Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation.

Hippocampal theta oscillations were proposed to be important for multiple functions, including memory and temporal coding of position. However, previous findings from bats have questioned these proposals by reporting absence of theta rhythmicity in bat hippocampal formation. Does this mean that temporal coding is unique to rodent hippocampus and does not generalize to other species? Here, we report that, surprisingly, bat hippocampal neurons do exhibit temporal coding similar to rodents, albeit without any continuous oscillations at the 1-20 Hz range. Bat neurons exhibited very strong locking to the non-rhythmic fluctuations of the field potential, such that neurons were synchronized together despite the absence of oscillations. Further, some neurons exhibited "phase precession" and phase coding of the bat's position-with spike phases shifting earlier as the animal moved through the place field. This demonstrates an unexpected type of neural coding in the mammalian brain-nonoscillatory phase coding-and highlights the importance of synchrony and temporal coding for hippocampal function across species.

A visual paired associate learning (vPAL) paradigm to study memory consolidation during sleep.

Sleep improves the consolidation and long-term stability of newly formed memories and associations. Most research on human declarative memory and its consolidation during sleep uses word-pair associations requiring exhaustive learning. In the present study, we present the visual paired association learning (vPAL) paradigm, in which participants learn new associations between images of celebrities and animals. The vPAL is based on a one-shot exposure that resembles learning in natural conditions. We tested if vPAL can reveal a role for sleep in memory consolidation by assessing the specificity of memory recognition, and the cued recall performance, before and after sleep. We found that a daytime nap improved the stability of recognition memory and discrimination abilities compared to identical intervals of wakefulness. By contrast, cued recall of associations did not exhibit significant sleep-dependent effects. High-density electroencephalography during naps further revealed an association between sleep spindle density and stability of recognition memory. Thus, the vPAL paradigm opens new avenues for future research on sleep and memory consolidation across ages and heterogeneous populations in health and disease.

Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation.

Spatial orientation and navigation rely on the acquisition of several types of sensory information. This information is then transformed into a neural code for space in the hippocampal formation through the activity of place cells, grid cells and head-direction cells. These spatial representations, in turn, are thought to guide long-range navigation. But how the representations encoded by these different cell types are integrated in the brain to form a neural 'map and compass' is largely unknown. Here, we discuss this problem in the context of spatial navigation by bats and rats. We review the experimental findings and theoretical models that provide insight into the mechanisms that link sensory systems to spatial representations and to large-scale natural navigation.

Proximity to boundaries reveals spatial context representation in human hippocampal CA1.

Recollection of real-world events is often accompanied by a sense of being in the place where the event transpired. Convergent evidence suggests the hippocampus plays a key role in supporting episodic memory by associating information with the time and place it was originally encountered. This representation is reinstated during memory retrieval. However, little is known about the roles of different subfields of the human hippocampus in this process. Research in humans and non-human animal models has suggested that spatial environmental boundaries have a powerful influence on spatial and episodic memory, as well as hippocampal representations of contexts and events. Here, we used high-resolution fMRI to investigate how boundaries influence hippocampal activity patterns during the recollection of objects encountered in different spatial contexts. During the encoding phase, participants viewed objects once in a naturalistic virtual reality task in which they passively explored two rooms in one of two houses. Following the encoding phase, participants were scanned while they recollected items in the absence of any spatial contextual information. Our behavioral results demonstrated that spatial context memory was enhanced for objects encountered near a boundary. Activity patterns in CA1 carried information about the spatial context associated with each of these boundary items. Exploratory analyses revealed that recollection performance was correlated with the fidelity of retrieved spatial context representations in anterior parahippocampal cortex and subiculum. Our results highlight the privileged role of boundaries in CA1 and suggest more generally a close relationship between memory for spatial contexts and representations in the hippocampus and parahippocampal region.

Augmenting hippocampal-prefrontal neuronal synchrony during sleep enhances memory consolidation in humans.

Memory consolidation during sleep is thought to depend on the coordinated interplay between cortical slow waves, thalamocortical sleep spindles and hippocampal ripples, but direct evidence is lacking. Here, we implemented real-time closed-loop deep brain stimulation in human prefrontal cortex during sleep and tested its effects on sleep electrophysiology and on overnight consolidation of declarative memory. Synchronizing the stimulation to the active phases of endogenous slow waves in the medial temporal lobe (MTL) enhanced sleep spindles, boosted locking of brain-wide neural spiking activity to MTL slow waves, and improved coupling between MTL ripples and thalamocortical oscillations. Furthermore, synchronized stimulation enhanced the accuracy of recognition memory. By contrast, identical stimulation without this precise time-locking was not associated with, and sometimes even degraded, these electrophysiological and behavioral effects. Notably, individual changes in memory accuracy were highly correlated with electrophysiological effects. Our results indicate that hippocampo-thalamocortical synchronization during sleep causally supports human memory consolidation.

Click-based echolocation in bats: not so primitive after all.

Echolocating bats of the genus Rousettus produce click sonar signals, using their tongue (lingual echolocation). These signals are often considered rudimentary and are believed to enable only crude performance. However, the main argument supporting this belief, namely the click's reported long duration, was recently shown to be an artifact. In fact, the sonar clicks of Rousettus bats are extremely short, ~50-100 µs, similar to dolphin vocalizations. Here, we present a comparison between the sonar systems of the 'model species' of laryngeal echolocation, the big brown bat (Eptesicus fuscus), and that of lingual echolocation, the Egyptian fruit bat (Rousettus aegyptiacus). We show experimentally that in tasks, such as accurate landing or detection of medium-sized objects, click-based echolocation enables performance similar to laryngeal echolocators. Further, we describe a sophisticated behavioral strategy for biosonar beam steering in clicking bats. Finally, theoretical analyses of the signal design--focusing on their autocorrelations and wideband ambiguity functions--predict that in some aspects, such as target ranging and Doppler-tolerance, click-based echolocation might outperform laryngeal echolocation. Therefore, we suggest that click-based echolocation in bats should be regarded as a viable echolocation strategy, which is in fact similar to the biosonar used by most echolocating animals, including whales and dolphins.

Contextual Codes in the Hippocampus.

The hippocampus is thought to support memory and decisions by binding relevant aspects of experiences within a context. A recent paper by Gulli et al. studies how activity in the macaque hippocampus varies according to different contextual requirements in the same space. This study demonstrates how a hippocampal cognitive map can flexibly reflect both spatial and nonspatial task demands.

Hippocampal global remapping for different sensory modalities in flying bats.

Hippocampal place cells encode the animal's spatial position. However, it is unknown how different long-range sensory systems affect spatial representations. Here we alternated usage of vision and echolocation in Egyptian fruit bats while recording from single neurons in hippocampal areas CA1 and subiculum. Bats flew back and forth along a linear flight track, employing echolocation in darkness or vision in light. Hippocampal representations remapped between vision and echolocation via two kinds of remapping: subiculum neurons turned on or off, while CA1 neurons shifted their place fields. Interneurons also exhibited strong remapping. Finally, hippocampal place fields were sharper under vision than echolocation, matching the superior sensory resolution of vision over echolocation. Simulating several theoretical models of place-cells suggested that combining sensory information and path integration best explains the experimental sharpening data. In summary, here we show sensory-based global remapping in a mammal, suggesting that the hippocampus does not contain an abstract spatial map but rather a 'cognitive atlas', with multiple maps for different sensory modalities.

Measuring and Characterizing the Human Nasal Cycle.

Nasal airflow is greater in one nostril than in the other because of transient asymmetric nasal passage obstruction by erectile tissue. The extent of obstruction alternates across nostrils with periodicity referred to as the nasal cycle. The nasal cycle is related to autonomic arousal and is indicative of asymmetry in brain function. Moreover, alterations in nasal cycle periodicity have been linked to various diseases. There is therefore need for a tool allowing continuous accurate measurement and recording of airflow in each nostril separately. Here we provide detailed instructions for constructing such a tool at minimal cost and effort. We demonstrate application of the tool in 33 right-handed healthy subjects, and derive several statistical measures for nasal cycle characterization. Using these measures applied to 24-hour recordings we observed that: 1: subjects spent slightly longer in left over right nostril dominance (left = 2.63 ± 0.89 hours, right = 2.17 ± 0.89 hours, t(32) = 2.07, p < 0.05), 2: cycle duration was shorter in wake than in sleep (wake = 2.02 ± 1.7 hours, sleep = 4.5 ± 1.7 hours, (t(30) = 5.73, p < 0.0001). 3: slower breathing was associated with a more powerful cycle (the extent of difference across nostrils) (r = 0.4, p < 0.0001), and 4: the cycle was influenced by body posture such that lying on one side was associated with greater flow in the contralateral nostril (p < 0.002). Finally, we provide evidence for an airflow cycle in each nostril alone. These results provide characterization of an easily obtained measure that may have diagnostic implications for neurological disease and cognitive state.