Rollik, L. | bioRxiv Science

bioRxiv2024

Replay of procedural experience is independent of the hippocampus

Sleep is critical for consolidating all forms of memory1-3, from episodic experience to the development of motor skills4-6. A core feature of the consolidation process is offline replay of neuronal firing patterns that occur during experience7,8. This replay is thought to originate in the hippocampus and trigger the reactivation of ensembles of cortical and subcortical neurons1,3,9-18. However, non-declarative memories do not require the hippocampus for learning or for sleep-dependent consolidation19-26 meaning what drives their consolidation is unknown. Here we show, using an unsupervised method, that replay occurs in the dorsal striatum of mice during offline consolidation of a non-declarative, procedural, memory and that this replay is generated independently of the hippocampus. Replay occurred at both real-world and time-compressed speeds and was also prioritised both at the level of the individual neurons and the type of neural sequence. Complete bilateral lesions of the hippocampus had no effect on any feature of this replay. Our results demonstrate that procedural replay during consolidation of a non-declarative memory is independent of the hippocampus. These results support the view that replay drives active consolidation of all types of memory during sleep but challenges the idea that the hippocampus is the source of this replay.

neuroscience↗

bioRxiv2022

Action prediction error: a value-free dopaminergic teaching signal that drives stable learning

Animals choice behavior is characterized by two main tendencies: taking actions that led to rewards and repeating past actions. Theory suggests these strategies may be reinforced by different types of dopaminergic teaching signals: reward prediction error (RPE) to reinforce value-based associations and movement-based action prediction errors to reinforce value-free repetitive associations. Here we use an auditory-discrimination task in mice to show that movement-related dopamine activity in the tail of the striatum encodes the hypothesized action prediction error signal. Causal manipulations reveal that this prediction error serves as a value-free teaching signal that supports learning by reinforcing repeated associations. Computational modeling and experiments demonstrate that action prediction errors alone cannot support reward-guided learning but when paired with the RPE circuitry they serve to consolidate stable sound-action associations in a value-free manner. Together we show that there are two types of dopaminergic prediction errors that work in tandem to support learning.

neuroscience↗