Simon Sponberg

• Professor (Assistant) at Georgia Institute of Technology

Flight control in insects is heavily dependent on vision. Thus, in dim light, the decreased reliability of visual signal detection also prompts consequences for insect flight. We have an emerging understanding of the neural mechanisms that different species employ to adapt the visual system to low light. However, much less explored are comparative...

Significance Animals rely on information drawn from a host of sensory systems to control their movement as they navigate in and interact with their environment. How the nervous system consolidates and processes these channels of information to govern locomotion is a challenging reverse engineering problem. To address this issue, we asked how a hawk...

Animals must operate under an enormous range of light intensities. Nocturnal and twilight flying insects are hypothesized to compensate for dim conditions by integrating light over longer times. This slowing of visual processing would increase light sensitivity but should also reduce movement response times. Using freely hovering moths tracking rob...

Muscles driving rhythmic locomotion typically show strong dependence of power on the timing or phase of activation. This is particularly true in insects' main flight muscles, canonical examples of muscles thought to have a dedicated power function. However, in the moth (Manduca sexta), these muscles normally activate at a phase where the instantane...

Convergent and divergent structures in the networks that make up biological brains are found across many species and brain regions at various spatial scales. Neurons in these networks fire action potentials, or “spikes,” whose precise timing is becoming increasingly appreciated as large sources of information about both sensory input and motor outp...

Crossbridge binding, state transitions, and force in active muscle is dependent on the radial spacing between the myosin-containing thick filament and the actin-containing thin filament in the filament lattice. This radial spacing has been previously shown through spatially explicit modeling and experimental efforts to greatly affect quasi-static,...

Flying insects are thought to achieve energy-efficient flapping flight by storing and releasing elastic energy in their muscles, tendons, and thorax. However, ‘spring-wing’ flight systems consisting of elastic elements coupled to nonlinear, unsteady aerodynamic forces present possible challenges to generating stable and responsive wing motion. The...

Across diverse organisms, the temporal dynamics of spiking responses between neurons, the neural synchrony, is crucial for encoding different stimuli. Neural synchrony is especially important in the insect antennal (olfactory) lobe (AL). Previous studies on synchronization, however, rely on pair-wise synchronization metrics including the cross-corr...

Convergent and divergent structures in the networks that make up biological brains are found universally across many species and brain regions at various scales. Neurons in these networks fire action potentials, or "spikes", whose precise timing is becoming increasingly appreciated as large sources of information about both sensory input and motor...

Insects show diverse flight kinematics and morphologies reflecting their evolutionary histories and ecological adaptations. Many silkmoths utilizing low wingbeat frequencies and large wings to fly display body oscillations: Their bodies pitch and bob periodically – synchronized with their wing flapping cycle. Similar oscillations in butterflies aug...

Synopsis The evolution of flight in an early winged insect ancestral lineage is recognized as a key adaptation explaining the unparalleled success and diversification of insects. Subsequent transitions and modifications to flight machinery, including secondary reductions and losses, also play a central role in shaping the impacts of insects on broa...

An insect’s wingbeat frequency is a critical determinant of its flight performance and varies by multiple orders of magnitude across Insecta. Despite potential energetic benefits for an insect that matches its wingbeat frequency to its resonant frequency, recent work has shown that moths may operate off their resonant peak. We hypothesized that acr...

Synopsis Dimensionless numbers have long been used in comparative biomechanics to quantify competing scaling relationships and connect morphology to animal performance. While common in aerodynamics, few relate the biomechanics of the organism to the forces produced on the environment during flight. We discuss the Weis-Fogh number, N, as a dimension...

Crossbridge binding and force in active muscle is dependent on the radial spacing between the thick and the thin filaments. This radial lattice spacing has been shown through spatially explicit modeling and experimental efforts to greatly affect isometric, force production in muscle. It has recently been suggested that this radial spacing might als...

Animals are much better at running than robots. The difference in performance arises in the important dimensions of agility, range, and robustness. To understand the underlying causes for this performance gap, we compare natural and artificial technologies in the five subsystems critical for running: power, frame, actuation, sensing, and control. W...

An insect’s wingbeat frequency is a critical determinant of its flight performance and varies by multiple orders of magnitude across Insecta. Despite potential energetic and kine-matic benefits for an insect that matches its wingbeat frequency to its resonant frequency, recent work has shown that moths may operate off of their resonant peak. We hyp...

Since taking flight, insects have undergone repeated evolutionary transitions between two seemingly distinct flight modes1–3. Some insects neurally activate their muscles synchronously with each wingstroke. However, many insects have achieved wingbeat frequencies beyond the speed limit of typical neuromuscular systems by evolving flight muscles tha...

Multisensory, goal-directed behaviors are ubiquitous and essential in animals across taxa. Individual sensory modalities may be significantly tuned by environmental context, and yet they must continue to combine and produce multisensory behaviors. This necessitates either behavioral robustness or goal-relevant adaptation in sensorimotor systems. In...

Flying insects solve a daunting control problem of generating a patterned and precise motor program to stay airborne and generate agile maneuvers. In this motor program consisting of every action potential controlling wing musculature, each muscle encodes significant information about movement in precise spike timing down to the millisecond scale....

Sensory inputs in nervous systems are often encoded at the millisecond scale in a precise spike timing code. There is now growing evidence in behaviors ranging from slow breathing to rapid flight for the prevalence of precise timing encoding in motor systems. Despite this, we largely do not know at what scale timing matters in these circuits due to...

Muscles act through elastic and dissipative elements to mediate movement, which can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by an insect's exoskeleton, which acts as a spring with frequency-independent material properties under purely sinusoida...

Blinking, the transient occlusion of the eye by one or more membranes, serves several functions including wetting, protecting, and cleaning the eye. This behavior is seen in nearly all living tetrapods and absent in other extant sarcopterygian lineages suggesting that it might have arisen during the water-to-land transition. Unfortunately, our unde...

Subject-to-subject variability is a common challenge in generalizing neural data models across subjects. While many methods exist that map one subject to another, it remains challenging to combine many subjects in a computationally efficient manner, especially with features that are highly non-linear such as when considering populations of spiking...

Muscle function during movement is more than a simple, linear transformation of neural activity into force. The classic work loop technique has pioneered our understanding of muscle, but typically only characterizes function during unperturbed movement cycles, such as those experienced during steady walking, running, swimming and flying. Yet pertur...

Muscles act through elastic and dissipative elements to mediate movement, but these elements can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by the insect's exoskeleton, which acts as a structurally damped spring under purely sinusoidal deformation...

Flying insects have elastic materials within their exoskeletons that could reduce the energetic cost of flight if their wingbeat frequency is matched to a mechanical resonance frequency. Flapping at resonance may be essential across flying insects because of the power demands of small-scale flapping flight. However, building up large-amplitude reso...

Across insects, wing shape and size have undergone dramatic divergence even in closely related sister groups. However, we do not know how morphology changes in tandem with kinematics to support body weight within available power and how the specific force production patterns are linked to differences in behaviour. Hawkmoths and wild silkmoths are d...

The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, w...

Sensory inputs in nervous systems are often encoded at the millisecond scale in a temporally precise code. There is now a growing appreciation for the prevalence of precise timing encoding in motor systems. Animals from moths to birds control motor outputs using precise spike timing, but we largely do not know at what scale timing matters in these...

Patterns of motor activity can be used to decode behavior state. Precise spike timing encoding is present in many motor systems, but is not frequently utilized to decode behavior or to examine how coordination is achieved across many motor units. Testing whether the same coordinated sets of muscles control different movements is difficult without a...

The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, w...

Insect wings serve two crucial functions in flight: propulsion and sensing. During flapping flight, complex spatiotemporal patterns of strain on the wing reflect mechanics, kinematics, and external perturbations; sensing wing deformation provides feedback necessary for flight control. Campaniform sensilla distributed across the wing transduce local...

Centimetre-scale fliers must contend with the high power requirements of flapping flight. Insects have elastic elements in their thoraxes which may reduce the inertial costs of their flapping wings. Matching wingbeat frequency to a mechanical resonance can be energetically favourable, but also poses control challenges. Many insects use frequency mo...

Flapping-wing insects, birds and robots are thought to offset the high power cost of oscillatory wing motion by using elastic elements for energy storage and return. Insects possess highly resilient elastic regions in their flight anatomy that may enable high dynamic efficiency. However, recent experiments highlight losses due to damping in the ins...

Wing integrity is crucial to the many insect species that spend distinct portions of their life in flight. How insects cope with the consequences of wing damage is therefore a central question when studying how robust flight performance is possible with such fragile chitinous wings. It has been shown in a variety of insect species that the loss in...

Flapping-wing insects, birds, and robots are thought to offset the high power cost of oscillatory wing motion by using elastic elements for energy storage and return. Insects possess highly resilient elastic regions in their flight anatomy that may enable high dynamic efficiency. However, recent experiments highlight losses due to damping in the in...

Centimeter-scale fliers that combine wings with springy elements must contend with the high power requirements and mechanical constraints of flapping wing flight. Insects utilize elastic energy exchange to reduce the inertial costs of flapping wing flight and potentially match wingbeat frequencies to a mechanical resonance. Flying at resonance may...

A wide diversity of wing shapes has evolved, but how is aerodynamic strategy coupled to morphological variation? Here we examine how wing shape has evolved across a phylogenetic split between hawkmoths (Sphingidae) and wild silkmoths (Saturniidae), which have divergent life histories, but agile flight behaviors. Combined with kinematics of exemplar...

The integrity of their wings is crucial to the many insect species that spend distinct portions of their life in flight. How insects cope with the consequences of wing damage is therefore a central question when studying how robust flight performance is possible with such fragile chitinous wings. It has been shown in a variety of insect species tha...

In many insects, wing movements are generated indirectly via exoskeletal deformations. Measurements of inertial and aerodynamic power suggest that elastic recovery of energy between wingstrokes might reduce power requirements of flight. We tested three questions. (1) Can the thorax itself provide significant energy return? (2) Does a simple damped...

Significance Brains can encode precise sensory stimuli, and specific motor systems also appear to be precise, but how important are millisecond changes in timing of neural spikes across the whole motor program for a behavior? We record nearly every spike that the hawk moth’s nervous system sends to its wing muscles. We show that all muscles convey...

Muscle mediates movement but movement is typically unsteady and perturbed. Muscle is known to behave non-linearly and with history dependent properties during steady locomotion, but the importance of history dependence in mediating muscles function during perturbations remains less clear. To explore muscle's capacity to mitigate perturbations durin...

The centralization of locomotor control from weak and local coupling to strong and global is hard to assess outside of particular modeling frameworks. We developed an empirical, model-free measure of centralization that compares information between control signals and both global and local states. A second measure, co-information, quantifies the ne...

In the vast majority of flying insects, wing movements are generated indirectly via the deformations of the exoskeleton. Indirect measurements of inertial and aerodynamic power requirements suggest that elastic energy exchange in spring-like structures may reduce the high power requirements of flight by recovering energy from one wingstroke to the...

Movement in biology is often achieved with distributed control of coupled subcomponents, e.g. muscles and limbs. Coupling could range from weak and local, i.e. decentralized, to strong and global, i.e. centralized. We developed a model-free measure of centralization that compares information shared between control signals and both global and local...

Sequences of action potentials, or spikes, carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. Acr...

Muscle mediates movement but movement is typically unsteady and perturbed. Muscle is known to behave non-linearly and with history dependent properties during steady locomotion, but the importance of history dependence in mediating muscles function during perturbations remains less clear. To explore muscle’s capacity to mitigate perturbations, we c...

Animals are remarkably stable during high-speed maneuvers. As the speed of locomotion increases, neural bandwidth and processing delays can limit the ability to achieve and maintain stable control. Processing the information of sensory stimuli into a control signal within the sensor itself could enable rapid implementation of whole-body feedback co...

What are the features of movement encoded by changing motor commands? Do motor commands encode movement independently or can they be represented in a reduced set of signals (i.e. synergies)? Motor encoding poses a computational and practical challenge because many muscles typically drive movement, and simultaneous electrophysiology recordings of al...

Control theory arose from a need to control synthetic systems. From regulating steam engines to tuning radios to devices capable of autonomous movement, it provided a formal mathematical basis for understanding the role of feedback in the stability (or change) of dynamical systems. It provides a framework for understanding any system with feedback...

A temperature gradient throughout the dominant flight muscle (dorsolongitudinal muscle, DLM(1)) of the hawkmoth Manduca sexta, together with temperature-dependent muscle contractile rates, demonstrates that significant spatial variation in power production is possible within a single muscle. Using in situ work-loop analyses under varying muscle tem...

Living cetaceans exhibit interspecific size ranging across several orders of magnitude, and rank among the largest vertebrates ever. Details of how cetaceans evolved different body sizes, however, remain obscure, because they lack basic morphological proxies that have been traditionally used in other fossil vertebrates. Here, we reconstruct the bod...

A neuromechanical approach to control requires understanding how mechanics alters the potential of neural feedback to control body dynamics. Here, we rewrite activation of individual motor units of a behaving animal to mimic the effects of neural feedback without concomitant changes in other muscles. We target a putative control muscle in the cockr...

Muscles are multi-functional structures that interface neural and mechanical systems. Muscle work depends on a large multi-dimensional space of stimulus (neural) and strain (mechanical) parameters. In our companion paper, we rewrote activation to individual muscles in intact, behaving cockroaches (Blaberus discoidalis L.), revealing a specific musc...

Geckos owe their remarkable stickiness to millions of dry, hard setae on their toes. In this study, we discovered that gecko setae stick more strongly the faster they slide, and do not wear out after 30,000 cycles. This is surprising because friction between dry, hard, macroscopic materials typically decreases at the onset of sliding, and as veloci...

A musculo-skeletal structure can stabilize rapid locomotion using neural and/or mechanical feedback. Neural feedback results in an altered feedforward activation pattern, whereas mechanical feedback using visco-elastic structures does not require a change in the neural motor code. We selected musculo-skeletal structures in the cockroach (Blaberus d...

The interplay between robotics and neuromechanics facilitates discoveries in both fields: nature provides roboticists with design ideas, while robotics research elucidates critical fea-tures that confer performance advantages to biological systems. Here, we explore a system particularly well suited to exploit the synergies between biology and robot...

Research into the neuromechanical basis of behavior, either in biomechanics, neuroethology, or neuroscience, is frequently limited by methods of data collection. Two of the most pressing needs are for methods with which to (1) record from multiple neurons or muscles simultaneously and (2) perform this recording in intact, behaving animals. In this...

Geckos have evolved one of the most versatile and effective adhesives known. The mechanism of dry adhesion in the millions of setae on the toes of geckos has been the focus of scientific study for over a century. We provide the first direct experimental evidence for dry adhesion of gecko setae by van der Waals forces, and reject the use of mechanis...

The tokay gecko (Gekko gecko) can adhere to nearly any surface through van der Waals interactions of the specialized setae (b-keratin "hairs") of its toe pads. Our recent research has suggested that a gecko is substantially overbuilt for static adhesion requiring as little as 0.03of its theoretical adhesive capacity. We performed the first sliding...