Sideways maneuvers enable narrow aperture negotiation by free-flying hummingbirds.

Many birds routinely fly fast through dense vegetation characterized by variably sized structures and voids. Successfully negotiating these cluttered environments requires maneuvering through narrow constrictions between obstacles. We show that Anna's hummingbirds (Calypte anna) can negotiate apertures less than one wingspan in diameter using a novel sideways maneuver that incorporates continuous, bilaterally asymmetric wing motions. Crucially, this maneuver allows hummingbirds to continue flapping as they negotiate the constriction. Even smaller openings are negotiated via a faster ballistic trajectory characterized by tucked and thus non-flapping wings, which reduces force production and increases descent rate relative to the asymmetric technique. Hummingbirds progressively shift to the swept method as they perform hundreds of consecutive transits, suggesting increased locomotor performance with task familiarity. Initial use of the slower asymmetric transit technique may allow birds to better assess upcoming obstacles and voids, thereby reducing the likelihood of subsequent collisions. Repeated disruptions of normal wing kinematics as birds negotiate tight apertures may determine the limits of flight performance in structurally complex environments. These strategies for aperture transit and associated flight trajectories can inform designs and algorithms for small aerial vehicles flying within cluttered environments.

ThermoMaze: A behavioral paradigm for readout of immobility-related brain events.

Brain states fluctuate between exploratory and consummatory phases of behavior. These state changes affect both internal computation and the organism's responses to sensory inputs. Understanding neuronal mechanisms supporting exploratory and consummatory states and their switching requires experimental control of behavioral shifts and collecting sufficient amounts of brain data. To achieve this goal, we developed the ThermoMaze, which exploits the animal's natural warmth-seeking homeostatic behavior. By decreasing the floor temperature and selectively heating unmarked areas, mice avoid the aversive state by exploring the maze and finding the warm spot. In its design, the ThermoMaze is analogous to the widely used water maze but without the inconvenience of a wet environment and, therefore, allows the collection of physiological data in many trials. We combined the ThermoMaze with electrophysiology recording, and report that spiking activity of hippocampal CA1 neurons during sharp-wave ripple events encode the position of the animal. Thus, place-specific firing is not confined to locomotion and associated theta oscillations but persist during waking immobility and sleep at the same location. The ThermoMaze will allow for detailed studies of brain correlates of immobility, preparatory-consummatory transitions and open new options for studying behavior-mediated temperature homeostasis.

A consensus statement on detection of hippocampal sharp wave ripples and differentiation from other fast oscillations.

Decades of rodent research have established the role of hippocampal sharp wave ripples (SPW-Rs) in consolidating and guiding experience. More recently, intracranial recordings in humans have suggested their role in episodic and semantic memory. Yet, common standards for recording, detection, and reporting do not exist. Here, we outline the methodological challenges involved in detecting ripple events and offer practical recommendations to improve separation from other high-frequency oscillations. We argue that shared experimental, detection, and reporting standards will provide a solid foundation for future translational discovery.

A metabolic function of the hippocampal sharp wave-ripple.

The hippocampus has previously been implicated in both cognitive and endocrine functions1-15. We simultaneously measured electrophysiological activity from the hippocampus and interstitial glucose concentrations in the body of freely behaving rats to identify an activity pattern that may link these disparate functions of the hippocampus. Here we report that clusters of sharp wave-ripples recorded from the hippocampus reliably predicted a decrease in peripheral glucose concentrations within about 10 min. This correlation was not dependent on circadian, ultradian or meal-triggered fluctuations, could be mimicked with optogenetically induced ripples in the hippocampus (but not in the parietal cortex) and was attenuated to chance levels by pharmacogenetically suppressing activity of the lateral septum, which is the major conduit between the hippocampus and the hypothalamus. Our findings demonstrate that a function of the sharp wave-ripple is to modulate peripheral glucose homeostasis, and offer a mechanism for the link between sleep disruption and blood glucose dysregulation in type 2 diabetes16-18.

Variable specificity of memory trace reactivation during hippocampal sharp wave ripples.

Hippocampal sharp wave-ripples (SWR) are thought to mediate brain-wide reactivation of memory traces in service of memory consolidation. However, rather than the faithful replay of neural activity observed during a specific experience, reactivation in both the hippocampus and downstream regions is more variable. We suggest that variable reactivation is a unifying feature of recurrent brain circuits. In the hippocampus, self-organized activation during offline states is constrained by existing attractor manifolds, or maps, and may be biased toward particular mapped locations by salient experience, which results in the appearance of experience-specific replay. Similarly, the impact of SWR-associated reactivation on downstream regions is not a simple transfer of hippocampal representational content. Rather, the response of downstream regions depends on a transformation function, defined by both the feedforward and local circuit architecture, as well as the 'listening state' of the downstream region. We hypothesize that SWRs act as a multiplexed signal, the mnemonic specificity of which is largely determined by this transformation function, and discuss the implications of this framing for theories of systems consolidation.

Position-theta-phase model of hippocampal place cell activity applied to quantification of running speed modulation of firing rate.

Spiking activity of place cells in the hippocampus encodes the animal's position as it moves through an environment. Within a cell's place field, both the firing rate and the phase of spiking in the local theta oscillation contain spatial information. We propose a position-theta-phase (PTP) model that captures the simultaneous expression of the firing-rate code and theta-phase code in place cell spiking. This model parametrically characterizes place fields to compare across cells, time, and conditions; generates realistic place cell simulation data; and conceptualizes a framework for principled hypothesis testing to identify additional features of place cell activity. We use the PTP model to assess the effect of running speed in place cell data recorded from rats running on linear tracks. For the majority of place fields, we do not find evidence for speed modulation of the firing rate. For a small subset of place fields, we find firing rates significantly increase or decrease with speed. We use the PTP model to compare candidate mechanisms of speed modulation in significantly modulated fields and determine that speed acts as a gain control on the magnitude of firing rate. Our model provides a tool that connects rigorous analysis with a computational framework for understanding place cell activity.

Enrichment drives emergence of functional columns and improves sensory coding in the whisker map in L2/3 of mouse S1.

Sensory maps in layer (L) 2/3 of rodent cortex lack precise functional column boundaries, and instead exhibit locally heterogeneous (salt-and-pepper) tuning superimposed on smooth global topography. Could this organization be a byproduct of impoverished experience in laboratory housing? We compared whisker map somatotopy in L2/3 and L4 excitatory cells of somatosensory (S1) cortex in normally housed vs. tactile-enriched mice, using GCaMP6s imaging. Normally housed mice had a dispersed, salt-and-pepper whisker map in L2/3, but L4 was more topographically precise. Enrichment (P21 to P46-71) sharpened whisker tuning and decreased, but did not abolish, local tuning heterogeneity. In L2/3, enrichment strengthened and sharpened whisker point representations, and created functional boundaries of tuning similarity and noise correlations at column edges. Thus, enrichment drives emergence of functional columnar topography in S1, and reduces local tuning heterogeneity. These changes predict better touch detection by neural populations within each column.