Examining the Role of the Human Hippocampus in Approach-Avoidance Decision Making Using a Novel Conflict Paradigm and Multivariate Functional Magnetic Resonance Imaging

Abstract

Rodent models of anxiety have implicated the ventral hippocampus in approach-avoidance conflict processing. Few studies have, however, examined whether the human hippocampus plays a similar role. We developed a novel decision-making paradigm to examine neural activity when participants made approach/avoidance decisions under conditions of high or absent approach-avoidance conflict. Critically, our task required participants to learn the associated reward/punishment values of previously neutral stimuli and controlled for mnemonic and spatial processing demands, both important issues given approach-avoidance behavior in humans is less tied to predation and foraging compared to rodents. Participants played a points-based game where they first attempted to maximize their score by determining which of a series of previously neutral image pairs should be approached or avoided. During functional magnetic resonance imaging, participants were then presented with novel pairings of these images. These pairings consisted of images of congruent or opposing learned valences, the latter creating conditions of high approach-avoidance conflict. A data-driven partial least squares multivariate analysis revealed two reliable patterns of activity, each revealing differential activity in the anterior hippocampus, the homolog of the rodent ventral hippocampus. The first was associated with greater hippocampal involvement during trials with high as opposed to no approach-avoidance conflict, regardless of approach or avoidance behavior. The second pattern encompassed greater hippocampal activity in a more anterior aspect during approach compared to avoid responses, for conflict and no-conflict conditions. Multivoxel pattern classification analyses yielded converging findings, underlining a role of the anterior hippocampus in approach-avoidance conflict decision making.

Significance statement: Approach-avoidance conflict has been linked to anxiety and occurs when a stimulus or situation is associated with reward and punishment. Although rodent work has implicated the hippocampus in approach-avoidance conflict processing, there is limited data on whether this role applies to learned, as opposed to innate, incentive values, and whether the human hippocampus plays a similar role. Using functional neuroimaging with a novel decision-making task that controlled for perceptual and mnemonic processing, we found that the human hippocampus was significantly active when approach-avoidance conflict was present for stimuli with learned incentive values. These findings demonstrate a role for the human hippocampus in approach-avoidance decision making that cannot be explained easily by hippocampal-dependent long-term memory or spatial cognition.

Keywords: approach–avoidance conflict; decision making; functional magnetic resonance imaging; hippocampus; memory.

Figure 1.

A, Examples of two positive valence and two negative valence face–scene image pairs (total 30 pairs each) along with the number of points gained or deducted following an approach (Ap) or avoid (Av) response. B, Schematic representation of the approach/avoidance and scrambled baseline trials. Each face–scene pair was followed by a feedback screen indicating the number of points gained or lost as well as the participant's cumulative score. No feedback was provided for the scrambled baseline trials.

Figure 2.

A, Examples of the recombined face–scene pairs that were presented during the decision phase (20 no-conflict positive, 20 no-conflict negative, and 20 conflict mixed pairs per fMRI run). The presented examples are recombinations of the image pairs shown in Figure 1A. No-conflict pairs were comprised of images from the learning phase of the same valence, whereas high-conflict pairs consisted of images from the learning phase of opposing valences. B, Schematic representation of the decision and scrambled baseline trials during fMRI scanning. No feedback was provided during the decision phase.

Figure 3.

A, B, Proportion of approach responses (±SE; A) and mean response times (±SE; B) across the 12 learning phase blocks and the refresher block (R) for the positive and negative valence face–scene pairs. C, Proportion of approach responses (±SE) across the three decision fMRI runs for no-conflict negative valence recombined pairs, no-conflict positive valence recombined pairs, and conflict mixed valence recombined pairs. D, Mean response times (±SE) across the three decision fMRI runs for no-conflict negative valence avoid trials, no-conflict positive valence approach trials, conflict mixed valence avoid trials, and conflict mixed valence approach trials.

Figure 4.

A, Significant relationship (r = 0.77, p < 0.0001) between no-conflict avoidance bias (proportion of avoid responses on no-conflict negative trials minus proportion of approach responses on no-conflict positive trials) and conflict avoidance bias (proportion of avoid responses minus proportion of approach responses on conflict mixed trials). B, Significant difference between mean no-conflict avoidance bias and conflict avoidance bias (t₍₁₇₎ = 2.23, p = 0.040). Error bars indicate SE.

Figure 5.

A, Linear contrast associated with the latent variable differentiating conflict conditions from the no-conflict and scrambled baseline conditions. Error bars indicate 95% CIs. B, Pattern of activity relating to A at TR2, with hippocampal activity highlighted with the red circles. Warm colors indicate greater activity during conflict trials compared to no-conflict and scrambled baseline trials, whereas cool colors indicate the opposite. Activity was thresholded at a bootstrap ratio of 2.81 (equivalent to p = 0.005) and rendered on the MNI-152 standard template (the left hemisphere on the coronal slice is the left side of the image). The voxel intensities (±SE) across conditions for the hippocampal voxel contributing most robustly to this pattern are also presented for display purposes.

Figure 6.

A, Linear contrast associated with the latent variable differentiating approach from avoid responses for no-conflict and conflict trials. Error bars indicate 95% CIs. B, Pattern of activity relating to A at TR2, with hippocampal activity highlighted with the red circles. Warm colors indicate greater activity during conflict trials compared to no-conflict and scrambled baseline trials, whereas cool colors indicate the opposite. Activity was thresholded at a bootstrap ratio of 2.81 (equivalent to p = 0.005) and rendered on the MNI-152 standard template (the left hemisphere on the coronal slice is the left side of the image). The voxel intensities (±SE) across conditions for the hippocampal voxel contributing most robustly to this pattern are also presented for display purposes.