within right PHC [MNI: 28 −44 −4; Tal: 28 −43 −1] during encoding for hits and misses of SCENE.OBJECT and OBJECT.OBJECT relative to CONTROL trials. Note that right PHC exhibited a subsequent memory effect for SCENE.OBJECT, but not OBJECT.OBJECT.