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. 2007 Oct 15;38(1):194-202.
doi: 10.1016/j.neuroimage.2007.06.038. Epub 2007 Jul 24.

Anticipation of novelty recruits reward system and hippocampus while promoting recollection

Bianca C Wittmann  1 , Nico Bunzeck, Raymond J Dolan, Emrah Düzel
Affiliations

Anticipation of novelty recruits reward system and hippocampus while promoting recollection

Bianca C Wittmann et al. Neuroimage. .

Abstract

The dopaminergic midbrain, which comprises the substantia nigra and ventral tegmental area (SN/VTA), plays a central role in reward processing. This region is also activated by novel stimuli, raising the possibility that novelty and reward have shared functional properties. It is currently unclear whether functional aspects of reward processing in the SN/VTA, namely, activation by unexpected rewards and cues that predict reward, also characterize novelty processing. To address this question, we conducted an fMRI experiment during which subjects viewed symbolic cues that predicted either novel or familiar images of scenes with 75% validity. We show that SN/VTA was activated by cues predicting novel images as well as by unexpected novel images that followed familiarity-predictive cues, an 'unexpected novelty' response. The hippocampus, a region implicated in detecting and encoding novel stimuli, showed an anticipatory novelty response but differed from the response profile of SN/VTA in responding at outcome to expected and 'unexpected' novelty. In a behavioral extension of the experiment, recollection increased relative to familiarity when comparing delayed recognition memory for anticipated novel stimuli with unexpected novel stimuli. These data reveal commonalities in SN/VTA responses to anticipating reward and anticipating novel stimuli. We suggest that this anticipatory response codes a motivational exploratory novelty signal that, together with anticipatory activation of the hippocampus, leads to enhanced encoding of novel events. In more general terms, the data suggest that dopaminergic processing of novelty might be important in driving exploration of new environments.

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Figures

Fig. 1
Fig. 1
Experimental design. (A) Trial sequence for the study phase. After a familiarization phase, colored cues predicted with an accuracy of 75% whether a familiar or new picture followed. Participants were informed about the probabilities and asked to indicate by button press for each picture whether it was familiar or new. (B) Trial sequence for the memory test. Pictures that had been presented in the study phase one day earlier were shown randomly alternating with new distractor pictures. Participants first made an old/new decision, then reported the quality of their recognition memory according to the remember/know/guess procedure.
Fig. 2
Fig. 2
‘Novelty anticipation’ response: Hemodynamic activity for cues predicting novel pictures vs. cues predicting familiar pictures. (A) Cluster of activation in right SN/VTA. (B) Estimated percent signal change of the hemodynamic response for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [4, − 22, − 12]; error bars indicate SEM. (C) Clusters of activation in bilateral hippocampus. (D) Signal change for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [28, − 10, − 8]; error bars indicate SEM; (A, C) p < 0.005 (uncorrected); p < 0.05 (SVC); cluster size > 5 voxels. (B, D) NC—novelty cue, FC—familiarity cue, EF—expected familiar outcome, UF—unexpected familiar outcome, EN—expected novel outcome, UN—unexpected novel outcome. (B, D) Note that our experimental design did not allow efficient estimation of baseline activity, and thus the absolute values of the parameter estimates are poorly estimated (i.e. the value of 0 on the y axis is somewhat arbitrary), although the differences between parameters are well estimated (Josephs and Henson, 1999).
Fig. 3
Fig. 3
‘Novel outcome’ response: Hemodynamic activity for all novel pictures vs. all familiar pictures, independent of the preceding cue. (A) Cluster of activation in left hippocampus. (B) Estimated percent signal change of the hemodynamic response for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [− 40, − 14, − 14]; error bars indicate SEM. (C) Cluster of activation in right hippocampus. (D) Signal change for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [34, − 22, − 12]; error bars indicate SEM; (A, C) p < 0.005 (uncorrected); p < 0.05 (SVC); cluster size > 5 voxels. (B, D) NC—novelty cue, FC—familiarity cue, EF—expected familiar outcome, UF—unexpected familiar outcome, EN—expected novel outcome, UN—unexpected novel outcome. (B, D) Note that our experimental design did not allow efficient estimation of baseline activity, and thus the absolute values of the parameter estimates are poorly estimated (i.e. the value of 0 on the y axis is somewhat arbitrary), although the differences between parameters are well estimated (Josephs and Henson, 1999).
Fig. 4
Fig. 4
‘Unexpected novelty’ response: Hemodynamic activity for unpredicted novel pictures, i.e. novel pictures shown after cues predicting familiar pictures, vs. predicted novel pictures, i.e. novel pictures predicted by the preceding cue. (A) Cluster of activation in right SN/VTA. (B) Estimated percent signal change of the hemodynamic response for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [12, − 24, − 7]; error bars indicate SEM. (C) Cluster of activation in right hippocampus. (D) Signal change for the two cues (light grey) and four outcome categories (dark grey). Talairach coordinates: [30, − 22, − 7]; error bars indicate SEM; (A, C) p < 0.005 (uncorrected); p < 0.05 (SVC); cluster size > 5 voxels. (B, D) NC—novelty cue, FC—familiarity cue, EF—expected familiar outcome, UF—unexpected familiar outcome, EN—expected novel outcome, UN—unexpected novel outcome. (B, D) Note that our experimental design did not allow efficient estimation of baseline activity, and thus the absolute values of the parameter estimates are poorly estimated (i.e. the value of 0 on the y axis is somewhat arbitrary), although the differences between parameters are well estimated (Josephs and Henson, 1999).
Fig. 5
Fig. 5
Correlation between SN/VTA activation and right hippocampal activity as tested on average percent signal change in response to novelty cues in the peak voxels of the ‘novelty vs. familiarity anticipation’ contrast.
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