Courtship behaviour reveals temporal regularity is a critical social cue in mouse communication

While animals navigating the real world face a barrage of sensory input, their brains evolved to perceptually compress multidimensional information by selectively extracting the features relevant for survival. Notably, communication signals supporting social interactions in several mammalian species consist of acoustically complex sequences of vocalisations. However, little is known about what information listeners extract from such time-varying sensory streams. Here, we utilise female mice’s natural behavioural response to male courtship songs to identify the relevant acoustic dimensions used in their social decisions. We found that females were highly sensitive to disruptions of song temporal regularity and preferentially approached playbacks of intact over rhythmically irregular versions of male songs. In contrast, female behaviour was invariant to manipulations affecting the songs’ sequential organisation or the spectro-temporal structure of individual syllables. The results reveal temporal regularity as a key acoustic cue extracted by mammalian listeners from complex vocal sequences during goal-directed social behaviour

Memory capacity and prioritization in female mice

Our brain's capacity for memory storage may be vast but is still finite. Given that we cannot remember the entirety of our experiences, how does our brain select what to remember and what to forget? Much like the triage of a hospital's emergency room, where urgent cases are prioritized and less critical patients receive delayed or even no care, the brain is believed to go through a similar process of memory triage. Recent salient memories are prioritized for consolidation, which helps create stable, long-term representations in the brain; less salient memories receive a lower priority, and are eventually forgotten if not sufficiently consolidated (Stickgold and Walker in Nat Neurosci 16(2):139-145, 2013). While rodents are a primary model for studying memory consolidation, common behavioral tests typically rely on a limited number of items or contexts, well within the memory capacity of the subject. A memory test allowing us to exceed an animal's memory capacity is key to investigating how memories are selectively strengthened or forgotten. Here we report a new serial novel object recognition task designed to measure memory capacity and prioritization, which we test and validate using female mice

A review of neurobiological factors underlying the selective enhancement of memory at encoding, consolidation, and retrieval

How is the strength of a memory determined? This review discusses three main factors that contribute to memory enhancement - 1) emotion, 2) targeted memory reactivation, and 3) neural reinstatement. Whilst the mechanisms through which memories become enhanced vary, this review demonstrates that activation of the basolateral amygdala and hippocampal formation are crucial for facilitating encoding, consolidation, and retrieval. Here we suggest methodological factors to consider in future studies, and discuss several unanswered questions that should be pursued in order to clarify selective memory enhancement

Awake replay: off the clock but on the job

Hippocampal replay is widely thought to support two key cognitive functions: online decision-making and offline memory consolidation. In this review, we take a closer look at the hypothesized link between awake replay and online decision-making in rodents, and find only marginal evidence in support of this role. By contrast, the consolidation view is bolstered by new computational ideas and recent data, suggesting that (i) replay performs offline fictive learning for later goal-oriented behavior; and (ii) replay tags memories prior to sleep, prioritizing them for consolidation. Based on these recent advances, we favor an updated and refined role for awake replay – that is, supporting prioritized offline learning and tagging outside the hippocampus – rather than a direct, online role in guiding behavior

The role of experience in prioritizing hippocampal replay

During sleep, recent memories are replayed by the hippocampus, leading to their consolidation, with a higher priority given to salient experiences. To examine the role of replay in the selective strengthening of memories, we recorded large ensembles of hippocampal place cells while male rats ran repeated spatial trajectories on two linear tracks, differing in either their familiarity or number of laps run. We observed that during sleep, the rate of replay events for a given track increased proportionally with the number of spatial trajectories run by the animal. In contrast, the rate of sleep replay events decreased if the animal was more familiar with the track. Furthermore, we find that the cumulative number of awake replay events occurring during behavior, influenced by both the novelty and duration of an experience, predicts which memories are prioritized for sleep replay, providing a more parsimonious neural correlate for the selective strengthening of memories

Experience-driven rate modulation is reinstated during hippocampal replay

Replay, the sequential reactivation within a neuronal ensemble, is a central hippocampal mechanism postulated to drive memory processing. While both rate and place representations are used by hippocampal place cells to encode behavioral episodes, replay has been largely defined by only the latter - based on the fidelity of sequential activity across neighboring place fields. Here we show that dorsal CA1 place cells in rats can modulate their firing rate between replay events of two different contexts. This experience-dependent phenomenon mirrors the same pattern of rate modulation observed during behavior and can be used independently from place information within replay sequences to discriminate between contexts. Our results reveal the existence of two complementary neural representations available for memory processes

Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

Theta oscillations are a hallmark of hippocampal activity across mammals and play a critical role in many hippocampal models of memory and spatial navigation. To reconcile the cross-species differences observed in the presence and properties of theta, we recorded hippocampal local field potentials in rats and ferrets during auditory and visual localisation tasks designed to vary locomotion and sensory attention. Here, we show that theta oscillations occur during locomotion in both ferrets and rats, however during periods of immobility, theta oscillations persist in the ferret, contrasting starkly with the switch to large irregular activity (LIA) in the rat. Theta during immobility in the ferret is identified as analogous to Type 2 theta that has been observed in rodents due to its sensitivity to atropine, and is modulated by behavioural state with the strongest theta observed during reward epochs. These results demonstrate that even under similar behavioural conditions, differences exist between species in the relationship between theta and behavioural state

Insights on the Neuromagnetic Representation of Temporal Asymmetry in Human Auditory Cortex.

Communication sounds are typically asymmetric in time and human listeners are highly sensitive to this short-term temporal asymmetry. Nevertheless, causal neurophysiological correlates of auditory perceptual asymmetry remain largely elusive to our current analyses and models. Auditory modelling and animal electrophysiological recordings suggest that perceptual asymmetry results from the presence of multiple time scales of temporal integration, central to the auditory periphery. To test this hypothesis we recorded auditory evoked fields (AEF) elicited by asymmetric sounds in humans. We found a strong correlation between perceived tonal salience of ramped and damped sinusoids and the AEFs, as quantified by the amplitude of the N100m dynamics. The N100m amplitude increased with stimulus half-life time, showing a maximum difference between the ramped and damped stimulus for a modulation half-life time of 4 ms which is greatly reduced at 0.5 ms and 32 ms. This behaviour of the N100m closely parallels psychophysical data in a manner that: i) longer half-life times are associated with a stronger tonal percept, and ii) perceptual differences between damped and ramped are maximal at 4 ms half-life time. Interestingly, differences in evoked fields were significantly stronger in the right hemisphere, indicating some degree of hemispheric specialisation. Furthermore, the N100m magnitude was successfully explained by a pitch perception model using multiple scales of temporal integration of auditory nerve activity patterns. This striking correlation between AEFs, perception, and model predictions suggests that the physiological mechanisms involved in the processing of pitch evoked by temporal asymmetric sounds are reflected in the N100m

Predictive maps in rats and humans for spatial navigation

Much of our understanding of navigation comes from the study of individual species, often with specific tasks tailored to those species. Here, we provide a novel experimental and analytic framework integrating across humans, rats, and simulated reinforcement learning (RL) agents to interrogate the dynamics of behavior during spatial navigation. We developed a novel open-field navigation task ("Tartarus maze") requiring dynamic adaptation (shortcuts and detours) to frequently changing obstructions on the path to a hidden goal. Humans and rats were remarkably similar in their trajectories. Both species showed the greatest similarity to RL agents utilizing a "successor representation," which creates a predictive map. Humans also displayed trajectory features similar to model-based RL agents, which implemented an optimal tree-search planning procedure. Our results help refine models seeking to explain mammalian navigation in dynamic environments and highlight the utility of modeling the behavior of different species to uncover the shared mechanisms that support behavior