Receptive field properties and intensity-response functions of polarization-sensitive neurons of the optic tubercle in gregarious and solitarious locusts

Many migrating insects rely on the plane of sky polarization as a cue to detect spatial directions. Desert locusts (Schistocerca gregaria), like other insects, perceive polarized light through specialized photoreceptors in a dorsal eye region. Desert locusts occur in two phases: a gregarious swarming phase, which migrates during the day, and a solitarious nocturnal phase. Neurons in a small brain area, the anterior optic tubercle (AOTu), are critically involved in processing polarized light in the locust brain. While polarization-sensitive intertubercle cells [lobula-tubercle neuron 1 (LoTu1) and tubercle-tubercle neuron 1 (TuTu1)] interconnect the AOTu of both hemispheres, tubercle-lateral accessory lobe tract (TuLAL1) neurons transmit sky compass signals to a polarization compass in the central brain. To better understand the neural network underlying polarized light processing in the AOTu and to investigate possible adaptations of the polarization vision system to a diurnal versus nocturnal lifestyle, we analyzed receptive field properties, intensity-response relationships, and daytime dependence of responses of AOTu neurons in gregarious and solitarious locusts. Surprisingly, no differences in the physiology of these neurons were found between the two locust phases. Instead, clear differences were observed between the different types of AOTu neurons. Whereas TuTu1 and TuLAL1 neurons encoded E-vector orientation independent of light intensity and would thus be operational in bright daylight, LoTu1 neurons were inhibited by high light intensity and provided strong polarization signaling only under dim light conditions. The presence of high- and low-intensity polarization channels might, therefore, allow solitarious and gregarious locusts to use the same polarization coding system despite their different activity cycles.     

Responses of a looming-sensitive neuron to compound and paired object approaches

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.     

Arousal facilitates collision avoidance mediated by a looming sensitive visual neuron in a flying locust

Locusts have two large collision-detecting neurons, the descending contralateral movement detectors (DCMDs) that signal object approach and trigger evasive glides during flight. We sought to investigate whether vision for action, when the locust is in an aroused state rather than a passive viewer, significantly alters visual processing in this collision-detecting pathway. To do this we used two different approaches to determine how the arousal state of a locust affects the prolonged periods of high-frequency spikes typical of the DCMD response to approaching objects that trigger evasive glides. First, we manipulated arousal state in the locust by applying a brief mechanical stimulation to the hind leg; this type of change of state occurs when gregarious locusts accumulate in high-density swarms. Second, we examined DCMD responses during flight because flight produces a heightened physiological state of arousal in locusts. When arousal was induced by either method we found that the DCMD response recovered from a previously habituated state; that it followed object motion throughout approach; and--most important--that it was significantly more likely to generate the maintained spike frequencies capable of evoking gliding dives even with extremely short intervals (1.8 s) between approaches. Overall, tethered flying locusts responded to 41% of simulated approaching objects (sets of 6 with 1.8 s ISI). When we injected epinastine, the neuronal octopamine receptor antagonist, into the hemolymph responsiveness declined to 12%, suggesting that octopamine plays a significant role in maintaining responsiveness of the DCMD and the locust to visual stimuli during flight.     

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.     

A looming-sensitive pathway responds to changes in the trajectory of object motion

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.     

The influence of gender and the estrous cycle on learned helplessness in the rat

Although the etiology of clinical depression is unknown, women are more likely to suffer from major depressive disorder than men. In addition, in some women, there is a clear association between depression and specific phases of the menstrual cycle. Surprisingly little research has examined gender differences and the influences of the estrous cycle in this and other animal behavioral models of clinical depression. Learned helplessness is a valid animal model of stress-induced behavioral depression in which prior exposure to inescapable stress produces deficits in escape testing. Learned helplessness was studied in rats using an inescapable tail shock stress followed by a shuttle box test to determine escape latencies. Animals with mean escape latencies of >or=20 s after shuttle-box testing are defined as learned helpless. Males and normal cycling female rats in the estrus and diestrus II phases were studied. Female rats in the diestrus II phase had significantly higher escape latencies and exhibited a more helpless behavior than female rats in the estrus phase. Male rat escape latencies were intermediate between the two female phases. These results suggest a role for gonadal hormones in the development of stress-induced behavioral depression or 'learned helplessness.'     

The enigma of behavioral inputs to the circadian clock: a test of function using restraint

Wheel running stimulated during the daily rest period can acutely shift circadian rhythms in Syrian hamsters. Spontaneous running, defining the active phase of the circadian rest-activity cycle, can shorten the circadian periodicity in constant light or dark in several nocturnal rodent species. The adaptive significance of these behavioral effects on pacemaker phase and period is unclear. Here we consider a hypothesis that behavioral inputs to the circadian pacemaker serve primarily to enhance the precision of light-dark entrainment and maintain daily activity onset close to lights-off (i.e., dusk) by stabilizing entrainment on a steeper portion of the delay zone of the phase-response curve to light. This hypothesis rests on the evidence that spontaneous activity early in the active period feeds back on the pacemaker to advance its motion. If so, then preventing activity at this time should induce a phase delay shift. Such delay shifts have been reported in Syrian hamsters physically restrained early in the active period. We show here that restraint can induce phase delays but that, using the Aschoff Type 2 procedure for measuring shifts, these delays are very small, are inversely related to behavioral sleep during restraint, and are positively correlated with 'rebound' increases in running following restraint, at a circadian time when stimulated running is known to induce phase delay shifts. Repeated bouts of restraint, to promote habituation, were associated with strong attenuation of 'rebound' running and no significant delay shifts. These results suggest that, in Syrian hamsters, spontaneous activity early at night has little effect on pacemaker motion, and argue against the stated hypothesis.     

Heat stress-mediated plasticity in a locust looming-sensitive visual interneuron

Neural circuits are strongly affected by temperature and failure ensues at extremes. However, detrimental effects of high temperature on neural pathways can be mitigated by prior exposure to high, but sublethal temperatures (heat shock). Using the migratory locust, Locusta migratoria, we investigated the effects of heat shock on the thermosensitivity of a visual interneuron [the descending contralateral movement detector (DCMD)]. Activity in the DCMD was elicited using a looming stimulus and the response was recorded from the axon using intracellular and extracellular methods. The thoracic region was perfused with temperature-controlled saline and measurements were taken at 5 degrees intervals starting at 25 degrees C. Activity in DCMD was decreased in control animals with increased temperature, whereas heat-shocked animals had a potentiated response such that the peak firing frequency was increased. Significant differences were also found in the thermosensitivity of the action potential properties between control and heat-shocked animals. Heat shock also had a potentiating effect on the amplitude of the afterdepolarization. The concurrent increase in peak firing frequency and maintenance of action potential properties after heat shock could enhance the reliability with which DCMD initiates visually guided behaviors at high temperature.     

Rostral ganglia are required for induction but not expression of crayfish escape reflex habituation: role of higher centers in reprogramming low-level circuits

It is widely assumed that learning results from alterations in the strength of synapses within the neural pathways that mediate a learned behavioral response and that these alterations are directly caused by training-induced activity of neurons connected by the changing synapses. Initial evidence for this view came from studies of habituation of defensive reflexes in several invertebrate species. However, more recent studies of habituation of the escape reflex in one of these species, the crayfish, have shown that habituation is substantially caused by tonic inhibitory input from cephalic ganglia; this descending inhibition suppresses the activity of neurons within the escape circuit, which reside in caudal ganglia. Such control by descending inhibition indicates that animals with encephalized nervous systems do not entirely abdicate to low-level circuitry the important decision of whether to habituate to stimuli that might warn of danger. Higher centers in fact play a major role in controlling the habituation of this potentially life-saving protective response. Another way for higher centers to control lower ones would be to induce alteration of the lower center's intrinsic properties. Here, we show that, whereas descending input from higher ganglia is needed to induce habituation, once established, habituation persists even after rostral ganglia are disconnected. This provides evidence that lower-level neural circuits can be reprogrammed through transient interaction with higher ganglia to decrease their intrinsic tendency to produce escape.     

Developmental and genetic variables in mouse startle response habituation.

A behavioral task insensitive to inherent sensory and motor limitations, specifically a startle response habituation technique, was used to investigate genetic (strains) and developmental (age) effects on behavior. All mice tested using two procedures exhibited evidence for habituation which was dependent on strain, age, and length of the testing process. Exploitation of this simple technique may permit clarfication of more complex types of behavior.     

Orthopteran DCMD neuron: a reevaluation of responses to moving objects. II. Critical cues for detecting approaching objects.

1. We examine the critical image cues that are used by the locust visual system for the descending contralateral motion detector (DCMD) neuron to distinguish approaching from receding objects. Images were controlled by computer and presented on an electrostatic monitor. 2. Changes in overall luminance elicited much smaller and briefer responses from the DCMD than objects that appeared to approach the eye. Although a decrease in overall luminance might boost the response to an approaching dark object, movement of edges of the image is more important. 3. When two pairs of lines, in a cross-hairs configuration, were moved apart and then together again, the DCMD showed no preference for divergence compared with convergence of edges. A directional response was obtained by either making the lines increase in extent during divergence and decrease in extent during convergence; or by continually increasing the velocity of line movement during divergence and decreasing velocity during convergence. 4. The DCMD consistently gave a larger response to growing than to shrinking solid rectangular images. An increase compared with a decrease in the extent of edge in an image is, therefore, an important cue for the directionality of the response. For single moving edges of fixed extent, the neuron gave the largest response to edges that subtended 15 degrees at the eye. 5. The DCMD was very sensitive to the amount by which an edge traveled between frames on the display screen, with the largest responses generated by 2.5 degrees of travel. This implies that the neurons in the optic lobe that drive this movement-detecting system have receptive fields of about the same extent as a single ommatidium. 6. For edges moving up to 250 degree/s, the excitation of the DCMD increases with velocity. The response to an edge moving at a constant velocity adapts rapidly, in a manner that depends on velocity. Movement over one part of the retina can adapt the subsequent response to movement over another part of the retina. 7. For the DCMD to track and continue to respond to the image of an approaching object, the edges of the image must continually increase in velocity. This is the second important stimulus cue. 8. Edges of opposite contrasts (light-dark compared with dark-light) are processed in separate pathways that inhibit each other. This would contribute to the reduction of responses to wide-field movements.     

Orthopteran DCMD neuron: a reevaluation of responses to moving objects. I. Selective responses to approaching objects.

1. The "descending contralateral movement detector" (DCMD) neuron in the locust has been challenged with a variety of moving stimuli, including scenes from a film (Star Wars), moving disks, and images generated by computer. The neuron responds well to any rapid movement. For a dark object moving along a straight path at a uniform velocity, the DCMD gives the strongest response when the object travels directly toward the eye, and the weakest when the object travels away from the eye. Instead of expressing selectivity for movements of small rather than large objects, the DCMD responds preferentially to approaching objects. 2. The neuron shows a clear selectivity for approach over recession for a variety of sizes and velocities of movement both of real objects and in simulated movements. When a disk that subtends > or = 5 degrees at the eye approaches the eye, there are two peaks in spike rate: one immediately after the start of movement; and a second that builds up during the approach. When a disk recedes from the eye, there is a single peak in response as the movement starts. There is a good correlation between spike rate and angular acceleration of the edges of the image over the eye. 3. When an object approaches from a distance sufficient for it to subtend less than one interommatidial angle at the start of its approach, there is a single peak in response. The DCMD tracks the approach, and, if the object moves at 1 m/s or faster, the spike rate increases throughout the duration of object movement. The size of the response depends on the speed of approach. 4. It is unlikely that the DCMD encodes the time to collision accurately, because the response depends on the size as well as the velocity of an approaching object. 5. Wide-field movements suppress the response to an approaching object. The suppression varies with the temporal frequency of the background pattern. 6. Over a wide range of contrasts of object against background, the DCMD gives a stronger response to approaching than to receding objects. For low contrasts, the selectivity is greater for objects that are darker than the background than for objects that are lighter.     

Aversive noise effects on performance and thalamocortical responsiveness in cats

The effects of noise bursts (115dBA) on runway performance, emotional behaviors, and visual thalamocortical responsiveness were examined in five cats. Aversion thresholds for noise were subsequently determined in a shuttle box preference test. For three animals the noise was aversive, produced a disruption of runway performance and escape behaviors, and significantly attenuated the intracortical evoked potential (EP) components produced by stimulation of the optic tract. Examination of videotapes taken during noise stimulation indicated that the EP returned to preaversion amplitudes simultaneously with behavioral habituation. The EP intracortical components remained within control levels for animals for whom the noise was not aversive. The aversion effects were concluded to be produced by high arousal activating cortical inhibition. The subsequent behavioral and electrophysiological habituation may involve negative feedback modulation of reticular activity, whereupon cortical functioning returns to preaversion levels.     

The effects of signal value on short- and long-term habituation

The present study examined the effects of signal value on short- and long-term habituation of the skin conductance response. Subjects (N = 48) attended the laboratory at the same time of day on two consecutive days. Day 1 comprised pretraining and training phases, and day 2 comprised the test phase. In the pretraining phase subjects received one presentation each of a tone and a vibration stimulus. In the training and test phases subjects received a randomly ordered sequence of 15 tones and 15 vibrations. All stimuli were of 4 s duration. During the training phase Groups E1 and E2 performed a motor response to the offset of one of the stimuli whereas a third group (Group C) did not. Neither Group E1 nor Group C performed the motor task during the pretraining and test phases. Both between- and within-group analyses of the training phase data indicated that responses were larger and habituation was slower to signal stimuli. Analyses of the test phase data and comparison of pretraining and test phase data indicated that long-term habituation occurred only to nonsignal stimuli. The results are discussed in terms of Wagner's (1978) theory of habituation.     

X-ray induced behavioral reactions and detection mechanisms in the shrimp.

Red Ghost Shrimp, Callianassa californiensis, were shown from behavioral and electrophysiological studies to respond to ionizing radiation. When exposed to X-rays at 52 R/sec, the majority of intact animals could detect and avoid further irradiation by escaping into a shielded section of the test chamber. Animals continued to display escape responses after removal of eyestalks and antennae. Significant avoidance activity also occurred with partial-body exposure and indicated the existence of a radiation-sensitive receptor on the abdomen. Electroretinograms elecited by beta- and X-radiation sources corresponded closely with the waveforms produced by visible light stimulation. Electroantennograms were recorded from isolated antennules following stimulation with glutamic acid, beta-, and X-radiation. Biphasic on-off phases were recorded with an intermediate phase present during the longer duration exposures. Similarly, bioelectrical potentials were recorded from swimmeret preparations with exposure to beta- and X-radiation. The electrophysiological evidence indicates that the eye, antennules, and possibly chemoreceptors on the abdominal segments serve as routes for detection of ionizing radiations.     

Circadian phase and intertrial interval interfere with social recognition memory

A modified version of the social habituation/dis-habituation paradigm was employed to examine social recognition memory in Wistar rats during two opposing (active and inactive) circadian phases, using different intertrial intervals (30 and 60 min). Wheel-running activity was monitored continuously to identify circadian phase. To avoid possible masking effects of the light-dark cycle, the rats were synchronized to a skeleton photoperiod, which allowed testing during different circadian phases under identical lighting conditions. In each trial, an infantile intruder was introduced into an adult's home-cage for a 5-minute interaction session, and social behaviors were registered. Rats were exposed to 5 trials per day for 4 consecutive days: on days 1 and 2, each resident was exposed to the same intruder; on days 3 and 4, each resident was exposed to a different intruder in each trial. The resident's social investigatory behavior was more intense when different intruders were presented compared to repeated presentation of the same intruder, suggesting social recognition memory. This effect was stronger when the rats were tested during the inactive phase and when the intertrial interval was 60 min. These findings suggest that social recognition memory, as evaluated in this modified habituation/dis-habituation paradigm, is influenced by the circadian rhythm phase during which testing is performed, and by intertrial interval.     

Presynaptic inhibition: the mechanism of protection from habituation of the crayfish lateral giant fibre escape response.

1. Mechanism of protection from habituation of the lateral giant escape reflex of the crayfish was studied. Experiments were designed to determine whether presynaptic inhibition of primary afferents for the reflex occurs following escape command neurone firing, and if so, whether it could account for protection of the first synapse from depression. 2. Synaptic transmission between afferents and interneurone A of the escape reflex is strongly inhibited following giant fibre spikes. 3. Giant fibre firing results in post-synaptic inhibition of interneurone A. However, inhibition of afferent input to interneurone A consistently outlasts both i.p.s.p.s and post-synaptic conductance increases in the neurone; the inhibition, therefore, is probably not exclusively post-synaptic. 4. Giant fibre firing results in excitability changes in sensory afferent terminals as measured by the amplitude of antidromic compound action potentials to focal electrical stimuli applied in the region of afferent terminals in the last abdominal ganglion. The time course of this effect parallels those of protection and inhibition of the first synapse. 5. The magnitude and time course of protection and inhibition of transmission to interneurone A parallel each other closely. Both processes considerably outlast measurable signs of post-synaptic inhibition. 6. We conclude that following giant fibre activity the first synapse of the lateral giant reflex is presynaptically inhibited and the presynaptic inhibition is responsible for the protection effect described in the preceding paper.     

Protection from habituation of the crayfish lateral giant fibre escape response

1. Habituation of the lateral giant fibre escape response in the crayfish to repetitive tactile stimuli is believed to result from homosynaptic depression at the first synapse of the reflex, between tactile afferents and interneurones. Normally, habituation of escape responses to repeated innocuous stimuli is presumed to be adaptive. Experiments reported here were undertaken to determine whether habituation would occur under circumstances when it would presumably be maladaptive - in particular, when tactile receptors are stimulated by an animal's own tail-flip movements.2. Experiments were carried out on the crayfish isolated abdominal nerve cord, which contains the lateral giant reflex pathway.3. Compound e.p.s.p.s elicited in the lateral giant by electrical stimulation of tactile afferents decline by from 25 to 36% over a series of eleven trials at 1/5 sec (control series).4. To determine whether such a decline would occur when sensory afferents are stimulated during a ;tail-flip', stimuli were given as in the control series but each stimulus occurred 20 msec after direct electrical stimulation of a medial giant or lateral giant escape-command fibre at which time tail flexion movements of an intact animal would be in progress. Under these conditions% e.p.s.p. decline over 11 trials at 1/5 sec was only 16-45% of that occurring on the control series.5. This protective effect starts at about 10 msec after escape command neurone firing, is maximal at 20 msec, and thereafter declines, remaining weakly detectable at 100 msec. This time course is commensurate with that required for execution of a tail-flip movement. Thus, sensory afferent-to-lateral giant transmission is protected from depression if stimuli occur when a tail-flip movement is or should be occurring.6. Giant fibre spikes do not superimpose facilitation upon a depressed reflex pathway, nor accelerate rate of recovery from depression; rather, protection is attributable to actual prevention of development of the depressed state.7. Protection was also examined at the first synapse of the reflex, where the depression responsible for habituation is believed to occur, by recording intracellularly in the largest of the first-order interneurones (interneurone A) of the pathway. In absence of protection, ten stimuli presented at 1/4 sec caused a mean decline of 32% in the e.p.s.p. in interneurone A. When such stimuli followed directly evoked escape command neurone firing by 20 msec this decline was reduced by 59-100%.8. We suggest that protection serves to prevent crayfish from habituating to stimuli produced by their own tail-flip movements.     

Spatial distribution of inputs and local receptive field properties of a wide-field, looming sensitive neuron

The lobula giant movement detector (LGMD) in the locust visual system and its target neuron, the descending contralateral movement detector (DCMD), respond to approaching objects looming on a collision course with the animal. They thus provide a good model to study the cellular and network mechanisms underlying the sensitivity to this specific class of behaviorally relevant stimuli. We determined over an entire locust eye the density distribution of optical axes describing the spatial organization of local inputs to the visual system and compared it with the sensitivity distribution of the LGMD/DCMD to local motion stimuli. The density of optical axes peaks in the equatorial region of the frontal eye. Local motion sensitivity, however, peaks in the equatorial region of the caudolateral visual field and only correlates positively with the dorso-ventral density of optical axes. On local stimulation, both the velocity tuning and the response latency of the LGMD/DCMD depend on stimulus position within the visual field. Spatial and temporal integration experiments in which several local motion stimuli were activated either simultaneously or at fixed delays reveal that the LGMD processes local motion in a strongly sublinear way. Thus the neuron's integration properties seem to depend on several factors including its dendritic morphology, the local characteristics of afferent fiber inputs, and inhibition mediated by different pathways or by voltage-gated conductances. Our study shows that the selectivity of this looming sensitive neuron to approaching objects relies on more complex biophysical mechanisms than previously thought.