Online evaluation of novel choices by simultaneous representation of multiple memories

Abstract

Prior experience is critical for decision-making. It enables explicit representation of potential outcomes and provides training to valuation mechanisms. However, we can also make choices in the absence of prior experience by merely imagining the consequences of a new experience. Using functional magnetic resonance imaging repetition suppression in humans, we examined how neuronal representations of novel rewards can be constructed and evaluated. A likely novel experience was constructed by invoking multiple independent memories in hippocampus and medial prefrontal cortex. This construction persisted for only a short time period, during which new associations were observed between the memories for component items. Together, these findings suggest that, in the absence of direct experience, coactivation of multiple relevant memories can provide a training signal to the valuation system that allows the consequences of new experiences to be imagined and acted on.

Figure 1. Experimental Design

(a) Thirteen novel ‘goods’ were made, each from the combination of two familiar food types that had not previously been tasted together. Two examples are shown here: avocado and raspberry smoothie (‘AB’), and tea-jelly ( ‘CD’). (b) Participants made binary decisions between the novel goods whilst in the scanner. (c) Prior to entering the scanner, two of the novel goods were chosen for each participant. Participants learnt to associate each of these novel goods and their respective components with two abstract stimuli. (d) In the scanner, participants vividly imagined the sensory properties of the food items in response to each abstract stimulus presented.

Figure 2. Neural correlates of constructing and evaluating a novel good

(a) Whilst participants made binary choices between novel goods, the mPFC (extending into dmPFC) encoded chosen value. (b) The mPFC and hippocampus showed repetition suppression to a novel good when preceded by a related component (e.g. tea-jelly preceded by tea), compared to when preceded by an unrelated component (e.g. tea-jelly preceded by avocado). (c) The mPFC showed repetition suppression to a component food item when preceded by the related component (e.g. tea preceded by jelly), compared to when preceded by an unrelated component (e.g. tea preceded by avocado). (d)(e) In mPFC and hippocampus respectively, a significant positive correlation was revealed between the amount of suppression between related components (across all blocks) and the average value participants assigned to the novel goods (after removing effects attributable to the value of the components, for mPFC: r = 0.51, p = 0.015, and hippocampus: r = 0.60, p = 0.004). (f) Both adaptation effects showed comparable effect size across the ventral-to-dorsal gradient of mPFC (mean ± s.e. across participants). Location of the ROIs is shown, and the effect size for both adaptation measures was scaled such that the peak value was equal to one. There was no significant difference between the two adaptation effects at any point on this gradient.

Figure 3. Sensory exposure to a novel good: comparison between the ‘unfamiliar’ and ‘familiar’ groups during the decision making task

(a) In the familiar group, the mPFC correlated with chosen value during the decision making task (thresholded at p<0.01, uncorrected for visualisation). (b) ROI used to assess value signals in both groups of participants during the decision task. (c) During the decision making task the unfamiliar and familiar groups showed comparable chosen value signals in mPFC (left side: average of all task blocks for each group), and in the unfamiliar group there was no change in the chosen value signal across time (right side: block 1 versus blocks 2 and 3). Parameter estimates were extracted from ROI shown in b (mean ± s.e. across participants).

Figure 4. Sensory exposure to a novel good: comparison between the ‘unfamiliar’ and ‘familiar’ groups during construction of a novel good

(a) ROI used to compare mPFC adaptation effects. (b) ROI used to compare hippocampus adaptation effects. (c) In mPFC the familiar group showed less adaptation between the novel-goods and their related components (left: p = 0.053, trend) and significantly less adaptation between related components (middle: p = 0.033; both extracted from ROI shown in a). In the hippocampus, the familiar group showed significantly less adaptation between the novel-goods and their related components (right: p = 0.008, extracted from ROIs shown in b). The stars (*) indicate p<0.05; bars and vertical lines correspond to mean ± s.e. across participants.

Figure 5. In the absence of sensory exposure, there was evidence for the construction mechanism only in early trials: block 1 compared to block 2 and 3 for unfamiliar subjects

(a) There was significantly less adaptation in blocks 2 and 3 between the novel-goods and their related components in mPFC and hippocampus respectively (left and middle: p = 0.024 and p = 0.024 respectively, ROIs shown). There was no significant reduction across time in mPFC adaptation of a component item to itself, when predicted by two different stimuli (right: p = 0.326, ROI shown). (b)(c) On the imagination task, the unfamiliar group showed an increase in accuracy (b) and a decrease in reaction time (c) across blocks. The stars (*) indicate p<0.05; bars and vertical lines correspond to mean ± s.e. across participants.

Figure 6. In the absence of sensory exposure, repetition suppression between related components was maintained across the duration of the experiment only if participants assigned high value to the compound goods

(a) Participants from the unfamiliar group showed significant reduction in adaptation between related components over time in mPFC, but not hippocampus (p = 0.041 and p = 0.785 respectively, ROIs shown). (b)(d) The correlations shown in Fig.2 were also significant in mPFC, b, and hippocampus, d, when considering suppression effects between related components in blocks 2 and 3 alone: the amount of suppression across participants correlated positively with the average value of the compound goods (mPFC: r = 0.64, p = 0.002; hippocampus: r = 0.63, p = 0.003). (c)(e) A median split of participants into those that assigned high and low values to the compound goods revealed significant suppression between related components in blocks 2 and 3 only in those participants who assigned high value (c ,mPFC: ‘High’ p = 0.022, and ‘High vs Low’ p = 0.028; e, hippocampus: ‘High’ p = 0.008, and ‘High vs Low’ p<0.001). The stars (*) indicate p<0.05; bars and vertical lines correspond to mean ± s.e. across participants.