Muscle receptor organs do not mediate load compensation during body roll and defense response extensions in the crayfish Cherax destructor.

It has been proposed that the abdominal muscle receptor organ (MRO) of decapod crustaceans acts in a sensory feedback loop to compensate for external load. There is not yet unequivocal evidence of MRO activity during slow abdominal extension in intact animals, however. This raises the possibility that MRO involvement in load compensation is context-dependent. We recorded from MRO tonic stretch receptors (SRs) in freely behaving crayfish (Cherax destructor) during abdominal extension occurring during two different behaviors: body roll and the defense response. Abdominal extensions are similar in many respects in both behaviors, although defense response extensions are more rapid. In both situations, SR activity typically ceased when the abdominal extension commenced, even if the joint of the SR being monitored was mechanically prevented from extending by a block. Since extensor motor neuron activity increased when the abdomen was prevented from extending, we concluded that the load compensation occurring in these behaviors was not mediated by the MROs.

Mechanisms of frequency-specific responses of omega neuron 1 in crickets (Teleogryllus oceanicus): a polysynaptic pathway for song?

In crickets (Teleogryllus oceanicus), the auditory interneuron omega neuron 1 (ON1) responds to sounds over a wide range of frequencies but is most sensitive to the frequency of conspecific songs (4.5 kHz). Response latency is longest for this same frequency. We investigate the mechanisms that might account for the longer latency of ON1 to cricket-like sounds. Intracellular recordings revealed no evidence for appropriately timed postsynaptic inhibition of ON1 that might increase its latency, nor was latency affected by picrotoxin. The onset of excitatory postsynaptic potentials (EPSPs) was delayed for 4.5 kHz stimuli compared with ultrasound stimuli, pointing to a presynaptic locus for the latency difference. When ON1 is stimulated with high frequencies, discrete, apparently unitary EPSPs can be recorded in its dendrite, and these are latency-locked to spikes recorded simultaneously in the auditory nerve. This suggests that input to ON1 from high-frequency-tuned auditory receptor neurons is monosynaptic. In agreement with this, brief ultrasound stimuli evoke a single, short-latency EPSP in ON1. In contrast, the EPSP evoked by a brief 4.5 kHz stimulus consists of an early component, similar in latency to that evoked by ultrasound and possibly evoked by ultrasound-tuned receptors, and a later, dominant component. We interpret the early peak as arising from a monosynaptic afferent pathway and the late peak from a polysynaptic afferent pathway. Multiple-peak EPSPs, with timing similar to those evoked by sound stimuli, were also evoked by electrical stimulation of the auditory nerve.

Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus).

In crickets (Teleogryllus oceanicus), the paired auditory interneuron Omega Neuron 1 (ON1) responds to sounds with frequencies in the range from 3 to 40 kHz. The neuron is tuned to frequencies similar to that of conspecific songs (4.5 kHz), but its latency is longest for these same frequencies by a margin of 5-10 ms. Each ON1 is strongly excited by input from the ipsilateral ear and inhibits contralateral auditory neurons that are excited by the contralateral ear, including the interneurons ascending neurons 1 and 2 (AN1 and AN2). We investigated the functional consequences of ON1's long latency to cricket-like sound and the resulting delay in inhibition of AN1 and AN2. Using dichotic stimuli, we controlled the timing of contralateral inhibition of the ANs relative to their excitation by ipsilateral stimuli. Advancing the stimulus to the ear driving ON1 relative to that driving the ANs "subtracted" ON1's additional latency to 4.5 kHz. This had little effect on the spike counts of AN1 and AN2. The response latencies of these neurons, however, increased markedly. This is because in the absence of a delay in ON1's response, inhibition arrived at AN1 and AN2 early enough to abolish the first spikes in their responses. This also increased the variability of AN1 latency. This suggests that one possible function of the delay in ON1's response may be to protect the precise timing of the onset of response in the contralateral AN1, thus preserving interaural difference in response latency as a reliable potential cue for sound localization. Hyperpolarizing ON1 removed all detectable contralateral inhibition of AN1 and AN2, suggesting that ON1 is the main, if not the only, source of contralateral inhibition.

Digging in sand crabs: coordination of joints in individual legs.

Sand crabs use their multi-jointed legs to dig into sand. Combined movement and electromyogram (EMG) analyses showed that the pattern of intra-leg coordination in the legs of two sand crabs of different families (Blepharipoda occidentalis and Emerita analoga) is similar in legs 2 and 3, but very different in leg 4. For example, the sequence of proximal joint movements in legs 2 and 3 is elevation, retraction, depression and protraction (similar to backward walking in most decapods), but the sequence of proximal joint movements in leg 4 is elevation, protraction, retraction and depression (similar to forward walking). The synergies are the same during leg movements in sea water and in sand, suggesting that the same motor programme is used in both situations. At the transition from sea water into sand, however, both the frequency and amplitude of the EMG potentials increase, and the phasing of the motor output to leg 2 (and presumably leg 3) changes from proportional (both power and return strokes co-vary with period) to return stroke constant (power strokes co-vary much more with period than do return strokes). The motor output to leg 4 remains intermediate between proportional and return stroke constant in sea water and in sand. On the basis of the segmental specialisation of the motor patterns for the legs, we hypothesize that sand crab digging may be an evolutionary mosaic of disparate ancestral locomotor behaviours.

A map of distal leg motor neurons in the thoracic ganglia of four decapod crustacean species.

We describe the numbers, central positions, and axonal exit routes of the distal leg motor neurons of four decapod species: squat lobsters (Munida quadrispina), spiny sand crabs (Blepharipoda occidentalis), mole sand crabs (Emerita analoga), and signal crayfish (Pacifastacus leniusculus). As predicted by previous physiological and anatomical identification of axons at the periphery in crayfish and lobsters, cobalt backfills reveal about seventeen cell bodies, which are found in four areas in the ganglion. By comparing their positions and neurite morphologies with the previously identified neurons, functional identifications could be assigned to most of them. The common inhibitor and stretcher inhibitor are located posterior-medial. An anterior-lateral cluster of about twelve somata includes the opener identical to stretcher excitor, one of two bender excitors (bender excitor alpha), four flexor excitors, and two excitors each to the extensor, reductor, and closer muscles. Three cell bodies are posterior-lateral. Of these, the opener inhibitor and the second bender excitor (bender excitor beta) are on about the same dorsoventral plane. The third posterior-lateral cell, the accessory flexor excitor, is noticeably more dorsal than the other two posterior-lateral cell bodies. The reductor muscle is innervated by at least three neurons: the putative common inhibitor and fast and slow excitors. None of the leg motor neurons project into the contralateral hemiganglion. The most variable feature across species is the nerve through which motor axons exit the ganglion: axons leave the ganglia via different routes in each of the four species examined. These differences in the axons' pathway, however, are insufficient to explain the differences in motor output and behaviour of these four species.

Digging in sand crabs (Decapoda, Anomura, Hippoidea): interleg coordination

Sand crabs (Decapoda, Anomura, Hippoidea) are highly specialised for digging into sand using their thoracic legs. Using video-recording and electromyography, we examined the digging leg movements of three species of sand crabs belonging to two families: Blepharipoda occidentalis (Albuneidae), Lepidopa californica (Albuneidae) and Emerita analoga (Hippidae). The digging patterns of all three species are similar. The ipsilateral legs 2 and 3 are tightly coupled and shovel sand forward from underneath the animal, whereas the movements of leg 4 are more variable, apparently stirring up sand and providing the purchase for rearward descent into the sand. The digging patterns of B. occidentalis and L. californica resemble each other more than either resembles that of E. analoga. In the albuneids, leg 4 cycles at the same frequency as legs 2 and 3, and both albuneid species switch gait from bilateral alternation to synchrony midway through digging. In E. analoga, right and left legs 2 and 3 always alternate. Legs 4 can cycle at about twice the frequency of legs 2 and 3, and they tend to move in bilateral synchrony during high-frequency leg movements (e.g. at the start of digging); their bilateral coupling becomes variable during low-frequency movements. Sand crab digging may have originated as a modified form of walking, but this behavioural innovation subsequently diverged in the sand crab superfamily.