Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally ...and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal's awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes' undulatory body motions induce reafferent feedback that can encode the body's instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors' preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Accurate sensory processing during movement requires the animal to distinguish between external (exafferent) and self-generated (reafferent) stimuli to maintain sensitivity to biologically relevant ...cues. The lateral line system in fishes is a mechanosensory organ that experiences reafferent sensory feedback, via detection of fluid motion relative to the body generated during behaviors such as swimming. For the first time in larval zebrafish (
), we employed simultaneous recordings of lateral line and motor activity to reveal the activity of afferent neurons arising from endogenous feedback from hindbrain efferent neurons during locomotion. Frequency of spontaneous spiking in posterior lateral line afferent neurons decreased during motor activity and was absent for more than half of swimming trials. Targeted photoablation of efferent neurons abolished the afferent inhibition that was correlated to swimming, indicating that inhibitory efferent neurons are necessary for modulating lateral line sensitivity during locomotion. We monitored calcium activity with
fish and found synchronous activity between putative cholinergic efferent neurons and motor neurons. We examined correlates of motor activity to determine which may best predict the attenuation of afferent activity and therefore what components of the motor signal are translated through the corollary discharge. Swim duration was most strongly correlated to the change in afferent spike frequency. Attenuated spike frequency persisted past the end of the fictive swim bout, suggesting that corollary discharge also affects the glide phase of burst and glide locomotion. The duration of the glide in which spike frequency was attenuated increased with swim duration but decreased with motor frequency. Our results detail a neuromodulatory mechanism in larval zebrafish that adaptively filters self-generated flow stimuli during both the active and passive phases of locomotion.
For the first time in vivo, we quantify the endogenous effect of efferent activity on afferent gain control in a vertebrate hair cell system during and after locomotion. We believe that this pervasive effect has been underestimated when afferent activity of octavolateralis systems is characterized in the current literature. We further identify a refractory period out of phase with efferent control and place this gain mechanism in the context of gliding behavior of freely moving animals.
Animals exhibit an abundant diversity of forms, and this diversity is even more evident when considering animals that can change shape on demand. The evolution of flexibility contributes to aspects ...of performance from propulsive efficiency to environmental navigation. It is, however, challenging to quantify and compare body parts that, by their nature, dynamically vary in shape over many time scales. Commonly, body configurations are tracked by labelled markers and quantified parametrically through conventional measures of size and shape (descriptor approach) or non-parametrically through data-driven analyses that broadly capture spatiotemporal deformation patterns (shape variable approach). We developed a weightless marker tracking technique and combined these analytic approaches to study wing morphological flexibility in hoverfeeding Anna's hummingbirds (Calypte anna). Four shape variables explained >95% of typical stroke cycle wing shape variation and were broadly correlated with specific conventional descriptors such as wing twist and area. Moreover, shape variables decomposed wing deformations into pairs of in-plane and out-of-plane components at integer multiples of the stroke frequency. This property allowed us to identify spatiotemporal deformation profiles characteristic of hoverfeeding with experimentally imposed kinematic constraints, including through shape variables explaining <10% of typical shape variation. Hoverfeeding in front of a visual barrier restricted stroke amplitude and elicited increased stroke frequencies together with in-plane and out-of-plane deformations throughout the stroke cycle. Lifting submaximal loads increased stroke amplitudes at similar stroke frequencies together with prominent in-plane deformations during the upstroke and pronation. Our study highlights how spatially and temporally distinct changes in wing shape can contribute to agile fluidic locomotion.
Bird flight is a remarkable adaptation that has allowed the approximately 10 000 extant species to colonize all terrestrial habitats on earth including high elevations, polar regions, distant ...islands, arid deserts, and many others. Birds exhibit numerous physiological and biomechanical adaptations for flight. Although bird flight is often studied at the level of aerodynamics, morphology, wingbeat kinematics, muscle activity, or sensory guidance independently, in reality these systems are naturally integrated. There has been an abundance of new studies in these mechanistic aspects of avian biology but comparatively less recent work on the physiological ecology of avian flight. Here we review research at the interface of the systems used in flight control and discuss several common themes. Modulation of aerodynamic forces to respond to different challenges is driven by three primary mechanisms: wing velocity about the shoulder, shape within the wing, and angle of attack. For birds that flap, the distinction between velocity and shape modulation synthesizes diverse studies in morphology, wing motion, and motor control. Recently developed tools for studying bird flight are influencing multiple areas of investigation, and in particular the role of sensory systems in flight control. How sensory information is transformed into motor commands in the avian brain remains, however, a largely unexplored frontier.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Flying animals of different masses vary widely in body proportions, but the functional implications of this variation are often unclear. We address this ambiguity by developing an integrative ...allometric approach, which we apply here to hummingbirds to examine how the physical environment, wing morphology and stroke kinematics have contributed to the evolution of their highly specialised flight. Surprisingly, hummingbirds maintain constant wing velocity despite an order of magnitude variation in body weight; increased weight is supported solely through disproportionate increases in wing area. Conversely, wing velocity increases with body weight within species, compensating for lower relative wing area in larger individuals. By comparing inter- and intraspecific allometries, we find that the extreme wing area allometry of hummingbirds is likely an adaptation to maintain constant burst flight capacity and induced power requirements with increasing weight. Selection for relatively large wings simultaneously maximises aerial performance and minimises flight costs, which are essential elements of humming bird life history.
Behavioural flexibility allows ectotherms to exploit the environment to govern their metabolic physiology, including in response to environmental stress. Hydrogen sulfide (H
S) is a widespread ...environmental toxin that can lethally inhibit metabolism. However, H
S can also alter behaviour and physiology, including a hypothesized induction of hibernation-like states characterized by downward shifts of the innate thermal set point (anapyrexia). Support for this hypothesis has proved controversial because it is difficult to isolate active and passive components of thermoregulation, especially in animals with high resting metabolic heat production. Here, we directly test this hypothesis by leveraging the natural behavioural thermoregulatory drive of fish to move between environments of different temperatures in accordance with their current physiological state and thermal preference. We observed a decrease in adult zebrafish (
) preferred body temperature with exposure to 0.02% H
S, which we interpret as a shift in the thermal set point. Individuals exhibited consistent differences in shuttling behaviour and preferred temperatures, which were reduced by a constant temperature magnitude during H
S exposure. Seeking lower temperatures alleviated H
S-induced metabolic stress, as measured by reduced rates of aquatic surface respiration. Our findings highlight the interactions between individual variation and sublethal impacts of environmental toxins on behaviour.
Although intraspecific variation in metabolic rate is associated with variation in body size, similarly sized individuals nonetheless vary greatly. At similar masses, hovering bumblebee workers ...(Bombus impatiens) can differ in metabolic rate up to twofold. We examined how such interindividual variation arises by studying covariation of flight metabolic rate with morphological and other physiological parameters. Body size alone explained roughly half the variation in flight metabolic rate. The remaining variation could be explained as the outcome of variation in wing morphology and possibly an association with variation in flight muscle metabolic enzyme activities. As shown using statistical models, for a given mass, higher metabolic rate was correlated with both higher thoracic temperature and higher wing stroke frequency, in turn resulting from smaller wing surface area. When organismal and cellular metabolism for a given mass were linked, variation in metabolic rate was positively correlated with the activities of trehalase and hexokinase. Altogether, covariation with morphology and other physiological parameters explains up to 75% of the variation in metabolic rate. We also investigated the role of flight experience and show that neither flight restriction nor the number of lifetime flights affected flight energetics or flight muscle phenotype. Additionally, manipulating the level of wing asymmetry increased flight wing stroke frequency, metabolic rate, and thoracic temperature, but it did not alter enzyme activity. We conclude that idiosyncrasies in body morphology largely explained interindividual variation in flight metabolic rate but flight muscle metabolic phenotype shows little variation associated with differences in flight experience.
Celotno besedilo
Dostopno za:
BFBNIB, DOBA, IZUM, KILJ, NMLJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Manoeuvring flight in animals requires precise adjustments of mechanical power output produced by the flight musculature. In many insects such as fruit flies, power generation is most likely varied ...by altering stretch-activated tension, that is set by sarcoplasmic calcium levels. The muscles reside in a thoracic shell that simultaneously drives both wings during wing flapping. Using a genetically expressed muscle calcium indicator, we here demonstrate in vivo the ability of this animal to bilaterally adjust its calcium activation to the mechanical power output required to sustain aerodynamic costs during flight. Motoneuron-specific comparisons of calcium activation during lift modulation and yaw turning behaviour suggest slightly higher calcium activation for dorso-longitudinal than for dorsoventral muscle fibres, which corroborates the elevated need for muscle mechanical power during the wings’ downstroke. During turning flight, calcium activation explains only up to 54 per cent of the required changes in mechanical power, suggesting substantial power transmission between both sides of the thoracic shell. The bilateral control of muscle calcium runs counter to the hypothesis that the thorax of flies acts as a single, equally proportional source for mechanical power production for both flapping wings. Collectively, power balancing highlights the precision with which insects adjust their flight motor to changing energetic requirements during aerial steering. This potentially enhances flight efficiency and is thus of interest for the development of technical vehicles that employ bioinspired strategies of power delivery to flapping wings.
The effects of habitat restoration are usually studied using cross‐sectional comparisons of species assemblages among sites of various ages or disturbance levels. Longitudinal studies, however, are ...necessary for detecting long‐term responses to habitat restoration and for understanding annual demographic variation.
To investigate the time course of bee community restoration in sites previously made uninhabitable by anthropogenic disturbance, we studied a former landfill site for 10 years from initial revegetation in 2003 until 2013, comparing two restored sites with three nearby, undisturbed control sites. We used permutational multivariate analysis of variance and generalised additive mixed models to investigate how bee abundance and species richness varied over time (years), between seasons and between restoration levels.
Landfill restoration and the creation of foraging and nesting habitat resulted in rapid and persistent occupation by bees, suggesting that efforts to restore bee communities can be successful when a source of colonists exists nearby.
Based on earlier studies, we predicted that in restored sites there would be an initial rapid increase in bee abundance and species richness, followed by a decline to a stable intermediate level. This prediction was supported as bee abundance and species richness in restored sites increased until 2006/2007 and subsequently declined.
In control sites, there were significant declines in abundance and species richness over time, despite a lack of anthropogenic disturbance. Possible contributors are changing weather patterns, especially severe droughts; plant community succession resulting in loss of bare ground for nesting sites; and increasing suburbanisation of the surrounding landscape.
Newly emerged adult holometabolous insects must still complete considerable morphological, metabolic, and neural maturation. Despite this, adults have frequently been documented to fly prior to ...finishing maturation and attaining peak physiological capacity. In some species, flight is limited by the unfurling of the wing, while in other species it may be limited by biochemical capacity. We charted maturation trajectories of adult bumblebee workers (Bombus impatiens) for both morphological and flight muscle metabolic capacities, and compared these to the first age at flight. Workers began regular flights as soon as two days after emergence. The unfurling of the wings was completed well before first flights and before any other studied factor, suggesting this did not initially limit flight. Wing beat frequencies, measured as a struggling response to grasping the hindlegs, were about 90% mature by two days old, and did not significantly change after three days. Conversely, by the initiation of flight, the mean enzyme maturation was only 63% completed relative to adult enzyme capacity, though specific enzyme profiles ranged from 42% to 73%. Maximum ADP-stimulated mitochondrial respiratory activity on pyruvate and proline matured along a similar time frame to glycolytic capacity, reaching its maximum three days after emergence. Bumblebees, as other adult insects, thus begin flights prior to fully maturing.
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