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Research on rodents and non-human primates has established the involvement of the superior colliculus in defensive behaviours and visual threat detection. The superior colliculus has been well-studied in humans for its functional roles in saccade and visual processing, but less is known about its involvement in affect. In standard functional MRI studies of the human superior colliculus, it is challenging to discern activity in the superior colliculus from activity in surrounding nuclei such as the periaqueductal gray due to technological and methodological limitations. Employing high-field strength (7 Tesla) fMRI techniques, this study imaged the superior colliculus at high (0.75 mm isotropic) resolution, which enabled isolation of the superior colliculus from other brainstem nuclei. Superior colliculus activation during emotionally aversive image viewing blocks was greater than that during neutral image viewing blocks. These findings suggest that the superior colliculus may play a role in shaping subjective emotional experiences in addition to its visuomotor functions, bridging the gap between affective research on humans and non-human animals.

No abstract

Motivation influences goals, decisions, and memory formation. Imperative motivation links urgent goals to actions, whereas interrogative motivation integrates goals over time and space, thus supporting broader learning. We induced motivational states by manipulating only the cover stories for a reinforcement learning task: The Imperative group imagined executing a museum heist, whereas the Interrogative group imagined planning a future heist. Participants repeatedly chose from four “doors” to sample trial-unique paintings with variable rewards, then performed a surprise next-day memory test. During reinforcement learning, the Interrogative group showed more directed (but not random) exploration and less exploitation relative to the Imperative group. At test, the Interrogative group showed superior recognition of paintings, metamemory sensitivity, and reward modulation of memory relative to the Imperative group. We show that a subtle instructional manipulation can modulate motivational states to simultaneously bias reinforcement learning and memory formation, bearing implications for education, behavior change, and clinical interventions.

Motivation influences goals, decisions, and memory formation. Imperative motivation links urgent goals to actions, narrowing the focus of attention and memory. Conversely, interrogative motivation integrates goals over time and space, supporting rich memory encoding for flexible future use. We manipulated motivational states via cover stories for a reinforcement learning task: The imperative group imagined executing a museum heist, whereas the interrogative group imagined planning a future heist. Participants repeatedly chose among four doors, representing different museum rooms, to sample trial-unique paintings with variable rewards (later converted to bonus payments). The next day, participants performed a surprise memory test. Crucially, only the cover stories differed between the imperative and interrogative groups; the reinforcement learning task was identical, and all participants had the same expectations about how and when bonus payments would be awarded. In an initial sample and a preregistered replication, we demonstrated that imperative motivation increased exploitation during reinforcement learning. Conversely, interrogative motivation increased directed (but not random) exploration, despite the cost to participants’ earnings. At test, the interrogative group was more accurate at recognizing paintings and recalling associated values. In the interrogative group, higher value paintings were more likely to be remembered; imperative motivation disrupted this effect of reward modulating memory. Overall, we demonstrate that a prelearning motivational manipulation can bias learning and memory, bearing implications for education, behavior change, clinical interventions, and communication.