The Role of Central Complex Neurons in Prey Detection and Tracking in the Freely Moving Praying Mantis (Tenodera sinensis).

Complex tasks like hunting moving prey in an unpredictable environment require high levels of motor and sensory integration. An animal needs to detect and track suitable prey objects, measure their distance and orientation relative to its own position, and finally produce the correct motor output to approach and capture the prey. In the insect brain, the central complex (CX) is one target area where integration is likely to take place. In this study, we performed extracellular multi-unit recordings on the CX of freely hunting praying mantises (Tenodera sinensis). Initially, we recorded the neural activity of freely moving mantises as they hunted live prey. The recordings showed activity in cells that either reflected the mantis's own movements or the actions of a prey individual, which the mantises focused on. In the latter case, the activity increased as the prey moved and decreased when it stopped. Interestingly, cells ignored the movement of the other prey than the one to which the mantis attended. To obtain quantitative data, we generated simulated prey targets presented on an LCD screen positioned below the clear floor of the arena. The simulated target oscillated back and forth at various angles and distances. We identified populations of cells whose activity patterns were strongly linked to the appearance, movement, and relative position of the virtual prey. We refer to these as sensory responses. We also found cells whose activity preceded orientation movement toward the prey. We call these motor responses. Some cells showed both sensory and motor properties. Stimulation through tetrodes in some of the preparations could also generate similar movements. These results suggest the crucial importance of the CX to prey-capture behavior in predatory insects like the praying mantis and, hence, further emphasize its role in behaviorally and ecologically relevant contexts.

Contrasting Electroencephalography-Derived Entropy and Neural Oscillations With Highly Skilled Meditators.

Meditation is an umbrella term for a number of mental training practices designed to improve the monitoring and regulation of attention and emotion. Some forms of meditation are now being used for clinical intervention. To accompany the increased clinical interest in meditation, research investigating the neural basis of these practices is needed. A central hypothesis of contemplative neuroscience is that meditative states, which are unique on a phenomenological level, differ on a neurophysiological level. To identify the electrophysiological correlates of meditation practice, the electrical brain activity of highly skilled meditators engaging in one of six meditation styles (shamatha, vipassana, zazen, dzogchen, tonglen, and visualization) was recorded. A mind-wandering task served as a control. Lempel-Ziv complexity showed differences in nonlinear brain dynamics (entropy) during meditation compared with mind wandering, suggesting that meditation, regardless of practice, affects neural complexity. In contrast, there were no differences in power spectra at six different frequency bands, likely due to the fact that participants engaged in different meditation practices. Finally, exploratory analyses suggest neurological differences among meditation practices. These findings highlight the importance of studying the electroencephalography (EEG) correlates of different meditative practices.

Predatory behavior changes with satiety or increased insulin levels in the praying mantis (Tenodera sinensis).

At any given moment, behavior is controlled by a combination of external stimuli and an animal's internal state. As physiological conditions change, vastly different behaviors might result from the same stimuli. For example, the motivation to hunt and hunting strategy are influenced by satiety. Here, we describe how sensory responsiveness and motor activity of a praying mantis (Tenodera sinensis) change as the insect feeds, leading to an altered hunting strategy. We further show that these changes can be induced by injection of insulin, which likely functions as a metabotropic indicator. Praying mantises directed their attention toward real and simulated prey less often as they fed and became sated. The range of distance and azimuth at which prey was detected decreased as did pursuit of prey, while opportunistic close-range attacks persisted. Together, these sensorimotor changes are indicative of a behavioral paradigm shift from 'pursuit' to 'ambush'. A similar effect was induced in starved praying mantises injected with 0.05 ml of 200 µg ml-1 bovine insulin. These experiments showed that insulin injection into the circulating hemolymph is sufficient to decrease prey orientation as well as in prey-directed locomotor behaviors (tracking and pursuit). The effects of prey consumption and insulin injection were similarly dose dependent. These results suggest that insulin is a signal of internal, physiological conditions that can modify responses to external stimuli. A change in hunting strategy thus results from coordinated effects of a neurohormone on a set of independent sensorimotor processes and the overall activity level of the animal.

Mantisbot is a robotic model of visually guided motion in the praying mantis.

Insects use highly distributed nervous systems to process exteroception from head sensors, compare that information with state-based goals, and direct posture or locomotion toward those goals. To study how descending commands from brain centers produce coordinated, goal-directed motion in distributed nervous systems, we have constructed a conductance-based neural system for our robot MantisBot, a 29 degree-of-freedom, 13.3:1 scale praying mantis robot. Using the literature on mantis prey tracking and insect locomotion, we designed a hierarchical, distributed neural controller that establishes the goal, coordinates different joints, and executes prey-tracking motion. In our controller, brain networks perceive the location of prey and predict its future location, store this location in memory, and formulate descending commands for ballistic saccades like those seen in the animal. The descending commands are simple, indicating only 1) whether the robot should walk or stand still, and 2) the intended direction of motion. Each joint's controller uses the descending commands differently to alter sensory-motor interactions, changing the sensory pathways that coordinate the joints' central pattern generators into one cohesive motion. Experiments with one leg of MantisBot show that visual input produces simple descending commands that alter walking kinematics, change the walking direction in a predictable manner, enact reflex reversals when necessary, and can control both static posture and locomotion with the same network.

Spatial Navigation and the Central Complex: Sensory Acquisition, Orientation, and Motor Control.

Cockroaches are scavengers that forage through dark, maze-like environments. Like other foraging animals, for instance rats, they must continually asses their situation to keep track of targets and negotiate barriers. While navigating a complex environment, all animals need to integrate sensory information in order to produce appropriate motor commands. The integrated sensory cues can be used to provide the animal with an environmental and contextual reference frame for the behavior. To successfully reach a goal location, navigational cues continuously derived from sensory inputs have to be utilized in the spatial guidance of motor commands. The sensory processes, contextual and spatial mechanisms, and motor outputs contributing to navigation have been heavily studied in rats. In contrast, many insect studies focused on the sensory and/or motor components of navigation, and our knowledge of the abstract representation of environmental context and spatial information in the insect brain is relatively limited. Recent reports from several laboratories have explored the role of the central complex (CX), a sensorimotor region of the insect brain, in navigational processes by recording the activity of CX neurons in freely-moving insects and in more constrained, experimenter-controlled situations. The results of these studies indicate that the CX participates in processing the temporal and spatial components of sensory cues, and utilizes these cues in creating an internal representation of orientation and context, while also directing motor control. Although these studies led to a better understanding of the CX's role in insect navigation, there are still major voids in the literature regarding the underlying mechanisms and brain regions involved in spatial navigation. The main goal of this review is to place the above listed findings in the wider context of animal navigation by providing an overview of the neural mechanisms of navigation in rats and summarizing and comparing our current knowledge on the CX's role in insect navigation to these processes. By doing so, we aimed to highlight some of the missing puzzle pieces in insect navigation and provide a different perspective for future directions.

Comparison of biological chromophores: photophysical properties of cyanophenylalanine derivatives.

Within this work, the family of cyanophenylalanine spectroscopic reporters is extended by showing the ortho and meta derivatives have intrinsic photophysical properties that are useful for studies of protein structure and dynamics. The molar absorptivities of 2-cyanophenylalanine and 3-cyanophenylalanine are shown to be comparable to that of 4-cyanophenylalanine with similar spectral features in their absorbance and emission profiles, demonstrating that these probes can be utilized interchangeably. The fluorescence quantum yields are also on the same scale as commonly used fluorophores in peptides and proteins, tyrosine and tryptophan. These new cyano-fluorophores can be paired with either 4-cyanophenylalanine or tryptophan to capture distances in peptide structure through Förster resonance energy transfer. Additionally, the spectroscopic properties of these chromophores can report the local solvent environment via changes in fluorescence emission intensity as a result of hydrogen bonding and/or hydration. A decrease in the quantum yield is also observed in basic environments due to photoinduced electron transfer from a deprotonated amine in the free PheCN species and at the N-terminus of a short peptide, providing an avenue to detect pH in biological systems. Our results show the potential of these probes, 2-cyanophenylalanine and 3-cyanophenylalanine, to be incorporated into a single peptide chain, either individually or in tandem with 4-cyanophenylalanine, tryptophan, or tyrosine, in order to obtain information about peptide structure and dynamics.

Neuromechanical model of praying mantis explores the role of descending commands in pre-strike pivots.

Praying mantises hunt by standing on their meso- and metathoracic legs and using them to rotate and translate (together, 'pivot') their bodies toward prey. We have developed a neuromechanical software model of the praying mantis Tenodera sinensis to use as a platform for testing postural controllers that the animal may use while hunting. Previous results showed that a feedforward model was insufficient for capturing the diversity of posture observed in the animal (Szczecinski et al 2014 Biomimetic and Biohybrid Syst. 3 296-307). Therefore we have expanded upon this model to make a flexible controller with feedback that more closely mimics the animal. The controller actuates 24 joints in the legs of a dynamical model to orient the head and translate the thorax toward prey. It is controlled by a simulation of nonspiking neurons assembled as a highly simplified version of networks that may exist in the mantid central complex and thoracic ganglia. Because of the distributed nature of these networks, we hypothesize that descending commands that orient the mantis toward prey may be simple direction-of-intent signals, which are turned into motor commands by the structure of low-level networks in the thoracic ganglia. We verify this through a series of experiments with the model. It captures the speed and range of mantid pivots as reported in other work (Yamawaki et al 2011 J. Insect Physiol. 57 1010-6). It is capable of pivoting toward prey from a variety of initial postures, as seen in the animal. Finally, we compare the model's joint kinematics during pivots to preliminary 3D kinematics collected from Tenodera.

Central-complex control of movement in the freely walking cockroach.

To navigate in the world, an animal's brain must produce commands to move, change direction, and negotiate obstacles. In the insect brain, the central complex integrates multiple forms of sensory information and guides locomotion during behaviors such as foraging, climbing over barriers, and navigating to memorized locations. These roles suggest that the central complex influences motor commands, directing the appropriate movement within the current context. Such commands are ultimately carried out by the limbs and must therefore interact with pattern generators and reflex circuits that coordinate them. Recent studies have described how neurons of the central complex encode sensory information: neurons subdivide the space around the animal, encoding the direction or orientation of stimuli used in navigation. Does a similar central-complex code directing movement exist, and if so, how does it effect changes in the control of limbs? Recording from central-complex neurons in freely walking cockroaches (Blaberus discoidalis), we identified classes of movement-predictive cells selective for slow or fast forward walking, left or right turns, or combinations of forward and turning speeds. Stimulation through recording wires produced consistent trajectories of forward walking or turning in these animals, and those that elicited turns also altered an inter-joint reflex to a pattern resembling spontaneous turning. When an animal transitioned to climbing over an obstacle, the encoding of movement in this new context changed for a subset of cells. These results indicate that encoding of movement in the central complex participates in motor control by a distributed, flexible code targeting limb reflex circuits.

Extracellular wire tetrode recording in brain of freely walking insects.

Increasing interest in the role of brain activity in insect motor control requires that we be able to monitor neural activity while insects perform natural behavior. We previously developed a technique for implanting tetrode wires into the central complex of cockroach brains that allowed us to record activity from multiple neurons simultaneously while a tethered cockroach turned or altered walking speed. While a major advance, tethered preparations provide access to limited behaviors and often lack feedback processes that occur in freely moving animals. We now present a modified version of that technique that allows us to record from the central complex of freely moving cockroaches as they walk in an arena and deal with barriers by turning, climbing or tunneling. Coupled with high speed video and cluster cutting, we can now relate brain activity to various parameters of the movement of freely behaving insects.

Synchronous firing of antennal-lobe projection neurons encodes the behaviorally effective ratio of sex-pheromone components in male Manduca sexta.

Olfactory stimuli that are essential to an animal's survival and reproduction are often complex mixtures of volatile organic compounds in characteristic proportions. Here, we investigated how these proportions are encoded in the primary olfactory processing center, the antennal lobe, of male Manduca sexta moths. Two key components of the female's sex pheromone, present in an approximately 2:1 ratio, are processed in each of two neighboring glomeruli in the macroglomerular complex (MGC) of males of this species. In wind-tunnel flight experiments, males exhibited behavioral selectivity for ratios approximating the ratio released by conspecific females. The ratio between components was poorly represented, however, in the firing-rate output of uniglomerular MGC projection neurons (PNs). PN firing rate was mostly insensitive to the ratio between components, and individual PNs did not exhibit a preference for a particular ratio. Recording simultaneously from pairs of PNs in the same glomerulus, we found that the natural ratio between components elicited the most synchronous spikes, and altering the proportion of either component decreased the proportion of synchronous spikes. The degree of synchronous firing between PNs in the same glomerulus thus selectively encodes the natural ratio that most effectively evokes the natural behavioral response to pheromone.

Photofragmentation dynamics of ICN(-)(CO2)n clusters following visible excitation.

Photodissociation of ICN(-)(CO2)n, n = 0-18, with 500-nm excitation is investigated using a dual time-of-flight mass spectrometer. Photoabsorption to the (2)Π(1/2) state is detected using ionic-photoproduct action spectroscopy; the maximum absorption occurs around 490 nm. Ionic-photoproduct distributions were determined for ICN(-)(CO2)n at 500 nm. Following photodissociation of bare ICN(-) via 430-650 nm excitation, a small fraction of CN(-) is produced, suggesting that nonadiabatic effects play a role in the photodissociation of this simple anion. Electronic structure calculations, carried out at the MR-SO-CISD level of theory, were used to evaluate the potential-energy surfaces for the ground and excited states of ICN(-). Analysis of the electronic structure supports the presence of nonadiabatic effects in the photodissociation dynamics. For n ≥ 2, the major ionic photoproduct has a mass corresponding to either partially solvated CN(-) or partially solvated [NCCO2](-).

Olfactory modulation by dopamine in the context of aversive learning.

The need to detect and process sensory cues varies in different behavioral contexts. Plasticity in sensory coding can be achieved by the context-specific release of neuromodulators in restricted brain areas. The context of aversion triggers the release of dopamine in the insect brain, yet the effects of dopamine on sensory coding are unknown. In this study, we characterize the morphology of dopaminergic neurons that innervate each of the antennal lobes (ALs; the first synaptic neuropils of the olfactory system) of the moth Manduca sexta and demonstrate with electrophysiology that dopamine enhances odor-evoked responses of the majority of AL neurons while reducing the responses of a small minority. Because dopamine release in higher brain areas mediates aversive learning we developed a naturalistic, ecologically inspired aversive learning paradigm in which an innately appetitive host plant floral odor is paired with a mimic of the aversive nectar of herbivorized host plants. This pairing resulted in a decrease in feeding behavior that was blocked when dopamine receptor antagonists were injected directly into the ALs. These results suggest that a transient dopaminergic enhancement of sensory output from the AL contributes to the formation of aversive memories. We propose a model of olfactory modulation in which specific contexts trigger the release of different neuromodulators in the AL to increase olfactory output to downstream areas of processing.

Dynamic mapping of CN rotation following photoexcitation of ICN-.

In a spin: the dynamics of photoexcited ICN(-) (Ar)(0-5) are presented. Photodetachment produces quasi-thermal electron emission that leaves ICN with up to 2.85 eV of internal energy. Photodissociation at 2.5 eV leads to one-atom caging and highly solvated anion products. Calculations indicate efficient energy transfer into CN rotation upon excitation to the (2)Π(1/2) excited state. CN rotation is vital to explain the unique dynamics observed.

The neurobiology of insect olfaction: sensory processing in a comparative context.

The simplicity and accessibility of the olfactory systems of insects underlie a body of research essential to understanding not only olfactory function but also general principles of sensory processing. As insect olfactory neurobiology takes advantage of a variety of species separated by millions of years of evolution, the field naturally has yielded some conflicting results. Far from impeding progress, the varieties of insect olfactory systems reflect the various natural histories, adaptations to specific environments, and the roles olfaction plays in the life of the species studied. We review current findings in insect olfactory neurobiology, with special attention to differences among species. We begin by describing the olfactory environments and olfactory-based behaviors of insects, as these form the context in which neurobiological findings are interpreted. Next, we review recent work describing changes in olfactory systems as adaptations to new environments or behaviors promoting speciation. We proceed to discuss variations on the basic anatomy of the antennal (olfactory) lobe of the brain and higher-order olfactory centers. Finally, we describe features of olfactory information processing including gain control, transformation between input and output by operations such as broadening and sharpening of tuning curves, the role of spiking synchrony in the antennal lobe, and the encoding of temporal features of encounters with an odor plume. In each section, we draw connections between particular features of the olfactory neurobiology of a species and the animal's life history. We propose that this perspective is beneficial for insect olfactory neurobiology in particular and sensory neurobiology in general.

Innate recognition of pheromone and food odors in moths: a common mechanism in the antennal lobe?

The survival of an animal often depends on an innate response to a particular sensory stimulus. For an adult male moth, two categories of odors are innately attractive: pheromone released by conspecific females, and the floral scents of certain, often co-evolved, plants. These odors consist of multiple volatiles in characteristic mixtures. Here, we review evidence that both categories of odors are processed as sensory objects, and we suggest a mechanism in the primary olfactory center, the antennal lobe (AL), that encodes the configuration of these mixtures and may underlie recognition of innately attractive odors. In the pheromone system, mixtures of two or three volatiles elicit upwind flight. Peripheral changes are associated with behavioral changes in speciation, and suggest the existence of a pattern recognition mechanism for pheromone mixtures in the AL. Moths are similarly innately attracted to certain floral scents. Though floral scents consist of multiple volatiles that activate a broad array of receptor neurons, only a smaller subset, numerically comparable to pheromone mixtures, is necessary and sufficient to elicit behavior. Both pheromone and floral scent mixtures that produce attraction to the odor source elicit synchronous action potentials in particular populations of output (projection) neurons (PNs) in the AL. We propose a model in which the synchronous output of a population of PNs encodes the configuration of an innately attractive mixture, and thus comprises an innate mechanism for releasing odor-tracking behavior. The particular example of olfaction in moths may inform the general question of how sensory objects trigger innate responses.

A combined experimental/theoretical investigation of the near-infrared photodissociation of IBr- (CO2)n.

We report the collaborative experimental and theoretical study of the time-resolved recombination dynamics of photodissociated IBr(-)(CO(2))(n) clusters. Excitation of the bare anionic chromophore to the dissociative A(') (2)Pi(1/2) state yields only I(-) and Br products. Interestingly, however, the addition of a few solvent molecules promotes recombination of the dissociating chromophore on the X (2)Sigma(1/2)(+) ground state, which correlates asymptotically with Br(-) and I products. This process is studied experimentally using time-resolved, pump-probe techniques and theoretically via nonadiabatic molecular dynamics simulations. In sharp contrast to previous I(2)(-) studies where more kinetic energy was released to the photofragments, the observed recombination times increase from picoseconds to nanoseconds with increasing cluster size up to n=10. The recombination times then drop dramatically back to picoseconds for cluster sizes n=11-14. This trend, seen both in experiment and theory, is explained by the presence of a solvent-induced well on the A(') state, the depth of which directly corresponds to the asymmetry of the solvation about the chromophore. The results seen for both the branching ratios and recombination times from experiment and theory show good qualitative agreement.

Time-resolved study of solvent-induced recombination in photodissociated IBr-(CO2)n clusters.

We report the time-resolved recombination of photodissociated IBr-(CO2)n (n = 5-10) clusters following excitation to the dissociative IBr-A' 2Pi12 state of the chromophore via a 180 fs, 795 nm laser pulse. Dissociation from the A' state of the bare anion results in I- and Br products. Upon solvation with CO2, the IBr- chromophore regains near-IR absorption only after recombination and vibrational relaxation on the ground electronic state. The recombination time was determined by using a delayed femtosecond probe laser, at the same wavelength as the pump, and detecting ionic photoproducts of the recombined IBr- cluster ions. In sharp contrast to previous studies involving solvated I2-, the observed recombination times for IBr-(CO2)n increase dramatically with increasing cluster size, from 12 ps for n = 5 to 900 ps for n = 8,10. The nanosecond recombination times are especially surprising in that the overall recombination probability for these cluster ions is unity. Over the range of 5-10 solvent molecules, calculations show that the solvent is very asymmetrically distributed, localized around the Br end of the IBr- chromophore. It is proposed that this asymmetric solvation delays the recombination of the dissociating IBr-, in part through a solvent-induced well in the A' state that (for n = 8,10) traps the evolving complex. Extensive electronic structure calculations and nonadiabatic molecular dynamics simulations provide a framework to understand this unexpected behavior.