The characterization and modelling of antipredator defensive behavior

The mammalian behavioral antipredator defense systems have been characterized in terms of reactions to present, localizable, threat stimuli: Analysis of the relationship between features of the predator and the environment, and specific defensive behaviors indicates that the latter can be predicted with a high degree of accuracy. A different set of defensive behaviors are seen when rats living in burrow systems are confronted by a predator outside the burrow. Flight to the burrow and immobility inside the burrow are followed by active investigation of the surface where the cat was seen (risk assessment), with all of these accompanied by inhibition of nondefensive behaviors such as eating, drinking, sexual behavior and aggression. Two additional behaviors are described in this context, ultrasonic cries made at a high initial rate (50% time) by animals inside the burrow systems, and declining over 1-2 hours following predator exposure, and, a specific modification of eating patterns when the subjects return to the surface and begin to eat. Eating bouts are shortened, with fewer episodes of continuous eating, interspersed with intervals of scanning of the environment, a vigilance activity previously reported in field research. This analysis of a broad spectrum of defensive behaviors is being used to develop test batteries providing simplified models of these phenomena.     

Neural evidence for representation-specific response selection

Response selection is the mental process of choosing representations for appropriate motor behaviors given particular environmental stimuli and one's current task situation and goals. Many cognitive theories of response selection postulate a unitary process. That is, one central response-selection mechanism chooses appropriate responses in most, if not all, task situations. However, neuroscience research shows that neural processing is often localized based on the type of information processed. Our current experiments investigate whether response selection is unitary or stimulus specific by manipulating response-selection difficulty in two functional magnetic resonance imaging experiments using spatial and nonspatial stimuli. The same participants were used in both experiments. We found spatial response selection involves the right prefrontal cortex, the bilateral premotor cortex, and the dorsal parietal cortical regions (precuneus and superior parietal lobule). Nonspatial response selection, conversely, involves the left prefrontal cortex and the more ventral posterior cortical regions (left middle temporal gyrus, left inferior parietal lobule, and right extrastriate cortex). Our brain activation data suggest a cognitive model for response selection in which different brain networks mediate the choice of appropriate responses for different types of stimuli. This model is consistent with behavioral research suggesting that response-selection processing may be more flexible and adaptive than originally proposed.     

EXECUTIVE PERSONALITY TRAITS AND EATING BEHAVIOR

Eating disorders, such as anorexia, bulimia, and binge eating disorder, commonly involve a dysregulation of behavior (e.g., a lack or excess of inhibition and impulsive eating patterns) that is suggestive of prefrontal dysfunction. Functional neuro-imaging studies show that prefrontal-subcortical systems play a role in eating behavior and appetite in healthy individuals, and that people with eating disorders have altered activity in these systems. Eating behavior is often disturbed by illnesses and injuries that impinge upon prefrontal-subcortical systems. This study examined relationships between executive functioning and eating behavior in healthy individuals using validated behavioral rating scales (Frontal Systems Behavior Scale and Eating Inventory). Correlations demonstrated that increased dysexecutive traits were associated with disinhibited eating and greater food cravings. There was also a positive association with cognitive restraint of eating, suggesting that increased compensatory behaviors follow disinhibited eating. These psychometric findings reinforce those of other methodologies, supporting a role for prefrontal systems in eating     

Executive personality traits and eating behavior

Eating disorders, such as anorexia, bulimia, and binge eating disorder, commonly involve a dysregulation of behavior (e.g., a lack or excess of inhibition and impulsive eating patterns) that is suggestive of prefrontal dysfunction. Functional neuro-imaging studies show that prefrontal-subcortical systems play a role in eating behavior and appetite in healthy individuals, and that people with eating disorders have altered activity in these systems. Eating behavior is often disturbed by illnesses and injuries that impinge upon prefrontal-subcortical systems. This study examined relationships between executive functioning and eating behavior in healthy individuals using validated behavioral rating scales (Frontal Systems Behavior Scale and Eating Inventory). Correlations demonstrated that increased dysexecutive traits were associated with disinhibited eating and greater food cravings. There was also a positive association with cognitive restraint of eating, suggesting that increased compensatory behaviors follow disinhibited eating. These psychometric findings reinforce those of other methodologies, supporting a role for prefrontal systems in eating.     

Organization of brainstem behavioral systems

A review of recent literature suggests that the brainstem may play a more fundamental role in the elaboration of adaptive behaviors than has often been assumed. This view is indicated by current reports documenting the substantial behavioral repertoire of decerebrate animals and by the recent findings that electrical stimulation of localized areas in all major levels of the brainstem can induce complex and coordinated behaviors, including eating, grooming and attack. Indeed, behaviors elicited from sites in the caudal brainstem evidence unexpected goal specificity and stimulus control over response topography. Additional neuroanatomical and behavioral data are reviewed which further implicate caudal brainstem networks in process of reward and aversion. From these and other findings it is argued that integrating mechanisms for the expression of many aspects of species-characteristic behaviors are intrinsic to the brainstem. In line with this view, rostral hypothalamic-limbic mechanisms, while perhaps contributing refinement to the integration of behaviors, may best be viewed as phylogenetically newer control mechanisms making the expression of species-characteristic behaviors subordinate to additional class of exteroceptive and interoceptive stimuli.     

A behavioral homeostasis theory of habituation and sensitization: II. Further developments and predictions

Habituation may be viewed as a decremental behavioral change to iterative stimuli of little immediate relevance. It is observed from protozoa to humans, indicating its evolutionary significance. If habituation is interpreted as the process of filtering out unimportant repetitive stimuli, then how should sensitization be interpreted? The 'behavioral homeostasis theory' of these two behaviors is based on the notion that organisms at a high level of 'alertness' prior to experiencing a new iterative stimulus will show a large initial response followed by a decrement (habituation) if the stimulus is of little significance. Conversely, the same organism at a low level of 'alertness' will show a small initial response to the same stimulus followed by an increase in 'alertness' and a larger response to the next stimulus (sensitization) in order to receive enough information to assess its significance. Circadian rhythmicity is hypothesized to play a role in determining 'alertness' to a new iterative stimulus at any given time. The level of responsiveness in initial habituaters and sensitizers, as an asymptote is approached, is a balance between being too 'alert' to an unimportant stimulus and missing other significant stimuli, and being too 'un-alert' and missing a change in the relevance of the present iterative stimulus. The concept of 'behavioral homeostasis' includes behaviors beyond habituation and sensitization across phylogeny. It includes instinctive as well as learned, and group as well as individual behavior. Such behavioral homeostatic processes to optimize detection and assessment of constantly occurring external stimuli are critical for organism survival. Clinical implications of this theory are also examined.     

Nucleo-olivary inhibition balances the interaction between the reactive and adaptive layers in motor control

In the acquisition of adaptive motor reflexes to aversive stimuli, the cerebellar output fulfills a double purpose: it controls a motor response and it relays a sensory prediction. However, the question of how these two apparently incompatible goals might be achieved by the same cerebellar area remains open. Here we propose a solution where the inhibition of the Inferior Olive (IO) by the cerebellar Deep Nuclei (DN) translates the motor command signal into a sensory prediction allowing a single cerebellar area to simultaneously tackle both aspects of the problem: execution and prediction. We demonstrate that having a graded error signal, the gain of the Nucleo-Olivary Inhibition (NOI) balances the generation of the response between the cerebellar and the reflexive controllers or, in other words, between the adaptive and the reactive layers of behavior. Moreover, we show that the resulting system is fully autonomous and can either acquire or erase adaptive responses according to their utility.     

A Sexually Dimorphic Olfactory Neuron Mediates Fixed Action Transition during Courtship Ritual in Drosophila melanogaster

Animals perform a series of actions in a fixed order during ritualistic innate behaviors. Although command neurons and sensory pathways responding to external stimuli that trigger these behaviors have been identified, how each action is induced in a fixed order in response to multimodal sensory stimuli remains unclear. Here, the sexually dimorphic lateral antennal lobe tract projection neuron 4 (lPN4) in male Drosophila melanogaster mediates the expression of a fixed behavioral action pattern at the beginning of the courtship ritual, in which a male taps a female body and then extends a wing unilaterally to produce a courtship song. We found that blocking the synaptic output of lPN4 caused an increase in the ratio of male flies that extended a wing unilaterally without tapping the female body, whereas excitation of lPN4 suppressed the transition from the tapping phase to the unilateral wing extension phase. Real-time calcium imaging showed that lPN4 is activated by a volatile pheromone, palmitoleic acid, whose responses were inhibited by simultaneous gustatory stimulation with female cuticular hydrocarbons, showing the existence of an “AND-gate” for multimodal sensory inputs during male courtship behaviors. These results suggest that the function of lPN4 is to suppress unilateral wing extension while responding to a female smell, which is released by appropriate contact chemosensory inputs received when tapping a female. As the female smell also promotes male courtship behaviors, the olfactory system is ready to simultaneously promote and suppress the progress of courtship actions while responding to a female smell.SIGNIFICANCE STATEMENT Although it has been 80 years since Konrad Lorenz and Niko Tinbergen introduced how multiple acts comprising separate innate behaviors are released in a fixed order according to external stimuli, the neural circuits responsible for such fixed action patterns remain largely unknown. The male courtship behavior of Drosophila melanogaster is a good model to investigate how such a fixed behavioral sequence is determined in the brain. Here, we show that lateral antennal lobe tract projection neuron 4 (lPN4) in D. melanogaster functions as an “AND-gate” for volatile and contact chemosensory inputs, mediating the expression of tapping behaviors before unilateral wing extension during male courtship rituals.     

Development of habituation in the crayfish due to selective weakening of electrical synapses

During posthatching development, transmission becomes substantially reduced at monosynaptic electrical synapses between tactile afferents and the command neuron for caudal tailflip escape responses of the crayfish. The effectiveness of a parallel disynaptic pathway to the same command neuron is unaltered during posthatching growth. In small crayfish both the monosynaptic and disynaptic sensory pathways can elicit command cell action potentials. At this stage, the characteristics of the tailflip neural circuit are evidently controlled by the shorter latency, non-labile monosynaptic pathway. Consequently, tailflips can be reliably elicited in young crayfish, even at brief (2 s) interstimulus intervals. Tailflip responses of large, older crayfish are known to habituate when tactile stimuli are repeated at intervals up to 5 min. This decline in behavioral responsiveness is presumed to be mediated by low frequency synaptic depression (LFD) at first-order synapses of the disynaptic pathway. The lability of these synapses does not change during post-hatching development. Weakening of the monosynaptic pathway may be caused by command cell growth during posthatching development.     

Memories as bifurcations: Realization by collective dynamics of spiking neurons under stochastic inputs

How the neural system proceeds from sensory stimuli to generate appropriate behaviors is a basic question that has not yet been fully answered. In contrast to the conventional viewpoint, in which the external stimulus dominantly drives the response behavior, recent studies have revealed that not only external stimuli, but also intrinsic neural dynamics, contribute to the generation of response behavior. In particular, spontaneous activity, which is neural activity without extensive external stimuli, has been found to exhibit similar patterns to those evoked by external inputs, from time to time. In order to further understand the role of this spontaneous activity on the response, we propose a viewpoint, memories-as-bifurcations, that differs from the traditional memories-as-attractors viewpoint. According to this viewpoint, memory is recalled when spontaneous neural activity is changed to an appropriate output activity upon the application of an input. After reviewing the previous rate-coding model embodying this viewpoint, we employ a model of a spiking neuron network that can embed input/output associations, and study the dynamics of collective neural activity. The organized neural activity, which matched the target pattern, is shown to be generated even under application of stochastic input, while the spontaneous activity, which apparently shows noisy dynamics, is found to exhibit selectively higher similarity with evoked activities corresponding to embedded target patterns. These results suggest that such an intrinsic structure in the spontaneous activity might play a role in generating the higher response. The relevance of these results to biological neural processing is also discussed.     

Context‐dependent coding and gain control in the auditory system of crickets

Sensory systems process stimuli that greatly vary in intensity and complexity. To maintain efficient information transmission, neural systems need to adjust their properties to these different sensory contexts, yielding adaptive or stimulus‐dependent codes. Here, we demonstrated adaptive spectrotemporal tuning in a small neural network, i.e. the peripheral auditory system of the cricket. We found that tuning of cricket auditory neurons was sharper for complex multi‐band than for simple single‐band stimuli. Information theoretical considerations revealed that this sharpening improved information transmission by separating the neural representations of individual stimulus components. A network model inspired by the structure of the cricket auditory system suggested two putative mechanisms underlying this adaptive tuning: a saturating peripheral nonlinearity could change the spectral tuning, whereas broad feed‐forward inhibition was able to reproduce the observed adaptive sharpening of temporal tuning. Our study revealed a surprisingly dynamic code usually found in more complex nervous systems and suggested that stimulus‐dependent codes could be implemented using common neural computations.     

Critical analysis of the neural systems organizing innate fear responses

Unconditioned emotional responses elicited by exposure to a predator have served as the prototypical exemplar for analyses of the behavioral biology of fear-related emotionality. However, the primary research model for the study of fear has involved shock-based cue and context conditioning. While these shock-based models have provided a good understanding of neural systems regulating specific conditioned fear-related behaviors (typically freezing), it is not known if the neural systems underlying an array of defensive responses to innate, unconditioned, painless threat stimuli, and conditioning to these stimuli, are the same as those involved in foot shock and its conditioning sequellae. Recent work involving lesions and c-Fos activation in conjunction with predator or predator odor exposure suggest specific neural systems for response to these, potentially different from the systems outlined in Pavlovian fear conditioning studies. As outlined in the present review, these systems include the medial hypothalamic defensive circuit; specific amygdalar and septo-hippocampal territories, involved in processing, respectively, cues related to the predator presence and environmental contextual analysis; and the periaqueductal gray, known to be critically involved in the expression of predator-induced responses. This information may be potentially important in analysis of defense-related psychopathologies and in the design of therapeutic interventions for them.     

Ventrolateral prefrontal cortex is required for performance of a strategy implementation task but not reinforcer devaluation effects in rhesus monkeys

The ability to apply behavioral strategies to obtain rewards efficiently and make choices based on changes in the value of rewards is fundamental to the adaptive control of behavior. The extent to which different regions of the prefrontal cortex are required for specific kinds of decisions is not well understood. We tested rhesus monkeys with bilateral ablations of the ventrolateral prefrontal cortex on tasks that required the use of behavioral strategies to optimize the rate with which rewards were accumulated, or to modify choice behavior in response to changes in the value of particular rewards. Monkeys with ventrolateral prefrontal lesions were impaired in performing the strategy-based task, but not on value-based decision-making. In contrast, orbital prefrontal ablations produced the opposite impairments in the same tasks. These findings support the conclusion that independent neural systems within the prefrontal cortex are necessary for control of choice behavior based on strategies or on stimulus value.     

Zebrafish (Danio rerio) responds differentially to stimulus fish: the effects of sympatric and allopatric predators and harmless fish

The zebrafish has been an excellent model organism of developmental biology and genetics. Studying its behavior will add to the already strong knowledge of its biology and will strengthen the use of this species in behavior genetics and neuroscience. Anxiety is one of the most problematic human psychiatric conditions. Arguably, it arises as a result of abnormally exaggerated natural fear responses. The zebrafish may be an appropriate model to investigate the biology of fear and anxiety. Fear responses are expressed by animals when exposed to predators, and these responses can be learned or innate. Here we investigated whether zebrafish respond differentially to a natural predator or other fish species upon their first exposure to these fish. Na?ve zebrafish were shown four species of fish chosen based on predatory status (predatory or harmless) and geographical origin (allopatric or sympatric). Our results suggest that na?ve zebrafish respond differentially to the stimulus fish. Particularly interesting is the antipredatory response elicited by the zebrafish's sympatric predator, the Indian Leaf Fish, and the fact that this latter species exhibited almost no predatory attacks. The findings obtained open a new avenue of research into what zebrafish perceive as "dangerous" or fear inducing. They will also allow us to develop fear and anxiety related behavioral test methods with which the contribution of genes to, or the effects of novel anxiolytic substances on these behaviors may be analyzed.     

Lipopolysaccharide does not affect acoustic startle reflex in mice

Bacterial endotoxin (lipopolysaccharide; LPS) evokes in rodents an adaptive sickness behavior. It also produces changes in stress hormones secretion and activity of brain serotonergic and noradrenergic systems that have been implicated in stress responses, fear, and anxiety. Acoustic startle reflex (ASR) is regarded as a protective behavioral response that is enhanced in threatening situations or following an aversive event, and it can be modulated by physiological and emotional state of an animal. Effects of intraperitoneal injections of LPS on ASR, prepulse inhibition (PPI), locomotor activity in open field, and blood plasma corticosterone concentration were studied in lines of mice that display high (HA line) or low (LA line) swim stress-induced analgesia and also differ in emotional behaviors, including the magnitude of ASR. In both lines LPS produced robust sickness behavior, as evidenced by a decrease in locomotion and body weight, and an increase in corticosterone concentration. However, in neither line LPS injections affected responses to acoustic stimuli as assessed by the ASR and PPI magnitudes. The findings suggest that in sickness behavior induced by LPS the protective responses to salient environmental stimuli are not impaired. The significance of this finding for the concept of sickness behavior is discussed.     

Behavioral differences between late preweanling and adult female Sprague-Dawley rat exploration of animate and inanimate stimuli and food

The late preweanling rat has potential as a preclinical model for disorders initially manifested in early childhood that are characterized by dysfunctional interactions with specific stimuli (e.g., obsessive-compulsive disorder and autism). No reports, however, of specific-stimulus exploration in the late preweanling rat are found in the literature. We examined the behavioral responses of normal late preweanling (PND 18-19) and adult rats when presented with exemplars of categorically-varied stimuli, including inanimate objects systematically varied in size and interactive properties, biological stimuli, and food. Preweanlings were faster to initiate specific stimulus exploration and were more interactive with most specific stimuli than adults; the magnitude of these preweanling-adult quantitative differences ranged from fairly small to very large depending upon the stimulus. In contrast, preweanlings were adult-like in their interaction with food and prey. Preweanling response to some stimuli, for example to live pups, was qualitatively different from that of adults; the preweanling behavioral repertoire was characterized by pup-seeking while the adult response was characterized by pup-avoidance. The specific stimulus interactions of preweanlings were less impacted than those of adults by the time of day of testing and placement of a stimulus in an anxiety-provoking location. The impact of novelty was stimulus dependent. The differences in interactions of preweanlings versus adults with specific stimuli suggests that CNS systems underlying these behavior patterns are at different stages of immaturity at PND 18 such that there may be an array of developmental trajectories for various categories of specific stimuli. These data provide a basis for the use of the preweanling as a preclinical model for understanding and medicating human disorders during development that are characterized by dysfunctional interactions with specific stimuli.     

Cross-Hemispheric Complementary Prefrontal Mechanisms during Task Switching under Perceptual Uncertainty

Flexible adaptation to changing environments is a representative executive control function implicated in the frontoparietal network that requires appropriate extraction of goal-relevant information through perception of the external environment. It remains unclear, however, how the flexibility is achieved under situations where goal-relevant information is uncertain. To address this issue, the current study examined neural mechanisms for task switching in which task-relevant information involved perceptual uncertainty. Twenty-eight human participants of both sexes alternated behavioral tasks in which they judged motion direction or color of visually presented colored dot stimuli that moved randomly. Task switching was associated with frontoparietal regions in the left hemisphere, and perception of ambiguous stimuli involved contralateral homologous frontoparietal regions. On the other hand, in stimulus-modality-dependent occipitotemporal regions, task coding information was increased during task switching. Effective connectivity analysis revealed that the frontal regions signaled toward the modality-dependent occipitotemporal regions when a relevant stimulus was more ambiguous, whereas the occipitotemporal regions signaled toward the frontal regions when the stimulus was more distinctive. These results suggest that complementary prefrontal mechanisms in the left and right hemispheres help to achieve a behavioral goal when the external environment involves perceptual uncertainty.SIGNIFICANCE STATEMENT In our daily life, environmental information to achieve a goal is not always certain, but we make judgments in such situations, and change our behavior accordingly. This study examined how the flexibility of behavior is achieved in a situation where goal-relevant information involves perceptual uncertainty. fMRI revealed that the lateral prefrontal cortex (PFC) in the left hemisphere is associated with behavioral flexibility, and the perception of ambiguous stimuli involves the PFC in the right hemisphere. These bilateral PFC signaled to stimulus-modality-dependent occipitotemporal regions, depending on perceptual uncertainty and the task to be performed. These top-down signals supplement task coding in the occipitotemporal regions, and highlight interhemispheric prefrontal mechanisms involved in executive control and perceptual decision-making.     

Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion

The advantages of using predator-related odor stimuli to study emotional responses in laboratory tests depend on whether such stimuli do elicit a relatively complete pattern of emotionality. This has been confirmed for cat fur/skin odor stimuli, which elicit a range of defensive behaviors in rats that may be reduced by anxiolytic drugs, produce residual anxiety-like behavior in the elevated plus maze and support rapid aversive conditioning to the context in which they were encountered. Although the synthetic fox fecal odor, trimethylthiazoline (TMT), elicits avoidance similar to that seen in response to cat fur/skin odor, this avoidance does not respond to anxiolytic drugs. In addition, TMT does not produce residual anxiety-like behaviors in the elevated plus maze, nor does it support conditioning.

As natural cat feces also elicit avoidance but fail to support conditioning, it is possible that the ability of a predator-related odor to serve as an effective unconditioned stimulus (US) relates to its predictive status with reference to the actual presence of the predator. Avoidance per se may reflect that a stimulus is aversive but not necessarily capable of eliciting an emotional response. This view is consonant with findings in a Mouse Defense Test Battery (MDTB) measuring a wide range of defensive responses to predator exposure. A contextual defense measure that may reflect either conditioned or residual but unconditioned emotional responses was almost never reduced by drug effects unless these also reduced risk assessment or defensive threat/attack measures. However, reductions in contextual defense without changes in flight/avoidance measures were much more common.

These findings suggest that flight/avoidance, although it obviously may occur as one component of a full pattern of defensive and emotional behaviors, is also somewhat separable from the others. When—as appears to be the case with TMT—it is the major or perhaps only consistent defensive behavior elicited, this may reflect a stimulus that is aversive or noxious but with little ability to predict the presence of threat or danger. That such stimuli fail to support rapid aversive conditioning suggests the need for a reanalysis of the characteristics required for an effective aversive US.     

Fear-like biochemical and behavioral responses in rats to the predator odor,TMT, are dependent on the exposure environment

Several laboratories have reported that exposure to predator odor can result in stress-like effects in rodents. While some laboratories have reported fear-like alterations in behavior, other laboratories, including our own, have failed to consistently observe fearful behaviors in rats exposed to the predator odor TMT. One potential contributing factor to this discrepancy is the handling of the rat and its test environment. In the current report, we examine biochemical, endocrinological, and behavioral effects of TMT in two distinct open fields: one small, familiar, and dimly lit, while the other was large, novel, and brightly lit. Only exposure to TMT in the large, novel open field resulted in fearful behavior; however, no increase in dopamine turnover was noted compared to no odor and control odor rats. As expected, the different open fields resulted in some biochemical and behavioral differences, including more horizontal locomotion and less grooming, higher serum corticosterone, and increased dopamine turnover in the ventral prefrontal cortex in the large open field. Finally, compared to the same open field controls, TMT exposure elevated rat serum corticosterone levels in both open fields and dopamine turnover in the dorsal and ventral medial prefrontal cortex and amygdala of rats only in the small, familiar open field. These results indicate that the TMT-induced biochemical activation of may occur without detectable fearful behaviors and may indicate a mechanism that prepares the animal for the expression of a fearful response if additional provocative stimuli are present.     

Bimodal optomotor response to plaids in blowflies: mechanisms of component selectivity and evidence for pattern selectivity

Many animals estimate their self-motion and the movement of external objects by exploiting panoramic patterns of visual motion. To probe how visual systems process compound motion patterns, superimposed visual gratings moving in different directions, plaid stimuli, have been successfully used in vertebrates. Surprisingly, nothing is known about how visually guided insects process plaids. Here, we explored in the blowfly how the well characterized yaw optomotor reflex and the activity of identified visual interneurons depend on plaid stimuli. We show that contrary to previous expectations, the yaw optomotor reflex shows a bimodal directional tuning for certain plaid stimuli. To understand the neural correlates of this behavior, we recorded the responses of a visual interneuron supporting the reflex, the H1 cell, which was also bimodally tuned to the plaid direction. Using a computational model, we identified the essential neural processing steps required to capture the observed response properties. These processing steps have functional parallels with mechanisms found in the primate visual system, despite different biophysical implementations. By characterizing other visual neurons supporting visually guided behaviors, we found responses that ranged from being bimodally tuned to the stimulus direction (component-selective), to responses that appear to be tuned to the direction of the global pattern (pattern-selective). Our results extend the current understanding of neural mechanisms of motion processing in insects, and indicate that the fly employs a wider range of behavioral responses to multiple motion cues than previously reported.