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Peter J Simmons

Publications and source records attributed to Peter J Simmons.

8 recordsLinked to original sources

Role of an identified looming-sensitive neuron in triggering a flying locust's escape.

Flying locusts perform a characteristic gliding dive in response to predator-sized stimuli looming from one side. These visual looming stimuli trigger trains of spikes in the descending contralateral movement detector (DCMD) neuron that increase in frequency as the stimulus gets nearer. Here we provide evidence that high-frequency (>150 Hz) DCMD spikes are involved in triggering the glide: the DCMD is the only excitatory input to a key gliding motor neuron during a loom; DCMD-mediated EPSPs only summate significantly in this motor neuron when they occur at >150 Hz; when a looming stimulus ceases approach prematurely, high-frequency DCMD spikes are removed from its response and the occurrence of gliding is reduced; and an axon important for glide triggering descends in the nerve cord contralateral to the eye detecting a looming stimulus, as the DCMD does. DCMD recordings from tethered flying locusts showed that glides follow high-frequency spikes in a DCMD, but analyses could not identify a feature of the DCMD response alone that was reliably associated with glides in all trials. This was because, for a glide to be triggered, the high-frequency spikes must be timed appropriately within the wingbeat cycle to coincide with wing elevation. We interpret this as flight-gating of the DCMD response resulting from rhythmic modulation of the flight motor neuron's membrane potential during flight. This means that the locust's escape behavior can vary in response to the same looming stimulus, meaning that a predator cannot exploit predictability in the locust's collision avoidance behavior.

Animals↗

Motor activity and trajectory control during escape jumping in the locust Locusta migratoria.

We investigated the escape jumps that locusts produce in response to approaching objects. Hindleg muscular activity during an escape jump is similar to that during a defensive kick. Locusts can direct their escape jumps up to 50 degrees either side of the direction of their long axis at the time of hindleg flexion, allowing them to consistently jump away from the side towards which an object is approaching. Variation in jump trajectory is achieved by rolling and yawing movements of the body that are controlled by the fore- and mesothoracic legs. During hindleg flexion, a locust flexes the foreleg ipsilateral to its eventual jump trajectory and then extends the contralateral foreleg. These foreleg movements continue throughout co-contraction of the hindleg tibial muscles, pivoting the locust's long axis towards its eventual jump trajectory. However, there are no bilateral differences in the motor programs of the left and right hindlegs that correlate with jump trajectory. Foreleg movements enable a locust to control its jump trajectory independent of the hindleg motor program, allowing a decision on jump trajectory to be made after the hindlegs have been cocked in preparation for a jump.

Animals↗

Reliability of signal transfer at a tonically transmitting, graded potential synapse of the locust ocellar pathway.

We assessed the performance of a synapse that transmits small, sustained, graded potentials between two classes of second-order ocellar "L-neurons" of the locust. We characterized the transmission of both fixed levels of membrane potential and fluctuating signals by recording postsynaptic responses to changes in presynaptic potential. To ensure repeatability between stimuli, we controlled presynaptic signals with a voltage clamp. We found that the synapse introduces noise above the level of background activity in the postsynaptic neuron. By driving the presynaptic neuron with slow-ramp changes in potential, we found that the number of discrete signal levels the synapse transmits is approximately 20. It can also transmit approximately 20 discrete levels when the presynaptic signal is a graded rebound spike. Synaptic noise level is constant over the operating range of the synapse, which would not be expected if presynaptic potential set the probability for the release of individual quanta of neurotransmitter according to Poisson statistics. Responses to individual quanta of neurotransmission could not be resolved, which is consistent with a synapse that operates with large numbers of vesicles evoking small responses. When challenged with white noise stimuli, the synapse can transmit information at rates up to 450 bits/s, a performance that is sufficient to transmit natural signals about changes in illumination.

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Differential expression of synapsin in visual neurons of the locust Schistocerca gregaria.

In many taxa, photoreceptors and their second-order neurons operate with graded changes in membrane potential and can release neurotransmitter tonically. A common feature of such neurons in vertebrates is that they have not been found to contain synapsins, a family of proteins that indicate the presence of a reserve pool of synaptic vesicles at synaptic sites. Here, we provide a detailed analysis of synapsin-like immunoreactivity in the compound eye and ocellar photoreceptor cells of the locust Schistocerca gregaria and in some of the second-order neurons. By combining confocal laser scanning microscopy with electron microscopy, we found that photoreceptor cells of both the compound eye and the ocellus lacked synapsin-like immunostaining. In contrast, lamina monopolar cells and large ocellar L interneurons of the lateral ocellus were immunopositive to synapsin. We also identified the output synapses of the photoreceptors and of the L interneurons, and, whereas the photoreceptor synapses lacked immunolabeling, the outputs of the L interneurons were clearly labeled for synapsin. These findings suggest that the photoreceptors and the large second-order neurons of the locust differ in the chemical architecture of their synapses, and we propose that differences in the time course of neurotransmission are the reason for this.

Animals↗

Gliding behaviour elicited by lateral looming stimuli in flying locusts.

We challenged tethered, flying locusts with visual stimuli looming from the side towards one eye in a way that mimics the approach of a predatory bird. Locusts respond to the lateral approach of a looming object with steering movements and a stereotyped, rapid behaviour in which the wingbeat pattern ceases and the wings are swept into a gliding posture. This gliding behaviour may cause the locust to dive. The gliding posture is maintained for 200 ms or more after which flight is resumed with an increased wingbeat frequency or else the wings are folded. A glide begins with a strong burst of activity in the mesothoracic second tergosternal motor neuron (no. 84) on both sides of the locust. Recordings of descending contralateral movement detector (DCMD) activity in a flying locust show that it responds to small (80-mm diameter) looming stimuli during tethered flight, with a prolonged burst of spikes that tracks stimulus approach and reaches peak instantaneous frequencies as, or after, stimulus motion ceases. There is a close match between the visual stimuli that elicit a gliding behaviour and those that are effective at exciting the DCMD neuron. Wing elevation into the gliding posture occurs during a maintained burst of high frequency DCMD spikes.

Animals↗

Presynaptic depolarization rate controls transmission at an invertebrate synapse.

Second-order neurons L1-3 of the locust ocellar pathway make inhibitory synapses with each other. Although the synapses transmit graded potentials, transmission depresses rapidly and completely so that a synapse only transmits when the presynaptic terminal depolarizes rapidly. The rate at which a presynaptic neuron depolarizes determines the rate at which a postsynaptic neuron hyperpolarizes, and neurotransmitter is only released during a fixed 2 ms long period. Consequently, the amplitude of a postsynaptic potential depends on the rate rather than the amplitude of a presynaptic depolarization. Following a postsynaptic potential, a synapse recovers from depression over about a second. The synapse recovers from depression even if the presynaptic terminal is held depolarized.

Action Potentials↗

Signal processing in a simple visual system: the locust ocellar system and its synapses.

The neurons with the widest axons that carry information into a locust brain belong to L-neurons, the large, second-order neurons of the ocelli. L-neurons play roles in flight control and boosting visual sensitivity. Their morphology is simple, and their axons convey graded potentials from the ocellus with little decrement to the brain, which makes them good subjects in which to study transmission of graded potentials. L-neurons are very sensitive to changes in light, due to an abnormally high gain in the sign inverting synapses they receive from photoreceptors. Adaptation ensures that L-neurons signal contrast in a light signal when average light intensity changes, and that their responses depend on the speed of change in light. Neurons L1-3 make excitatory output synapses with third-order neurons and with L4-5. These synapses transmit tonically, but are unable to convey hyperpolarising signals about large increases in light. Graded rebound spikes enhance depolarising responses. L1-3 also make reciprocal inhibitory synapses with each other and transmission at these decrements so rapidly that it normally requires a presynaptic spike. The resolution with which graded potentials can be transferred has been studied at the inhibitory synapses, and is limited by intrinsic variability in the mechanism that determines neurotransmitter release. Electron microscopy has shown that each excitatory connection made from an L-neuron to a postsynaptic partner consists of thousands of discrete synaptic contacts, in which individual dense-staining bars in the presynaptic neuron are associated with clouds of vesicles. Acetylcholine is likely to be a neurotransmitter released by L-neurons.

Adaptation, Physiological↗

The organization of synaptic vesicles at tonically transmitting connections of locust visual interneurons.

Large, second-order neurons of locust ocelli, or L-neurons, make some output connections that transmit small changes in membrane potential and can sustain transmission tonically. The synaptic connections are made from the axons of L-neurons in the lateral ocellar tracts, and are characterized by bar-shaped presynaptic densities and densely packed clouds of vesicles near to the cell membrane. A cloud of vesicles can extend much of the length of this synaptic zone, and there is no border between the vesicles that are associated with neighboring presynaptic densities. In some axons, presynaptic densities are associated with discrete small clusters of vesicles. Up to 6% of the volume of a length of axon in a synaptic zone can be occupied with a vesicle cloud, packed with 4.5 to 5.5 thousand vesicles per microm(3). Presynaptic densities vary in length, from less than 70 nm to 1.5 microm, with shorter presynaptic densities being most frequent. The distribution of vesicles around short presynaptic densities was indistinguishable from that around long presynaptic densities, and vesicles were distributed in a similar way right along the length of a presynaptic density. Within the cytoplasm, vesicles are homogeneously distributed within a cloud. We found no differences in the distribution of vesicles in clouds between locusts that had been dark-adapted and locusts that had been light-adapted before fixation.

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