Responses of a Looming-Sensitive Neuron to Compound and Paired Object Approaches

2006 ◽  
Vol 95 (3) ◽  
pp. 1428-1441 ◽  
Author(s):  
Bruce B. Guest ◽  
John R. Gray

The lobula giant movement detector (LGMD) and its target neuron, the descending contralateral movement detector (DCMD), constitute a motion-sensitive pathway in the locust visual system that responds preferentially to objects approaching on a collision course. LGMD receptive field properties, anisotropic distribution of local retinotopic inputs across the visual field, and localized habituation to repeated stimuli suggest that this pathway should be sensitive to approaches of individual objects within a complex visual scene. We presented locusts with compound looming objects while recording from the DCMD to test the effects of nonuniform edge expansion on looming responses. We also presented paired objects approaching from different regions of the visual field at nonoverlapping, closely timed and simultaneous approach intervals to study DCMD responses to multiple looming stimuli. We found that looming compound objects evoked characteristic responses in the DCMD and that the time of peak firing was consistent with predicted values based on a weighted ratio of the half size of each distinct object edge and the absolute approach velocity. We also found that the azimuthal position and interval of paired approaches affected DCMD firing properties and that DCMDs responded to individual objects approaching within 106 ms of each other. Moreover, comparisons between individual and paired approaches revealed that overlapping approaches are processed in a strongly sublinear manner. These findings are consistent with biophysical mechanisms that produce nonlinear integration of excitatory and feed-forward inhibitory inputs onto the LGMD that have been shown to underlie responses to looming stimuli.

2012 ◽  
Vol 108 (4) ◽  
pp. 1052-1068 ◽  
Author(s):  
Glyn A. McMillan ◽  
John R. Gray

Two identified locust neurons, the lobula giant movement detector (LGMD) and its postsynaptic partner, the descending contralateral movement detector (DCMD), constitute one motion-sensitive pathway in the visual system that responds preferentially to objects that approach on a direct collision course and are implicated in collision-avoidance behavior. Previously described responses to the approach of paired objects and approaches at different time intervals (Guest BB, Gray JR. J Neurophysiol 95: 1428–1441, 2006) suggest that this pathway may also be affected by more complicated movements in the locust's visual environment. To test this possibility we presented stationary locusts with disks traveling along combinations of colliding (looming), noncolliding (translatory), and near-miss trajectories. Distinctly different responses to different trajectories and trajectory changes demonstrate that DCMD responds to complex aspects of local visual motion. DCMD peak firing rates associated with the time of collision remained relatively invariant after a trajectory change from translation to looming. Translatory motion initiated in the frontal visual field generated a larger peak firing rate relative to object motion initiated in the posterior visual field, and the peak varied with simulated distance from the eye. Transition from translation to looming produced a transient decrease in the firing rate, whereas transition away from looming produced a transient increase. The change in firing rate at the time of transition was strongly correlated with unique expansion parameters described by the instantaneous angular acceleration of the leading edge and subtense angle of the disk. However, response time remained invariant. While these results may reflect low spatial resolution of the compound eye, they also suggest that this motion-sensitive pathway may be capable of monitoring dynamic expansion properties of objects that change the trajectory of motion.


2014 ◽  
Vol 111 (9) ◽  
pp. 1736-1745 ◽  
Author(s):  
Paul C. Dick ◽  
John R. Gray

The lobula giant movement detector (LGMD) and descending contralateral movement detector (DCMD) constitute one motion-sensitive pathway in the locust visual system that is implicated in collision-avoidance behaviors. While this pathway is thought to respond preferentially to objects approaching on a direct collision course, emerging studies suggest the firing rate is able to monitor more complicated movements that would occur under natural conditions. While previous studies have compared the response of the DCMD to objects on collision courses that travel at different speeds, velocity has not been manipulated for other simple or compound trajectories. Here we test the possibility that the LGMD/DCMD pathway is capable of responding uniquely to complex aspects of object motion, including translation and trajectory changes at different velocities. We found that the response of the DCMD to translational motion initiated in the caudal visual field was a low-amplitude peak in firing rate that occurred before the object crossed 90° azimuth that was invariant to different object velocities. Direct looms at different velocities resulted in peak firing rates that occurred later in time and with greater amplitude for higher velocities. In response to transitions from translational motion to a collision course, the firing rate change depended on both the location within the visual field and the velocity. These results suggest that this pathway is capable of conveying information about multiple properties of a moving object's trajectory.


1974 ◽  
Vol 60 (1) ◽  
pp. 1-12
Author(s):  
M. O'SHEA ◽  
C. H. F. ROWELL ◽  
J. L. D. WILLIAMS

1. The DCMD neurone is physiologically well-known and runs from the brain to the metathoracic ganglion. It responds to novel movement of small contrasting objects in the visual field and synapses on metathoracic motoneurones which mediate the jump of the locust. Its anatomy, here reported, has been visualized by intracellular cobalt staining. 2. The soma is 50 µm in diameter and lies on the upper posterior face of the protocerebrum, lateral to the midline. A neurite runs to a thickened integrating segment 20 µm. in diameter, which bears numerous dendrites; none of these extends to the optic lobe. An axon leaves the integrating segment, crosses the brain, thickens to about 17µm and descends the contralateral nerve cord. 3. The descending axon terminates in the metathoracic ganglion, where it has three major branches both ipsi- and contralateral. Its branching in the mesothoracic ganglion is similar, but extends only ipsilaterally; in the prothoracic ganglion there is reduced branching, and in the suboesophageal ganglion none at all. 4. The branching pattern in the metathorax is compatible with, and entirely explicable by, the known synaptic connexions with motoneurones. 5. The morphological description of the cell has made possible intracellular recording from axon, integrating segment and soma.


1980 ◽  
Vol 86 (1) ◽  
pp. 87-97
Author(s):  
PETER SIMMONS

Both of the descending contralateral movement detector (DCMD) neurones of Schistocerca americana gregaria, which respond to stimulation of the contralateral eye or to loud noises, mediate excitatory postsynaptic potentials in most ipsilateral flight motoneurones.


2004 ◽  
Vol 91 (1) ◽  
pp. 1-12 ◽  
Author(s):  
Thomas Matheson ◽  
Stephen M. Rogers ◽  
Holger G. Krapp

We demonstrate pronounced differences in the visual system of a polyphenic locust species that can change reversibly between two forms (phases), which vary in morphology and behavior. At low population densities, individuals of Schistocerca gregaria develop into the solitarious phase, are cryptic, and tend to avoid other locusts. At high densities, individuals develop instead into the swarm-forming gregarious phase. We analyzed in both phases the responses of an identified visual interneuron, the descending contralateral movement detector (DCMD), which responds to approaching objects. We demonstrate that habituation of DCMD is fivefold stronger in solitarious locusts. In both phases, the mean time of peak firing relative to the time to collision nevertheless occurs with a similar characteristic delay after an approaching object reaches a particular angular extent on the retina. Variation in the time of peak firing is greater in solitarious locusts, which have lower firing rates. Threshold angle and delay are therefore conserved despite changes in habituation or behavioral phase state. The different rates of habituation should contribute to different predator escape strategies or flight control for locusts living either in a swarm or as isolated individuals. For example, increased variability in the habituated responses of solitarious locusts should render their escape behaviors less predictable. Relative resistance to habituation in gregarious locusts should permit the continued responsiveness required to avoid colliding with other locusts in a swarm. These results will permit us to analyze neuronal plasticity in a model system with a well-defined and controllable behavioral context.


2006 ◽  
Vol 95 (6) ◽  
pp. 3391-3400 ◽  
Author(s):  
Roger D. Santer ◽  
F. Claire Rind ◽  
Richard Stafford ◽  
Peter J. Simmons

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.


Development ◽  
1984 ◽  
Vol 83 (1) ◽  
pp. 189-211
Author(s):  
D. J. Emery ◽  
K. A. Bell ◽  
W. Chapco ◽  
J. D. Steeves

A reduced-eye (re) mutant grasshopper of Melanoplus sanguinipes has been characterized by small flat compound eyes lacking facets, no lateral ocelli and only a remnant of the median ocellus. The re grasshoppers walk, jump, fly and feed in a normal manner, but do not respond to visual and auditory stimuli, suggesting they may be blind and deaf. Extracellular recordings from the ventral nerve cord of re mutants verified the lack of neural activity in response to visual and auditory inputs, yet the mutants detected mechanical and tactile stimuli. Electroretinograms implied that a visual deficit may be within the photoreceptors of the compound eye. Histological examination of the compound eyes and ocelli indicated that the cells of the mutant compound eye incompletely differentiate. The optic lamina underlying the retina is missing, as is the outer optic chiasma. The medulla and lobula of the mutant optic lobe are present, however, the neuropil of the medulla lacks the characteristic axonal projection patterns of wild-type grasshoppers. The re grasshopper also lacks all ocellar nerves. Ocellar nerves are normally formed from processes of second order ocellar neurons (SONs), suggesting that if the mutant SONs are present within the protocerebrum, their morphology is drastically altered. Comparison of embryos and juvenile nymphs supports the suggestion that the alterations in the re visual system are the result of abnormal differentiation during development. Even though there is clear evidence of morphological alterations in second and third order optic lobe interneurons, one higher order visual interneuron of the midbrain, the descending contralateral movement detector (DCMD), has the same morphology as the DCMD in a wildtype brain. In this instance, the complete deprivation of the primary sensory input does not appear to alter cellular development.


1995 ◽  
Vol 74 (6) ◽  
pp. 2739-2743 ◽  
Author(s):  
J. P. Bacon ◽  
K. S. Thompson ◽  
M. Stern

1. Habituation is the declining responsiveness of a neural circuit (or behavior) to repetitive stimulation. Dishabituation (or arousal) can be brought about by the sudden presentation of an additional, novel stimulus. A clear example of arousal in the locust is provided by the visual system: the habituated response of the descending contralateral movement detector (DCMD) interneuron to repetitive visual stimuli can be dishabituated by a variety of other visual and tactile stimuli. 2. Application of octopamine to the locust brain and optic lobes dishabituates the DCMD in a manner similar to the effect of visual and tactile stimulation. 3. The locust CNS contains two pairs of octopamine-immunoreactive cells, the protocerebral medulla 4 (PM4) neurons, that could potentially mediate this dishabituation effect; PM4 neurons arborize in the optic lobe, they contain octopamine, and they respond to the same visual and tactile stimuli that dishabituate the DCMD. 4. To investigate whether PM4 activity dishabituates the DCMD, we recorded intracellularly from one of the PM4 neurons while recording extracellularly from the DCMD. When the PM4 neuron is injected with hyperpolarizing current to render it completely inactive, the DCMD exhibits its characteristic habituation to a moving visual stimulus. However, depolarizing the PM4 neuron, to produce action potentials at approximately 20 Hz, significantly increases the number of DCMD action potentials per stimulus. 5. The PM4 neurons may therefore play an important role in dishabituating the DCMD to novel stimuli. This effect is presumably mediated by PM4 neurons releasing endogenous octopamine within the optic lobe.


1997 ◽  
Vol 200 (16) ◽  
pp. 2209-2216 ◽  
Author(s):  
S Judge ◽  
F Rind

A Silicon Graphics computer was used to challenge the locust descending contralateral movement detector (DCMD) neurone with images of approaching objects. The DCMD gave its strongest response, measured as either total spike number or spike frequency, to objects approaching on a direct collision course. Deviation in either a horizontal or vertical direction from a direct collision course resulted in a reduced response. The decline in the DCMD response with increasing deviation from a collision course was used as a measure of the tightness of DCMD tuning for collision trajectories. Tuning was defined as the half-width of the response when it had fallen to half its maximum level. The response tuning, measured as averaged mean spike number versus deviation away from a collision course, had a half-width at half-maximum response of 2.4 °­3.0 ° for a deviation in the horizontal direction and 3.0 ° for a deviation in the vertical direction. Mean peak spike frequency showed an even sharper tuning, with a half-width at half-maximum response of 1.8 ° for deviations away from a collision course in the horizontal plane.


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