Dynamic dendritic compartmentalization underlies stimulus-specific adaptation in an insect neuron.

In many neural systems, repeated stimulation leads to stimulus-specific adaptation (SSA), with responses to repeated signals being reduced while responses to novel stimuli remain unaffected. The underlying mechanisms of SSA remain mostly hypothetical. One hypothesis is that dendritic processes generate SSA. Evidence for such a mechanism was recently described in an insect auditory interneuron (TN-1 in Neoconocephalus triops). Afferents, tuned to different frequencies, connect with different parts of the TN-1 dendrite. The specific adaptation of these inputs relies on calcium and sodium accumulation within the dendrite, with calcium having a transient and sodium a tonic effect. Using imaging techniques, we tested here whether the accumulation of these ions remained limited to the stimulated parts of the dendrite. Stimulation with a fast pulse rate, which results in strong adaptation, elicited a transient dendritic calcium signal. In contrast, the sodium signal was tonic, remaining high during the fast pulse rate stimulus. These time courses followed the predictions from the previous pharmacological experiments. The peak positions of the calcium and sodium signals differed with the carrier frequency of the stimulus; at 15 kHz, peak locations were significantly more rostral than at 40 kHz. This matched the predictions made from neuroanatomical data. Our findings confirm that excitatory postsynaptic potentials rather than spiking cause the increase of dendritic calcium and sodium concentrations and that these increases remain limited to the stimulated parts of the dendrite. This supports the hypothesis of "dynamic dendritic compartmentalization" underlying SSA in this auditory interneuron.

Mechanical properties of the cuticles of three cockroach species that differ in their wind-evoked escape behavior.

The structural and material properties of insect cuticle remain largely unexplored, even though they comprise the majority (approximately 80%) of animals. Insect cuticle serves many functions, including protection against predatory attacks, which is especially beneficial to species failing to employ effective running escape responses. Despite recent advances in our understanding of insect escape behaviors and the biomechanics of insect cuticle, there are limited studies on the protective qualities of cuticle to extreme mechanical stresses and strains imposed by predatory attacks, and how these qualities vary between species employing different escape responses. Blattarians (cockroaches) provide an appropriate model system for such studies. Wind-evoked running escape responses are strong in Periplaneta americana, weak in Blaberus craniifer and absent in Gromphodorhina portentosa, putting the latter two species at greater risk of being struck by a predator. We hypothesized that the exoskeletons in these two larger species could provide more protection from predatory strikes relative to the exoskeleton of P. americana. We quantified the protective qualities of the exoskeletons by measuring the puncture resistance, tensile strength, strain energy storage, and peak strain in fresh samples of thoracic and abdominal cuticles from these three species. We found a continuum in puncture resistance, tensile strength, and strain energy storage between the three species, which were greatest in G. portentosa, moderate in B. craniifer, and smallest in P. americana. Histological measurements of total cuticle thickness followed this same pattern. However, peak strain followed a different trend between species. The comparisons in the material properties drawn between the cuticles of G. portentosa, B. craniifer, and P. americana demonstrate parallels between cuticular biomechanics and predator running escape responses.

Neural responses from the filiform receptor neuron afferents of the wind-sensitive cercal system in three cockroach species.

The wind-sensitive insect cercal system is involved in many important behaviors, such as initiating terrestrial escape responses and providing sensory feedback during flight. The occurrence of these behaviors vary in cockroach species Periplaneta americana (strong terrestrial response and flight), Blaberus craniifer (weak terrestrial response and flight), and Gromphodorhina portentosa (no terrestrial response and no flight). A previous study focusing on wind-sensitive interneuron (WSI) responses demonstrated that variations in sensory processing of wind information accompany these behavioral differences. In this study, we recorded extracellularly from the cercal nerve to characterize filiform afferent population responses to different wind velocities to investigate how sensory processing differs across these species at the initial encoding of wind. We compared these results and responses from the WSI population to examine information transfer at the first synapse. Our main results were: (1) G. portentosa had the weakest responses of the three species over the stimulus duration and possessed the smallest cerci with the least filiform hair receptors of the three species; (2) B. craniifer filiform responses were similar to or greater than P. americana responses even though B. craniifer possessed smaller cerci with less filiform hair receptors than P. americana; (3) the greater filiform afferent responses in B. craniifer, including a larger amplitude second positive peak compared to the other two species, suggest more synchronous activity between filiform afferents in this species; (4) the transfer of information at the first synapse appears to be similar in both P. americana and G. portentosa, but different in B. craniifer.

Neural responses from the wind-sensitive interneuron population in four cockroach species.

The wind-sensitive insect cercal sensory system is involved in important behaviors including predator detection and initiating terrestrial escape responses as well as flight maintenance. However, not all insects possessing a cercal system exhibit these behaviors. In cockroaches, wind evokes strong terrestrial escape responses in Periplaneta americana and Blattella germanica, but only weak escape responses in Blaberus craniifer and no escape responses in Gromphadorhina portentosa. Both P. americana and B. craniifer possesses pink flight muscles correlated with flight ability while B. germanica possesses white flight muscles that cannot support flight and G. portentosa lacks wings. These different behavioral combinations could correlate with differences in sensory processing of wind information by the cercal system. In this study, we focused on the wind-sensitive interneurons (WSIs) since they provide input to the premotor/motor neurons that influence terrestrial escape and flight behavior. Using extracellular recordings, we characterized the responses from the WSI population by generating stimulus-response (S-R) curves and examining spike firing rates. Using cluster analysis, we also examined the activity of individual units (four per species, though not necessarily homologous) comprising the population response in each species. Our main results were: (1) all four species possessed ascending WSIs in the abdominal connectives; (2) wind elicited the weakest WSI responses (lowest spike counts and spike rates) in G. portentosa; (3) wind elicited WSI responses in B. craniifer that were greater than P. americana or B. germanica; (4) the activity of four individual units comprising the WSI population response in each species was similar across species.

Dendritic mechanisms contribute to stimulus-specific adaptation in an insect neuron.

Reduced neuronal activation to repetitive stimulation is a common feature of information processing in nervous systems. Such stimulus-specific adaptation (SSA) occurs in many systems, but the underlying neural mechanisms are not well understood. The Neoconocephalus (Orthoptera, Tettigoniidae) TN-1 auditory neuron exhibits an SSA-like process, characterized by reliably detecting deviant pulses after response cessation to common standard pulses. Therefore, TN-1 provides a model system to study the cellular mechanisms underlying SSA with an identified neuron. Here we test the hypothesis that dendritic mechanisms underlie TN-1 response cessation to fast-pulse rate repeated signals. Electrically stimulating TN-1 with either high-rate or continuous-current pulses resulted in a decreased ability in TN-1 to generate action potentials but failed to elicit cessation of spiking activity as observed with acoustic stimulation. BAPTA injection into TN-1 delayed the onset of response cessation to fast-pulse rate acoustic stimuli in TN-1 but did not eliminate it. These results indicate that calcium-mediated processes contribute to the fast cessation of spiking activity in TN-1 but are insufficient to cause spike cessation on its own. Replacing normal saline with low-Na(+) saline (replacing sodium chloride with either lithium chloride or choline chloride) eliminated response cessation, and TN-1 no longer responded selectively to the deviant pulses. Sodium-mediated potassium channels are the most likely candidates underlying sodium-mediated response suppression in TN-1, triggered by Na(+) influx in dendritic regions activated by acoustic stimuli. On the basis of these results, we present a model for a cellular mechanism for SSA in a single auditory neuron.

Auditory change detection by a single neuron in an insect.

The detection of novel signals in the auditory scene is an elementary task of any hearing system. In Neoconocephalus katydids, a primary auditory interneuron (TN-1) with broad spectral sensitivity, responded preferentially to rare deviant pulses (7 pulses/s repetition rate) embedded among common standard pulses (140 pulses/s repetition rate). Eliminating inhibitory input did not affect the detection of the deviant pulses. Detection thresholds for deviant pulses increased significantly with increasing amplitude of standard pulses. Responses to deviant pulses occurred when the carrier frequencies of deviant and standard were sufficiently different, both when the deviant had a higher or lower carrier frequency than the standard. Recordings from receptor neurons revealed that TN-1 responses to the deviant pulses did not depend on the population response strength of the receptors, but on the distribution of the receptor cell activity. TN-1 responses to the deviant pulse occurred only when the standard and deviant pulses were transmitted by different groups of receptor cells. TN-1 responses parallel stimulus specific adaptation (SSA) described in mammalian auditory system. The results support the hypothesis that the mechanisms underlying SSA and change-detection are located in the TN-1 dendrite, rather than the receptor cells.

Behavioral responses of big brown bats to dives by praying mantises.

Insectivorous echolocating bats face a formidable array of defenses employed by their airborne prey. One such insect defense is the ultrasound-triggered dive, which is a sudden, rapid drop in altitude, sometimes all the way to the ground. Although many previous studies have investigated the dynamics of such dives and their effect on insect survival rate, there has been little work on how bats may adapt to such an insect defense employed in the middle of pursuit. In this study we investigated how big brown bats (Eptesicus fuscus) adjust their pursuit strategy when flying praying mantises (Parasphendale agrionina) execute evasive, ultrasound-triggered dives. Although the mantis dive occasionally forced the bat to completely abort its chase (25% trials), in a number of cases (75% trials) the bat followed the mantis into the dive. In such cases the bat kept its sonar beam locked onto the target and maneuvered to maintain the same time efficient strategy it adopted during level flight pursuit, though it was ultimately defeated by the dive. This study suggests that although the mantis dive can be effective in evading the bat, it does not always deter the bat from continuing pursuit and, given enough altitude, the bat can potentially capture diving prey using the same flight strategy it employs to intercept prey in level flight.

Wind generated by an attacking bat: anemometric measurements and detection by the praying mantis cercal system.

The wind-sensitive cercal system, well-known for mediating terrestrial escape responses, may also mediate insect aerial bat-avoidance responses triggered by wind generated by the approaching bat. One crucial question is whether enough time exists between detection and capture for the insect to perform a successful evasive maneuver. A previous study estimated this time to be 16 ms, based on cockroach behavioral latencies and a prediction for the detection time derived from a simulated predator moving toward a simulated prey. However, the detection time may be underestimated since both the simulated predator and prey lacked certain characteristics present in the natural situation. In the present study, actual detection times are measured by recording from wind-sensitive interneurons of a tethered praying mantis that serves as the target for a flying, attacking bat. Furthermore, using hot-wire anemometry, we describe and quantify the wind generated by an attacking bat. Anemometer measurements revealed that the velocity of the bat-generated wind consistently peaks early with a high acceleration component (an important parameter for triggering wind-mediated terrestrial responses). The physiological recordings determined that the mantis cercal system detected an approaching bat 74 ms before contact, which would provide the insect with 36 ms to perform a maneuver before capture. This should be sufficient time for the mantis to respond. Although it probably would not have time for a full response that completely evades the bat, even a partial response might alter the mantid's trajectory enough to cause the bat to mishandle the insect, allowing it to escape.

Timing of praying mantis evasive responses during simulated bat attack sequences.

Praying mantids perform evasive maneuvers that vary with the level of danger posed by their bat predators. The vocalization pattern of attacking bats provides cues that mantids can potentially use to decide how and when to respond. Using pulse trains simulating bat attack echolocation sequences, this study determines when in the attack sequence the mantis power dive (its response to high-level threat) occurs and predicts the parameters within the echolocation sequence that are important for eliciting the response. For sequences with a rapid transition from low to high pulse repetition rates (PRRs), the evasive response occurred close to the point during the simulated sequence when the bat would have contacted the mantis. However, the evasive response occurred earlier if the transition was gradual. Regardless of the transition type, the prediction data show that sequences trigger the response when PRRs reach 20-40 pulses s(-1). These results suggest that a bat gradually increasing its PRR could 'tip off' the mantis, enabling it to escape. Attack sequences contain gradual transitions when bats engage in strobing behavior, an echolocation phenomenon that may help the bat perceive the auditory scene. Conversely, bat attack sequences that contain rapid increases in PRR close to the point of capture could circumvent the mantid's auditory defense. Based on these findings, mantids as well as other insects could benefit from having a back-up defense response to offset any advantage the bat gains by rapidly switching from low to high PRRs.

Implanted electrode recordings from a praying mantis auditory interneuron during flying bat attacks.

Using an implanted electrode, we recorded the responses from the ultrasound-sensitive mantis interneuron 501-T3 during flying bat attacks in a large flight room where the mantis served as the target. 501-T3 responds to each vocalization emitted with multi-spike bursts when pulse repetition rates (PRRs) are below 55 pulses x s(-1). As PRR increases and pulse durations fall below 3 ms, 501-T3 ceases burst activity. On average, spike bursts cease 272 ms before contact (when the bat is 73 cm away from the preparation). The timing of cessation of activity in 501-T3 is similar to the latency for the diving portion of the response of the mantid (242 ms). Experiments using vocalizing stationary bats confirm that 501-T3 responds more reliably to longer pulse durations (> or =3 ms) when intensities are below 90 dB pe SPL. The cessation of 501-T3 activity is probably due both to the increasing PRR and to the decreasing pulse duration that occur in the terminal buzz phase of a bat attack. 501-T3 may be actively shut off at high PRRs and/or intensities to protect the interneuron from habituation while the mantis performs an escape response. The cessation of 501-T3 activity is consistent with the lack of a very late ultrasound-mediated evasive response by the mantis. However, cessation of 501-T3 activity may allow a true 'last-chance' response to be mediated by other neural systems.