Looming Stimuli Research Articles

Background visual motion affects responses of an insect motion-sensitive neuron to objects deviating from a collision course.

Stimulus complexity affects the response of looming sensitive neurons in a variety of animal taxa. The Lobula Giant Movement Detector/Descending Contralateral Movement Detector (LGMD/DCMD) pathway is well‐characterized in the locust visual system. It responds to simple objects approaching on a direct collision course (i.e., looming) as well as complex motion defined by changes in stimulus velocity, trajectory, and transitions, all of which are affected by the presence or absence of background visual motion. In this study, we focused on DCMD responses to objects transitioning away from a collision course, which emulates a successful locust avoidance behavior. We presented each of 20 locusts with a sequence of complex three‐dimensional visual stimuli in simple, scattered, and progressive flow field backgrounds while simultaneously recording DCMD activity extracellularly. DCMD responses to looming stimuli were generally characteristic irrespective of stimulus background. However, changing background complexity affected, peak firing rates, peak time, and caused changes in peak rise and fall phases. The DCMD response to complex object motion also varied with the azimuthal approach angle and the dynamics of object edge expansion. These data fit with an existing correlational model that relates expansion properties to firing rate modulation during trajectory changes.

Structure and Function of Dragonfly Looming‐Sensitive Neurons

In this project, I aim to identify specific neurons in the dragonfly brain that respond selectively to looming stimuli. In the dragonfly nerve cord, there are large visual neurons, called Target Selective Descending Neurons (TSDNs). These neurons respond selectively to small moving stimuli, which mimic the movements of dragonfly prey. The response of these neurons is the steering movement of the dragonfly's wings, allowing them to predict the location of their prey for accurate interception. A subset of the TSDNs show large and precisely timed responses to the expanding image of an approaching object. I will be studying these “looming‐sensitive” neurons, researching what visual information they are sending to the flight system. This material will allow for the analysis of the anatomical structure in the dragonfly brain. The visual responses of these dragonflies suggests that the looming‐sensitive neurons are the specific TSDNs called MDT3 and DIT3, but in order to confirm this prediction, we must visualize the anatomy of the brain. With the use of a dye called Lucifer yellow, we can trace the response of the looming stimuli to a specific area of the brain. By injecting the dye with a recording microelectrode, we can positively identify these specific neurons.Support or Funding InformationUnion College Undergraduate Research Committee

Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

Escape behaviors deliver organisms away from imminent catastrophe. Here, we characterize behavioral responses of freely swimming larval zebrafish to looming visual stimuli simulating predators. We report that the visual system alone can recruit lateralized, rapid escape motor programs, similar to those elicited by mechanosensory modalities. Two-photon calcium imaging of retino-recipient midbrain regions isolated the optic tectum as an important center processing looming stimuli, with ensemble activity encoding the critical image size determining escape latency. Furthermore, we describe activity in retinal ganglion cell terminals and superficial inhibitory interneurons in the tectum during looming and propose a model for how temporal dynamics in tectal periventricular neurons might arise from computations between these two fundamental constituents. Finally, laser ablations of hindbrain circuitry confirmed that visual and mechanosensory modalities share the same premotor output network. We establish a circuit for the processing of aversive stimuli in the context of an innate visual behavior.

Commentary: Burst Firing in a Motion-Sensitive Neural Pathway Correlates with Expansion Properties of Looming Objects That Evoke Avoidance Behaviors.

Commentary: Burst Firing in a Motion-Sensitive Neural Pathway Correlates with Expansion Properties of Looming Objects That Evoke Avoidance Behaviors.

Object approach computation by a giant neuron and its relationship with the speed of escape in the crab Neohelice.

Upon detection of an approaching object, the crab Neohelice granulata continuously regulates the direction and speed of escape according to ongoing visual information. These visuomotor transformations are thought to be largely accounted for by a small number of motion-sensitive giant neurons projecting from the lobula (third optic neuropil) towards the supraesophageal ganglion. One of these elements, the monostratified lobula giant neuron of type 2 (MLG2), proved to be highly sensitive to looming stimuli (a 2D representation of an object approach). By performing in vivo intracellular recordings, we assessed the response of the MLG2 neuron to a variety of looming stimuli representing objects of different sizes and velocities of approach. This allowed us to: (1) identify some of the physiological mechanisms involved in the regulation of the MLG2 activity and test a simplified biophysical model of its response to looming stimuli; (2) identify the stimulus optical parameters encoded by the MLG2 and formulate a phenomenological model able to predict the temporal course of the neural firing responses to all looming stimuli; and (3) incorporate the MLG2-encoded information of the stimulus (in terms of firing rate) into a mathematical model able to fit the speed of the escape run of the animal. The agreement between the model predictions and the actual escape speed measured on a treadmill for all tested stimuli strengthens our interpretation of the computations performed by the MLG2 and of the involvement of this neuron in the regulation of the animal's speed of run while escaping from objects approaching with constant speed.

Burst Firing in a Motion-Sensitive Neural Pathway Correlates with Expansion Properties of Looming Objects that Evoke Avoidance Behaviors.

The locust visual system contains a well-defined motion-sensitive pathway that transfers visual input to motor centers involved in predator evasion and collision avoidance. One interneuron in this pathway, the descending contralateral movement detector (DCMD), is typically described as using rate coding; edge expansion of approaching objects causes an increased rate of neuronal firing that peaks after a certain retinal threshold angle is exceeded. However, evidence of intrinsic DCMD bursting properties combined with observable oscillations in mean firing rates and tight clustering of spikes in raw traces, suggest that bursting may be important for motion detection. Sensory neuron bursting provides important timing information about dynamic stimuli in many model systems, yet no studies have rigorously investigated if bursting occurs in the locust DCMD during object approach. We presented repetitions of 30 looming stimuli known to generate behavioral responses to each of 20 locusts in order to identify and quantify putative bursting activity in the DCMD. Overall, we found a bimodal distribution of inter-spike intervals (ISI) with peaks of more frequent and shorter ISIs occurring from 1–8 ms and longer less frequent ISIs occurring from 40–50 ms. Subsequent analysis identified bursts and isolated single spikes from the responses. Bursting frequency increased in the latter phase of an approach and peaked at the time of collision, while isolated spiking was predominant during the beginning of stimulus approach. We also found that the majority of inter-burst intervals (IBIs) occurred at 40–50 ms (or 20–25 bursts/s). Bursting also occurred across varied stimulus parameters and suggests that burst timing may be a key component of looming detection. Our findings suggest that the DCMD uses two modes of coding to transmit information about looming stimuli and that these modes change dynamically with a changing stimulus at a behaviorally-relevant time.

Condition-dependent physiological and behavioural responses to anthropogenic noise

Anthropogenic (man-made) noise, a global pollutant of international concern, is known to affect the physiology and behaviour of a range of organisms. However, experimental studies have tended to focus on trait means; intra-population variation in responses are likely, but have rarely been explored. Here we use established experimental methods to demonstrate a condition-dependent effect of additional noise. We show that juvenile European eels (Anguilla anguilla) in good condition do not respond differently to playbacks of ambient coastal noise and coastal noise with passing ships. By contrast, the additional noise of ship passes caused an increase in ventilation rate and a decrease in startling to a looming predatory stimulus in poor condition eels. Intra-population variation in responses to noise has important implications both for population dynamics and the planning of mitigation measures.

Looming sensitive cortical regions without V1 input: evidence from a patient with bilateral cortical blindness.

Fast and automatic behavioral responses are required to avoid collision with an approaching stimulus. Accordingly, looming stimuli have been found to be highly salient and efficient attractors of attention due to the implication of potential collision and potential threat. Here, we address the question of whether looming motion is processed in the absence of any functional primary visual cortex and consequently without awareness. For this, we investigated a patient (TN) suffering from complete, bilateral damage to his primary visual cortex. Using an fMRI paradigm, we measured TN's brain activation during the presentation of looming, receding, rotating, and static point lights, of which he was unaware. When contrasted with other conditions, looming was found to produce bilateral activation of the middle temporal areas, as well as the superior temporal sulcus and inferior parietal lobe (IPL). The latter are generally thought to be involved in multisensory processing of motion in extrapersonal space, as well as attentional capture and saliency. No activity was found close to the lesioned V1 area. This demonstrates that looming motion is processed in the absence of awareness through direct subcortical projections to areas involved in multisensory processing of motion and saliency that bypass V1.

Fear learning through the two visual systems, a commentary on: "A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice".

Fear learning through the two visual systems, a commentary on: "A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice".

Evolutionary-based threat modulates perception of looming visual stimuli in human infants

Research with both human and non-human primates suggests that the visual system exhibits specialized processing of evolutionary-based threats. Adult humans (Ohman & Mineka, 2001) and monkeys (Shibasaki & Kawai, 2009) detect images of snakes and spiders faster than neutral images during visual search. Moreover, human infants orient more quickly to a threatening compared to a non-threatening image, when presented with two images simultaneously (e.g., a snake and a flower). Taken together, these results suggest a perceptual bias for threat that exists prior to the development of overt fear and that may be innate in human development (LoBue & DeLoache, 2009). Yet differential orientating in infants and visual search paradigms typically used with adult humans and nonhuman primates are heavily dependent on contrast images; there are also influences of stimulus familiarity and strategic processes (Frischen, Eastwood, & Smilek, 2008), raising questions about the mechanisms underlying the perceptual basis of sensitivity to evolutionarily-based threats. The current study extends existing research by examining infants’ defensive blinking in a visual looming paradigm. We tested 60 6- to 12- month-old infants. Infants were presented with images of snakes, spiders, rabbits, and butterflies. Each image loomed towards them, one at a time, at six velocities, creating different time-to-contacts (TTCs). As in previous studies (Kayed & van der Meer, 2000), analyses revealed that infants’ blinks scaled according to TTC. We also found that defensive blinking was modulated by the threat value of stimuli. Infants blinked sooner to snakes and spiders compared to rabbits and butterflies at all TTCs (ps < .05). Critically, this effect cannot be accounted for by familiarity, as infants looked longer overall to the non-threatening than threatening animals (p < .05). That infants’ defensive blinks were modulated by the threat value of the animal provides evidence for specialized spatiotemporal perceptual processing of evolutionary-based threat. Meeting abstract presented at VSS 2015

Threat modulates neural responses to looming visual stimuli.

Objects on a collision course with an observer produce a specific pattern of optical expansion on the retina known as looming, which in theory exactly specifies the time-to-collision (TTC) of approaching objects. It was recently demonstrated that the affective content of looming stimuli influences perceived TTC, with threatening objects judged as approaching sooner than non-threatening objects. Here, the neural mechanisms by which perceived threat modulates spatiotemporal perception were investigated. Participants judged the TTC of threatening (snakes, spiders) or non-threatening (butterflies, rabbits) stimuli, which expanded in size at a rate indicating one of five TTCs. Visual-evoked potentials (VEPs) and oscillatory neural responses measured with electroencephalography were analysed. The arrival time of threatening stimuli was underestimated compared with non-threatening stimuli, though an interaction suggested that this underestimation was not constant across TTCs. Further, both speed of approach and threat modulated both VEPs and oscillatory responses. Speed of approach modulated the N1 parietal and oscillations in the beta band. Threat modulated several VEP components (P1, N1 frontal, N1 occipital, early posterior negativity and late positive potential) and oscillations in the alpha and high gamma band. The results for the high gamma band suggest an interaction between these two factors. Previous evidence suggests that looming stimuli activate sensorimotor areas, even in the absence of an intended action. The current results show that threat disrupts the synchronization over the sensorimotor areas that are likely activated by the presentation of a looming stimulus.

A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish

Avoiding the strike of an approaching predator requires rapid visual detection of a looming object, followed by a directed escape maneuver. While looming-sensitive neurons have been discovered in various animal species, the relative importance of stimulus features that are extracted by the visual system is still unclear. Furthermore, the neural mechanisms that compute object approach are largely unknown. We found that a virtual looming stimulus, i.e., a dark expanding disk on a bright background, reliably evoked rapid escape movements. Related stimuli, such as dimming, receding, or bright looming objects, were substantially less effective, and angular size was a critical determinant of escape initiation. Two-photon calcium imaging in retinal ganglion cell (RGC) axons revealed three retinorecipient areas that responded robustly to looming stimuli. One of these areas, the optic tectum, is innervated by a subset of RGC axons that respond selectively to looming stimuli. Laser-induced lesions of the tectal neuropil impaired the behavior. Our findings demonstrate a visually mediated escape behavior in zebrafish larvae exposed to objects approaching on a collision course. This response is sensitive to spatiotemporal parameters of the looming stimulus. Our data indicate that a subset of RGC axons within the tectum responds selectively to features of looming stimuli and that this input is necessary for visually evoked escape.

Processing of visually evoked innate fear by a non-canonical thalamic pathway.

The ability of animals to respond to life-threatening stimuli is essential for survival. Although vision provides one of the major sensory inputs for detecting threats across animal species, the circuitry underlying defensive responses to visual stimuli remains poorly defined. Here, we investigate the circuitry underlying innate defensive behaviours elicited by predator-like visual stimuli in mice. Our results demonstrate that neurons in the superior colliculus (SC) are essential for a variety of acute and persistent defensive responses to overhead looming stimuli. Optogenetic mapping revealed that SC projections to the lateral posterior nucleus (LP) of the thalamus, a non-canonical polymodal sensory relay, are sufficient to mimic visually evoked fear responses. In vivo electrophysiology experiments identified a di-synaptic circuit from SC through LP to the lateral amygdale (Amg), and lesions of the Amg blocked the full range of visually evoked defensive responses. Our results reveal a novel collicular–thalamic–Amg circuit important for innate defensive responses to visual threats.

Impact prediction by looming visual stimuli enhances tactile detection.

From an ecological point of view, approaching objects are potentially more harmful than receding objects. A predator, a dominant conspecific, or a mere branch coming up at high speed can all be dangerous if one does not detect them and produce the appropriate escape behavior fast enough. And indeed, looming stimuli trigger stereotyped defensive responses in both monkeys and human infants. However, while the heteromodal somatosensory consequences of visual looming stimuli can be fully predicted by their spatiotemporal dynamics, few studies if any have explored whether visual stimuli looming toward the face predictively enhance heteromodal tactile sensitivity around the expected time of impact and at its expected location on the body. In the present study, we report that, in addition to triggering a defensive motor repertoire, looming stimuli toward the face provide the nervous system with predictive cues that enhance tactile sensitivity on the face. Specifically, we describe an enhancement of tactile processes at the expected time and location of impact of the stimulus on the face. We additionally show that a looming stimulus that brushes past the face also enhances tactile sensitivity on the nearby cheek, suggesting that the space close to the face is incorporated into the subjects' body schema. We propose that this cross-modal predictive facilitation involves multisensory convergence areas subserving the representation of a peripersonal space and a safety boundary of self.

GABAergic neurotransmission and retinal ganglion cell function.

Ganglion cells are the output retinal neurons that convey visual information to the brain. There are ~20 different types of ganglion cells, each encoding a specific aspect of the visual scene as spatial and temporal contrast, orientation, direction of movement, presence of looming stimuli; etc. Ganglion cell functioning depends on the intrinsic properties of ganglion cell's membrane as well as on the excitatory and inhibitory inputs that these cells receive from other retinal neurons. GABA is one of the most abundant inhibitory neurotransmitters in the retina. How it modulates the activity of different types of ganglion cells and what is its significance in extracting the basic features from visual scene are questions with fundamental importance in visual neuroscience. The present review summarizes current data concerning the types of membrane receptors that mediate GABA action in proximal retina; the effects of GABA and its antagonists on the ganglion cell light-evoked postsynaptic potentials and spike discharges; the action of GABAergic agents on centre-surround organization of the receptive fields and feature related ganglion cell activity. Special emphasis is put on the GABA action regarding the ON-OFF and sustained-transient ganglion cell dichotomy in both nonmammalian and mammalian retina.

Suppressed visual looming stimuli are not integrated with auditory looming signals: Evidence from continuous flash suppression.

Previous studies using binocular rivalry have shown that signals in a modality other than the visual can bias dominance durations depending on their congruency with the rivaling stimuli. More recently, studies using continuous flash suppression (CFS) have reported that multisensory integration influences how long visual stimuli remain suppressed. In this study, using CFS, we examined whether the contrast thresholds for detecting visual looming stimuli are influenced by a congruent auditory stimulus. In Experiment 1, we show that a looming visual stimulus can result in lower detection thresholds compared to a static concentric grating, but that auditory tone pips congruent with the looming stimulus did not lower suppression thresholds any further. In Experiments 2, 3, and 4, we again observed no advantage for congruent multisensory stimuli. These results add to our understanding of the conditions under which multisensory integration is possible, and suggest that certain forms of multisensory integration are not evident when the visual stimulus is suppressed from awareness using CFS.

Background complexity affects response of a looming-sensitive neuron to object motion.

An increasing number of studies show how stimulus complexity affects the responses of looming-sensitive neurons across multiple animal taxa. Locusts contain a well-described, descending motion-sensitive pathway that is preferentially looming sensitive. However, the lobula giant movement detector/descending contralateral movement detector (LGMD/DCMD) pathway responds to more than simple objects approaching at constant, predictable trajectories. In this study, we presented Locusta migratoria with a series of complex three-dimensional visual stimuli presented while simultaneously recording DCMD activity extracellularly. In addition to a frontal looming stimulus, we used a combination of compound trajectories (nonlooming transitioning to looming) presented at different velocities and onto a simple, scattered, or progressive flow field background. Regardless of stimulus background, DCMD responses to looming were characteristic and related to previously described effects of azimuthal approach angle and velocity of object expansion. However, increasing background complexity caused reduced firing rates, delayed peaks, shorter rise phases, and longer fall phases. DCMD responded to transitions to looming with a characteristic drop in a firing rate that was relatively invariant across most stimulus combinations and occurred regardless of stimulus background. Spike numbers were higher in the presence of the scattered background and reduced in the flow field background. We show that DCMD response time to a transition depends on unique expansion parameters of the moving stimulus irrespective of background complexity. Our results show how background complexity shapes DCMD responses to looming stimuli, which is explained within a behavioral context.

Visual Cortex Modulates the Magnitude but Not the Selectivity of Looming-Evoked Responses in the Superior Colliculus of Awake Mice

Neural circuits in the brain often receive inputs from multiple sources, such as the bottom-up input from early processing stages and the top-down input from higher-order areas. Here we study the function of top-down input in the mouse superior colliculus (SC), which receives convergent inputs from the retina and visual cortex. Neurons in the superficial SC display robust responses and speed tuning to looming stimuli that mimic approaching objects. The looming-evoked responses are reduced by almost half when the visual cortex is optogenetically silenced in awake, but not in anesthetized, mice. Silencing the cortex does not change the looming speed tuning of SC neurons, or the response time course, except at the lowest tested speed. Furthermore, the regulation of SC responses by the corticotectal input is organized retinotopically. This effect we revealed may thus provide a potential substrate for the cortex, an evolutionarily new structure, to modulate SC-mediated visual behaviors.

Excitation and inhibition in recurrent networks mediate collision avoidance in Xenopus tadpoles.

Information processing in the vertebrate brain is thought to be mediated through distributed neural networks, but it is still unclear how sensory stimuli are encoded and detected by these networks, and what role synaptic inhibition plays in this process. Here we used a collision avoidance behavior in Xenopus tadpoles as a model for stimulus discrimination and recognition. We showed that the visual system of the tadpole is selective for behaviorally relevant looming stimuli, and that the detection of these stimuli first occurs in the optic tectum. By comparing visually guided behavior, optic nerve recordings, excitatory and inhibitory synaptic currents, and the spike output of tectal neurons, we showed that collision detection in the tadpole relies on the emergent properties of distributed recurrent networks within the tectum. We found that synaptic inhibition was temporally correlated with excitation, and did not actively sculpt stimulus selectivity, but rather it regulated the amount of integration between direct inputs from the retina and recurrent inputs from the tectum. Both pharmacological suppression and enhancement of synaptic inhibition disrupted emergent selectivity for looming stimuli. Taken together these findings suggested that, by regulating the amount of network activity, inhibition plays a critical role in maintaining selective sensitivity to behaviorally-relevant visual stimuli.

A spike-timing mechanism for action selection

We discovered a bimodal behavior in the genetically tractable organism Drosophila melanogaster that allowed us to directly probe the neural mechanisms of an action selection process. When confronted by a predator-mimicking looming stimulus, a fly responds with either a long-duration escape behavior sequence that initiates stable flight or a distinct, short-duration sequence that sacrifices flight stability for speed. Intracellular recording of the descending giant fiber (GF) interneuron during head-fixed escape revealed that GF spike timing relative to parallel circuits for escape actions determined which of the two behavioral responses was elicited. The process was well described by a simple model in which the GF circuit has a higher activation threshold than the parallel circuits, but can override ongoing behavior to force a short takeoff. Our findings suggest a neural mechanism for action selection in which relative activation timing of parallel circuits creates the appropriate motor output.