Bilateral interactions of optic-flow sensitive neurons coordinate course control in flies.

Animals rely on compensatory actions to maintain stability and navigate their environment efficiently. These actions depend on global visual motion cues known as optic-flow. While the optomotor response has been the traditional focus for studying optic-flow compensation in insects, its simplicity has been insufficient to determine the role of the intricate optic-flow processing network involved in visual course control. Here, we reveal a series of course control behaviours in Drosophila and link them to specific neural circuits. We show that bilateral electrical coupling of optic-flow-sensitive neurons in the fly's lobula plate are required for a proper course control. This electrical interaction works alongside chemical synapses within the HS-H2 network to control the dynamics and direction of turning behaviours. Our findings reveal how insects use bilateral motion cues for navigation, assigning a new functional significance to the HS-H2 network and suggesting a previously unknown role for gap junctions in non-linear operations.

Precision and temporal dynamics in heading perception assessed by continuous psychophysics.

It is a well-established finding that more informative optic flow (e.g., faster, denser, or presented over a larger portion of the visual field) yields decreased variability in heading judgements. Current models of heading perception further predict faster processing under such circumstances, which has, however, not been supported empirically so far. In this study, we validate a novel continuous psychophysics paradigm by replicating the effect of the speed and density of optic flow on variability in performance, and we investigate how these manipulations affect the temporal dynamics. To this end, we tested 30 participants in a continuous psychophysics paradigm administered in Virtual Reality. We immersed them in a simple virtual environment where they experienced four 90-second blocks of optic flow where their linear heading direction (no simulated rotation) at any given moment was determined by a random walk. We asked them to continuously indicate with a joystick the direction in which they perceived themselves to be moving. In each of the four blocks they experienced a different combination of simulated self-motion speeds (SLOW and FAST) and density of optic flow (SPARSE and DENSE). Using a Cross-Correlogram Analysis, we determined that participants reacted faster and displayed lower variability in their performance in the FAST and DENSE conditions than in the SLOW and SPARSE conditions, respectively. Using a Kalman Filter-based analysis approach, we found a similar pattern, where the fitted perceptual noise parameters were higher for SLOW and SPARSE. While replicating previous results on variability, we show that more informative optic flow can speed up heading judgements, while at the same time validating a continuous psychophysics as an efficient method for studying heading perception.

Optokinetic response in D. melanogaster reveals the nature of common repellent odorants.

Animals' ability to orient and navigate relies on selecting an appropriate motor response based on the perception and integration of the environmental information. This is the case, for instance, of the optokinetic response (OKR) in Drosophila melanogaster, where optic flow visual stimulation modulates head movements. Despite a large body of literature on the OKR, there is still a limited understanding, in flies, of the impact on OKR of concomitant, and potentially conflicting, inputs. To evaluate the impact of this multimodal integration, we combined in D. melanogaster, while flying in a tethered condition, the optic flow stimulation leading to OKR with the simultaneous presentation of olfactory cues, based on repellent or masking compounds typically used against noxious insect species. First, this approach allowed us to directly quantify the effect of several substances and of their concentration on the dynamics of the flies' OKR in response to moving gratings by evaluating the number of saccades and the velocity of the slow phase. Subsequently, this analysis was capable of easily revealing the actual effect, i.e. masking vs. repellent, of the compound tested. In conclusion, we show that D. melanogaster, a cost-affordable species, represents a viable option for studying the effects of several compounds on the navigational abilities of insects.

A Bayesian inference model can predict the effects of attention on the serial dependence in heading estimation from optic flow.

It has been demonstrated that observers can accurately estimate their self-motion direction (i.e., heading) from optic flow, which can be affected by attention. However, it remains unclear how attention affects the serial dependence in the estimation. In the current study, participants conducted two experiments. The results showed that the estimation accuracy decreased when attentional resources allocated to the heading estimation task were reduced. Additionally, the estimates of currently presented headings were biased toward the headings of previously seen headings, showing serial dependence. Especially, this effect decreased (increased) when the attentional resources allocated to the previously (currently) seen headings were reduced. Furthermore, importantly, we developed a Bayesian inference model, which incorporated attention-modulated likelihoods and qualitatively predicted changes in the estimation accuracy and serial dependence. In summary, the current study shows that attention affects the serial dependence in heading estimation from optic flow and reveals the Bayesian computational mechanism behind the heading estimation.

Tunnel motion: Pupil dilations to optic flow within illusory dark holes.

We showed to the same observers both dynamic and static 2D patterns that can both evoke distinctive perceptions of motion or optic flow, as if moving in a tunnel or into a dark hole. At all times pupil diameters were monitored with an infrared eye tracker. We found a converging set of results indicating stronger pupil dilations to expansive growth of shapes or optic flows evoking a forward motion into a dark tunnel. Multiple regression analyses showed that the pupil responses to the illusory expanding black holes of static patterns were predicted by the individuals' pupil response to optic flows showing spiraling motion or "free fall" into a black hole. Also, individuals' pupil responses to spiraling motion into dark tunnels predicted the individuals' sense of illusory expansion with the static, illusory expanding, dark holes. This correspondence across individuals between their pupil responses to both dynamic and static, illusory expanding, holes suggests that these percepts reflect a common perceptual mechanism, deriving motion from 2D scenes, and that the observers' pupil adjustments reflect the direction and strength of motion they perceive and the expected outcome of an increase in darkness.

Rats rely on airflow cues for self-motion perception.

Self-motion perception is a vital skill for all species. It is an inherently multisensory process that combines inertial (body-based) and relative (with respect to the environment) motion cues. Although extensively studied in human and non-human primates, there is currently no paradigm to test self-motion perception in rodents using both inertial and relative self-motion cues. We developed a novel rodent motion simulator using two synchronized robotic arms to generate inertial, relative, or combined (inertial and relative) cues of self-motion. Eight rats were trained to perform a task of heading discrimination, similar to the popular primate paradigm. Strikingly, the rats relied heavily on airflow for relative self-motion perception, with little contribution from the (limited) optic flow cues provided-performance in the dark was almost as good. Relative self-motion (airflow) was perceived with greater reliability vs. inertial. Disrupting airflow, using a fan or windshield, damaged relative, but not inertial, self-motion perception. However, whiskers were not needed for this function. Lastly, the rats integrated relative and inertial self-motion cues in a reliability-based (Bayesian-like) manner. These results implicate airflow as an important cue for self-motion perception in rats and provide a new domain to investigate the neural bases of self-motion perception and multisensory processing in awake behaving rodents.

Control and recalibration of path integration in place cells using optic flow.

Hippocampal place cells are influenced by both self-motion (idiothetic) signals and external sensory landmarks as an animal navigates its environment. To continuously update a position signal on an internal 'cognitive map', the hippocampal system integrates self-motion signals over time, a process that relies on a finely calibrated path integration gain that relates movement in physical space to movement on the cognitive map. It is unclear whether idiothetic cues alone, such as optic flow, exert sufficient influence on the cognitive map to enable recalibration of path integration, or if polarizing position information provided by landmarks is essential for this recalibration. Here, we demonstrate both recalibration of path integration gain and systematic control of place fields by pure optic flow information in freely moving rats. These findings demonstrate that the brain continuously rebalances the influence of conflicting idiothetic cues to fine-tune the neural dynamics of path integration, and that this recalibration process does not require a top-down, unambiguous position signal from landmarks.

Detection method for unrecognized spatial disorientation based on optical flow stimuli.

BACKGROUND: Flight accidents caused by spatial disorientation (SD) greatly affect flight safety. OBJECTIVE: Few studies have been devoted to the evaluation of SD. METHODS: 10 pilots and 10 non-pilots were recruited for the experimental induction of SD. Videos for giving optical flow stimuli were played at two different flow speeds to induce SD. Subjective judgment and center of foot pressure (CoP) data were collected from the tests. The data were combined to determine the occurrence of SD and analyze the SD types. RESULTS: The number of self-reported SD events was slightly smaller in the pilots than in the non-pilots. The average upper bound of the confidence interval for the standard deviation of CoP was 0.32 ± 0.09 cm and 0.38 ± 0.12 cm in the pilots and non-pilots, respectively. This indicator was significantly lower in the pilots than in the non-pilots (P= 0.03). The success rate of the experimental induction of unrecognized SD was 26.7% and 45.0% in the pilots and non-pilots, respectively. CONCLUSION: The method offered a new to analyze unrecognized SD. We could determine the occurrence unrecognized SD. This is an essential means of reducing flight accidents caused by unrecognized SD.

Common and specific activations supporting optic flow processing and navigation as revealed by a meta-analysis of neuroimaging studies.

Optic flow provides useful information in service of spatial navigation. However, whether brain networks supporting these two functions overlap is still unclear. Here we used Activation Likelihood Estimation (ALE) to assess the correspondence between brain correlates of optic flow processing and spatial navigation and their specific neural activations. Since computational and connectivity evidence suggests that visual input from optic flow provides information mainly during egocentric navigation, we further tested the correspondence between brain correlates of optic flow processing and that of both egocentric and allocentric navigation. Optic flow processing shared activation with egocentric (but not allocentric) navigation in the anterior precuneus, suggesting its role in providing information about self-motion, as derived from the analysis of optic flow, in service of egocentric navigation. We further documented that optic flow perception and navigation are partially segregated into two functional and anatomical networks, i.e., the dorsal and the ventromedial networks. Present results point to a dynamic interplay between the dorsal and ventral visual pathways aimed at coordinating visually guided navigation in the environment.

Jumping and leaping estimations using optic flow.

Optic flow provides information on movement direction and speed during locomotion. Changing the relationship between optic flow and walking speed via training has been shown to influence subsequent distance and hill steepness estimations. Previous research has shown that experience with slow optic flow at a given walking speed was associated with increased effort and distance overestimation in comparison to experiencing with fast optic flow at the same walking speed. Here, we investigated whether exposure to different optic flow speeds relative to gait influences perceptions of leaping and jumping ability. Participants estimated their maximum leaping and jumping ability after exposure to either fast or moderate optic flow at the same walking speed. Those calibrated to fast optic flow estimated farther leaping and jumping abilities than those calibrated to moderate optic flow. Findings suggest that recalibration between optic flow and walking speed may specify an action boundary when calibrated or scaled to actions such as leaping, and possibly, the manipulation of optic flow speed has resulted in a change in the associated anticipated effort for walking a prescribed distance, which in turn influence one's perceived action capabilities for jumping and leaping.

The influence of spontaneous and visual activity on the development of direction selectivity maps in mouse retina.

In mice, retinal direction selectivity is organized in a map that aligns to the body and gravitational axes of optic flow, and little is known about how this map develops. We find direction selectivity maps are largely present at eye opening and develop normally in the absence of visual experience. Remarkably, in mice lacking the beta2 subunit of neuronal nicotinic acetylcholine receptors (ß2-nAChR-KO), which exhibit drastically reduced cholinergic retinal waves in the first postnatal week, selectivity to horizontal motion is absent while selectivity to vertical motion remains. We tested several possible mechanisms that could explain the loss of horizontal direction selectivity in ß2-nAChR-KO mice (wave propagation bias, FRMD7 expression, starburst amacrine cell morphology), but all were found to be intact when compared with WT mice. This work establishes a role for retinal waves in the development of asymmetric circuitry that mediates retinal direction selectivity via an unknown mechanism.

Response properties of optic flow neurons in the accessory optic system of hummingbirds versus zebra finches and pigeons.

Optokinetic responses function to maintain retinal image stabilization by minimizing optic flow that occurs during self-motion. The hovering ability of hummingbirds is an extreme example of this behavior. Optokinetic responses are mediated by direction-selective neurons with large receptive fields in the accessory optic system (AOS) and pretectum. Recent studies in hummingbirds showed that, compared with other bird species, 1) the pretectal nucleus lentiformis mesencephali (LM) is hypertrophied, 2) LM has a unique distribution of direction preferences, and 3) LM neurons are more tightly tuned to stimulus velocity. In this study, we sought to determine if there are concomitant changes in the nucleus of the basal optic root (nBOR) of the AOS. We recorded the visual response properties of nBOR neurons to large-field-drifting random dot patterns and sine-wave gratings in Anna's hummingbirds and zebra finches and compared these with archival data from pigeons. We found no differences with respect to the distribution of direction preferences: Neurons responsive to upward, downward, and nasal-to-temporal motion were equally represented in all three species, and neurons responsive to temporal-to-nasal motion were rare or absent (<5%). Compared with zebra finches and pigeons, however, hummingbird nBOR neurons were more tightly tuned to stimulus velocity of random dot stimuli. Moreover, in response to drifting gratings, hummingbird nBOR neurons are more tightly tuned in the spatiotemporal domain. These results, in combination with specialization in LM, support a hypothesis that hummingbirds have evolved to be "optic flow specialists" to cope with the optomotor demands of sustained hovering flight.NEW & NOTEWORTHY Hummingbirds have specialized response properties to optic flow in the pretectal nucleus lentiformis mesencephali (LM). The LM works with the nucleus of the basal optic root (nBOR) of the accessory optic system (AOS) to process global visual motion, but whether the neural response specializations observed in the LM extend to the nBOR is unknown. Hummingbird nBOR neurons are more tightly tuned to visual stimulus velocity, and in the spatiotemporal domain, compared with two nonhovering species.

Temporal synchrony effects of optic flow and vestibular inputs on multisensory heading perception.

Precise heading perception requires integration of optic flow and vestibular cues, yet the two cues often carry distinct temporal dynamics that may confound cue integration benefit. Here, we varied temporal offset between the two sensory inputs while macaques discriminated headings around straight ahead. We find the best heading performance does not occur under natural condition of synchronous inputs with zero offset but rather when visual stimuli are artificially adjusted to lead vestibular by a few hundreds of milliseconds. This amount exactly matches the lag between the vestibular acceleration and visual speed signals as measured from single-unit-activity in frontal and posterior parietal cortices. Manually aligning cues in these areas best facilitates integration with some nonlinear gain modulation effects. These findings are consistent with predictions from a model by which the brain integrates optic flow speed with a faster vestibular acceleration signal for sensing instantaneous heading direction during self-motion in the environment.

Facilitation of neural responses to targets moving against optic flow.

For the human observer, it can be difficult to follow the motion of small objects, especially when they move against background clutter. In contrast, insects efficiently do this, as evidenced by their ability to capture prey, pursue conspecifics, or defend territories, even in highly textured surrounds. We here recorded from target selective descending neurons (TSDNs), which likely subserve these impressive behaviors. To simulate the type of optic flow that would be generated by the pursuer's own movements through the world, we used the motion of a perspective corrected sparse dot field. We show that hoverfly TSDN responses to target motion are suppressed when such optic flow moves syn-directional to the target. Indeed, neural responses are strongly suppressed when targets move over either translational sideslip or rotational yaw. More strikingly, we show that TSDNs are facilitated by optic flow moving counterdirectional to the target, if the target moves horizontally. Furthermore, we show that a small, frontal spatial window of optic flow is enough to fully facilitate or suppress TSDN responses to target motion. We argue that such TSDN response facilitation could be beneficial in modulating corrective turns during target pursuit.

Circuit Organization Underlying Optic Flow Processing in Zebrafish.

Animals' self-motion generates a drifting movement of the visual scene in the entire field of view called optic flow. Animals use the sensation of optic flow to estimate their own movements and accordingly adjust their body posture and position and stabilize the direction of gaze. In zebrafish and other vertebrates, optic flow typically drives the optokinetic response (OKR) and optomotor response (OMR). Recent functional imaging studies in larval zebrafish have identified the pretectum as a primary center for optic flow processing. In contrast to the view that the pretectum acts as a relay station of direction-selective retinal inputs, pretectal neurons respond to much more complex visual features relevant to behavior, such as spatially and temporally integrated optic flow information. Furthermore, optic flow signals, as well as motor signals, are represented in the cerebellum in a region-specific manner. Here we review recent findings on the circuit organization that underlies the optic flow processing driving OKR and OMR.

Action-dependent processing of self-motion in parietal cortex of macaque monkeys.

Successful interaction with the environment requires the dissociation of self-induced from externally induced sensory stimulation. Temporal proximity of action and effect is hereby often used as an indicator of whether an observed event should be interpreted as a result of own actions or not. We tested how the delay between an action (press of a touch bar) and an effect (onset of simulated self-motion) influences the processing of visually simulated self-motion in the ventral intraparietal area (VIP) of macaque monkeys. We found that a delay between the action and the start of the self-motion stimulus led to a rise of activity above the baseline activity before motion onset in a subpopulation of 21% of the investigated neurons. In the responses to the stimulus, we found a significantly lower sustained activity when the press of a touch bar and the motion onset were contiguous compared to the condition when the motion onset was delayed. We speculate that this weak inhibitory effect might be part of a mechanism that sharpens the tuning of VIP neurons during self-induced motion and thus has the potential to increase the precision of heading information that is required to adjust the orientation of self-motion in everyday navigational tasks.NEW & NOTEWORTHY Neurons in macaque ventral intraparietal area (VIP) are responding to sensory stimulation related to self-motion, e.g. visual optic flow. Here, we found that self-motion induced activation depends on the sense of agency, i.e., it differed when optic flow was perceived as self- or externally induced. This demonstrates that area VIP is well suited for study of the interplay between active behavior and sensory processing during self-motion.

Visual-vestibular integration is preserved with healthy aging in a simple acceleration detection task.

Aging is associated with a gradual decline in the sensory systems and noisier sensory information. Some research has found that older adults compensate for this with enhanced multisensory integration. However, less is known about how aging influences visual-vestibular integration, an ability that underlies self-motion perception. We examined how visual-vestibular integration changes in participants from across the lifespan (18-79 years old) with a simple reaction time task. Participants were instructed to respond to visual (optic flow) and vestibular (inertial motion) acceleration cues, presented either alone or at a stimulus onset asynchrony. We measured reaction times and computed the violation area relative to the race model inequality as a measure of visual-vestibular integration. Across all ages, the greatest visual-vestibular integration occurred when the vestibular cue was presented first. Age was associated with longer reaction times and a significantly lower detection rate in the vestibular-only condition, a finding that is consistent with an age-related increase in vestibular noise. Although the relationship between age and visual-vestibular integration was positive, the effect size was very small and did not reach statistical significance. Our results suggest that although age is associated with a significant increase in vestibular perceptual threshold, the relative amount of visual-vestibular integration remains largely intact.

Forward optic flow is prioritised in visual awareness independently of walking direction.

When two different images are presented separately to each eye, one experiences smooth transitions between them-a phenomenon called binocular rivalry. Previous studies have shown that exposure to signals from other senses can enhance the access of stimulation-congruent images to conscious perception. However, despite our ability to infer perceptual consequences from bodily movements, evidence that action can have an analogous influence on visual awareness is scarce and mainly limited to hand movements. Here, we investigated whether one's direction of locomotion affects perceptual access to optic flow patterns during binocular rivalry. Participants walked forwards and backwards on a treadmill while viewing highly-realistic visualisations of self-motion in a virtual environment. We hypothesised that visualisations congruent with walking direction would predominate in visual awareness over incongruent ones, and that this effect would increase with the precision of one's active proprioception. These predictions were not confirmed: optic flow consistent with forward locomotion was prioritised in visual awareness independently of walking direction and proprioceptive abilities. Our findings suggest the limited role of kinaesthetic-proprioceptive information in disambiguating visually perceived direction of self-motion and indicate that vision might be tuned to the (expanding) optic flow patterns prevalent in everyday life.

Auditory cues facilitate object movement processing in human extrastriate visual cortex during simulated self-motion: A pilot study.

Visual segregation of moving objects is a considerable computational challenge when the observer moves through space. Recent psychophysical studies suggest that directionally congruent, moving auditory cues can substantially improve parsing object motion in such settings, but the exact brain mechanisms and visual processing stages that mediate these effects are still incompletely known. Here, we utilized multivariate pattern analyses (MVPA) of MRI-informed magnetoencephalography (MEG) source estimates to examine how crossmodal auditory cues facilitate motion detection during the observer's self-motion. During MEG recordings, participants identified a target object that moved either forward or backward within a visual scene that included nine identically textured objects simulating forward observer translation. Auditory motion cues 1) improved the behavioral accuracy of target localization, 2) significantly modulated the MEG source activity in the areas V2 and human middle temporal complex (hMT+), and 3) increased the accuracy at which the target movement direction could be decoded from hMT+ activity using MVPA. The increase of decoding accuracy by auditory cues in hMT+ was significant also when superior temporal activations in or near auditory cortices were regressed out from the hMT+ source activity to control for source estimation biases caused by point spread. Taken together, these results suggest that parsing object motion from self-motion-induced optic flow in the human extrastriate visual cortex can be facilitated by crossmodal influences from auditory system.

Natural image statistics in the dorsal and ventral visual field match a switch in flight behaviour of a hawkmoth.

Many animals use visual cues to navigate their environment. To encode the large input ranges of natural signals optimally, their sensory systems have adapted to the stimulus statistics experienced in their natural habitats1. A striking example, shared across animal phyla, is the retinal tuning to the relative abundance of blue light from the sky, and green light from the ground, evident in the frequency of each photoreceptor type in the two retinal hemispheres2. By adhering only to specific regions of the visual field that contain the relevant information, as for the high-acuity dorsal regions in the eyes of male flies chasing females3, the neural investment can be further reduced. Regionalisation can even lead to activation of the appropriate visual pathway by target location, rather than by stimulus features. This has been shown in fruit flies, which increase their landing attempts when an expanding disc is presented in their frontal visual field, while lateral presentation increases obstacle avoidance responses4. We here report a similar switch in behavioural responses for extended visual scenes. Using a free-flight paradigm, we show that the hummingbird hawkmoth (Macroglossum stellatarum) responds with flight-control adjustments to translational optic-flow cues exclusively in their ventral and lateral visual fields, while identical stimuli presented dorsally elicit a novel directional flight response. This response split is predicted by our quantitative imaging data from natural visual scenes in a variety of habitats, which demonstrate higher magnitudes of translational optic flow in the ventral hemisphere, and the opposite distribution for contrast edges containing directional information.