Wide-field, motion-sensitive neurons and matched filters for optic flow fields

 The receptive field organization of a class of visual interneurons in the fly brain (vertical system, or VS neurons) shows a striking similarity to certain self-motion-induced optic flow fields. The present study compares the measured motion sensitivities of the VS neurons (Krapp et al. 1998) to a matched filter model for optic flow fields generated by rotation or translation. The model minimizes the variance of the filter output caused by noise and distance variability between different scenes. To that end, prior knowledge about distance and self-motion statistics is incorporated in the form of a “world model”. We show that a special case of the matched filter model is able to predict the local motion sensitivities observed in some VS neurons. This suggests that their receptive field organization enables the VS neurons to maintain a consistent output when the same type of self-motion occurs in different situations. Received: 14 June 1999 / Accepted in revised form: 20 March 2000     

Local and global motion preferences in descending neurons of the fly

For a moving animal, optic flow is an important source of information about its ego-motion. In flies, the processing of optic flow is performed by motion sensitive tangential cells in the lobula plate. Amongst them, cells of the vertical system (VS cells) have receptive fields with similarities to optic flows generated during rotations around different body axes. Their output signals are further processed by pre-motor descending neurons. Here, we investigate the local motion preferences of two descending neurons called descending neurons of the ocellar and vertical system (DNOVS1 and DNOVS2). Using an LED arena subtending 240° × 95° of visual space, we mapped the receptive fields of DNOVS1 and DNOVS2 as well as those of their presynaptic elements, i.e. VS cells 1–10 and V2. The receptive field of DNOVS1 can be predicted in detail from the receptive fields of those VS cells that are most strongly coupled to the cell. The receptive field of DNOVS2 is a combination of V2 and VS cells receptive fields. Predicting the global motion preferences from the receptive field revealed a linear spatial integration in DNOVS1 and a superlinear spatial integration in DNOVS2. In addition, the superlinear integration of V2 output is necessary for DNOVS2 to differentiate between a roll rotation and a lift translation of the fly.     

Neural action fields for optic flow based navigation: a simulation study of the fly lobula plate network

Optic flow based navigation is a fundamental way of visual course control described in many different species including man. In the fly, an essential part of optic flow analysis is performed in the lobula plate, a retinotopic map of motion in the environment. There, the so-called lobula plate tangential cells possess large receptive fields with different preferred directions in different parts of the visual field. Previous studies demonstrated an extensive connectivity between different tangential cells, providing, in principle, the structural basis for their large and complex receptive fields. We present a network simulation of the tangential cells, comprising most of the neurons studied so far (22 on each hemisphere) with all the known connectivity between them. On their dendrite, model neurons receive input from a retinotopic array of Reichardt-type motion detectors. Model neurons exhibit receptive fields much like their natural counterparts, demonstrating that the connectivity between the lobula plate tangential cells indeed can account for their complex receptive field structure. We describe the tuning of a model neuron to particular types of ego-motion (rotation as well as translation around/along a given body axis) by its 'action field'. As we show for model neurons of the vertical system (VS-cells), each of them displays a different type of action field, i.e., responds maximally when the fly is rotating around a particular body axis. However, the tuning width of the rotational action fields is relatively broad, comparable to the one with dendritic input only. The additional intra-lobula-plate connectivity mainly reduces their translational action field amplitude, i.e., their sensitivity to translational movements along any body axis of the fly.     

Retinotopic organization of small-field-target-detecting neurons in the insect visual system

BACKGROUND: Despite having tiny brains and relatively low-resolution compound eyes, many fly species frequently engage in precisely controlled aerobatic pursuits of conspecifics. Recent investigations into high-order processing in the fly visual system have revealed a class of neurons, coined small-target-motion detectors (STMDs), capable of responding robustly to target motion against the motion of background clutter. Despite limited spatial acuity in the insect eye, these neurons display exquisite sensitivity to small targets. RESULTS: We recorded intracellularly from morphologically identified columnar neurons in the lobula complex of the hoverfly Eristalis tenax. We show that these columnar neurons with exquisitely small receptive fields, like their large-field counterparts recently described from both male and female flies, have an extreme selectivity for the motion of small targets. In doing so, we provide the first physiological characterization of small-field neurons in female flies. These retinotopically organized columnar neurons include both direction-selective and nondirection-selective classes covering a large area of visual space. CONCLUSIONS: The retinotopic arrangement of lobula columnar neurons sensitive to the motion of small targets makes a strong case for these neurons as important precursors in the local processing of target motion. Furthermore, the continued response of STMDs with such small receptive fields to the motion of small targets in the presence of moving background clutter places further constraints on the potential mechanisms underlying their small-target tuning.     

Response properties of motion-sensitive visual interneurons in the lobula plate of Drosophila melanogaster

The crystalline-like structure of the optic lobes of the fruit fly Drosophila melanogaster has made them a model system for the study of neuronal cell-fate determination, axonal path finding, and target selection. For functional studies, however, the small size of the constituting visual interneurons has so far presented a formidable barrier. We have overcome this problem by establishing in vivo whole-cell recordings from genetically targeted visual interneurons of Drosophila. Here, we describe the response properties of six motion-sensitive large-field neurons in the lobula plate that form a network consisting of individually identifiable, directionally selective cells most sensitive to vertical image motion (VS cells). Individual VS cell responses to visual motion stimuli exhibit all the characteristics that are indicative of presynaptic input from elementary motion detectors of the correlation type. Different VS cells possess distinct receptive fields that are arranged sequentially along the eye's azimuth, corresponding to their characteristic cellular morphology and position within the retinotopically organized lobula plate. In addition, lateral connections between individual VS cells cause strongly overlapping receptive fields that are wider than expected from their dendritic input. Our results suggest that motion vision in different dipteran fly species is accomplished in similar circuitries and according to common algorithmic rules. The underlying neural mechanisms of population coding within the VS cell network and of elementary motion detection, respectively, can now be analyzed by the combination of electrophysiology and genetic intervention in Drosophila.     

Responses of optokinetic neurons in the pretectum and accessory optic system of the pigeon to large-field plaids

The accessory optic system and pretectum are highly conserved brainstem visual pathways that process the visual consequences of self-motion (i.e. optic flow) and generate the optokinetic response. Neurons in these nuclei have very large receptive fields in the contalateral eye, and exhibit direction-selectivity to large-field moving stimuli. Previous research on visual motion pathways in the geniculostriate system has employed "plaids" composed of two non-parallel sine-wave gratings to investigate the visual system's ability to detect the global direction of pattern motion as opposed to the direction of motion of the components within the plaids. In this study, using standard extracellular techniques, we recorded the responses of 47 neurons in the nucleus of the basal optic root of the accessory optic system and 49 cells in the pretectal nucleus lentiformis mesencephali of pigeons to large-field gratings and plaids. We found that most neurons were classified as pattern-selective (41-49%) whereas fewer were classified as component-selective (8-17%). There were no striking differences between nucleus of the basal optic root and lentiformis mesencephali neurons in this regard. These data indicate that most of the input to the optokinetic system is orientation-insensitive but a small proportion is orientation-selective. The implications for the connectivity of the motion processing system are discussed.     

Encoding of motion in real time by the fly visual system.

Direction-selective cells in the fly visual system that have large receptive fields play a decisive role in encoding the time-dependent optic flow the animal encounters during locomotion. Recent experiments on the computations performed by these cells have highlighted the significance of dendritic integration and have addressed the role of spikes versus graded membrane potential changes in encoding optic flow information. It is becoming increasingly clear that the way optic flow is encoded in real time is constrained both by the computational needs of the animal in visually guided behaviour as well as by the specific properties of the underlying neuronal hardware.     

Motion sensitive interneurons in the optomotor system of the fly

The functional properties of the three horizontal cells (north horizontal cell, HSN; equatorial horizontal cell, HSE; south horizontal cell, HSS) in the lobula plate of the blowflyCalliphora erythrocephala were investigated electrophysiologically. 1. The receptive fields of the HSN, HSE, and HSS cover the dorsal, equatorial and ventral part of the ipsilateral visual field, respectively. In all three cells, the sensitivity to visual stimulation is highest in the frontal visual field and decreases laterally. The receptive fields and spatial sensitivity distributions of the horizontal cells are directly determined by the position and extension of their dendritic fields in the lobula plate and the dendritic density distributions within these fields. 2. The horizontal cells respond mainly to progressive (front to back) motion and are inhibited by motion in the reverse direction, the preferred and null direction being antiparallel. The amplitudes of motion induced excitatory and inhibitory responses decline like a cosine function with increasing deviation of the direction of motion from the preferred direction. Stimulation with motion in directions perpendicular to the preferred direction is ineffective. 3. The preferred directions of the horizontal cells show characteristic gradual orientation changes in different parts of the receptive fields: they are horizontally oriented only in the equatorial region and increasingly tilted vertically towards the dorsofrontal and ventrofrontal margins of the visual field. These orientation changes can be correlated with equivalent changes in the local orientation of the lattice of ommatidial axes in the pertinent compound eye. 4. The response amplitudes of the horizontal cells under stimulation with a moving periodic grating depend strongly on the contrast frequency of the stimulus. Maximal responses were found at contrast frequencies of 2–5 Hz. 5. The spatial integration properties of the horizontal cells (studied in the HSE) are highly nonlinear. Under stimulation with extended moving patterns, their response amplitudes are nearly independent of the size of the stimuli. It is demonstrated that this response behaviour does not result from postsynaptic saturation in the dendrites of the cells. The results indicate that the horizontal system is essentially involved in the neural control of optomotor torque responses performed by the fly in order to minimize unvoluntary deviations from a straight flight course.     

A system of insect neurons sensitive to horizontal and vertical image motion connects the medulla and midbrain

Summary The response properties and gross morphologies of neurons that connect the medulla and midbrain in the butterfly Papilio aegeus are described. The neurons presented give direction-selective responses, i.e. they are excited by motion in the preferred direction and the background activity of the cells is inhibited by motion in the opposite, null, direction. The neurons are either maximally sensitive to horizontal motion or to slightly off-axis vertical upward or vertical downward motion, when tested in the frontal visual field. The responses of the cells are dependent on the contrast frequency of the stimulus with peak values at 5–10 Hz. The receptive fields of the medulla neurons are large and are most sensitive in the frontal visual field. Examination of the local and global properties of the receptive fields of the medulla neurons indicates that (1) they are fed by local elementary motion-detectors consistent with the correlation model and (2) there is a non-linear spatial integration mechanism in operation.     

‘Vector white noise’: a technique for mapping the motion receptive fields of direction-selective visual neurons

A technique is described and tested for mapping the sensitivities and preferred directions of motion at different locations within the receptive fields of direction-selective motion-detecting visual neurons. The procedure is to record the responses to a number of visual stimuli, each stimulus presentation consisting of a set of short, randomly-oriented, moving bars arranged in a square grid. Each bar moves perpendicularly to its long axis. The vector describing the sensitivity and preferred direction of motion at each grid location is obtained as a sum of the unit vectors defining the directions of motion of the bars in each of the stimuli at that location, weighted by the strengths of the corresponding responses. The resulting vector field specifies the optimum flow field for the neuron. The advantage of this technique over the conventional approach of probing the receptive field sequentially at each grid location is that the parallel nature of the stimulus is sensitive to nonlinear interactions (such as shunting inhibition for mutual facilitation) between different regions of the visual field. The technique is used to determine accurately the motion receptive fields of direction-selective motion detecting neurons in the optic lobes of insects. It is potentially applicable to motion-sensitive neurons with highly structured receptive fields, such as those in the optic tectum of the pigeon or in area MST of the monkey.     

Dissociation of neuronal and psychophysical responses to local and global motion

Most neurons in cortical area MT (V5) are strongly direction selective, and their activity is closely associated with the perception of visual motion. These neurons have large receptive fields built by combining inputs with smaller receptive fields that respond to local motion. Humans integrate motion over large areas and can perceive what has been referred to as global motion. The large size and direction selectivity of MT receptive fields suggests that MT neurons may represent global motion. We have explored this possibility by measuring responses to a stimulus in which the directions of simultaneously presented local and global motion are independently controlled. Surprisingly, MT responses depended only on the local motion and were unaffected by the global motion. Yet, under similar conditions, human observers perceive global motion and are impaired in discriminating local motion. Although local motion perception might depend on MT signals, global motion perception depends on mechanisms qualitatively different from those in MT. Motion perception therefore does not depend on a single cortical area but reflects the action and interaction of multiple brain systems.     

Optic flow representation in the optic lobes of Diptera: modeling the role of T5 directional tuning properties

An evolutionarily conserved system of small retinotopic neurons in dipteran insects, called bushy T-cells, provides information about directional motion to large collator neurons in the lobula plate. Physiological and anatomical features of these cells provide the basis for a model that is used to investigate requirements for generating optic flow selectivity in collators while allowing for evolutionary variations. This account focuses on the role of physiological tuning properties of T5 neurons. Various flow fields are defined as inputs to retinotopic arrays of T5 cells, the responses of which are mapped onto collators using innervation matrices that promote selectivity for flow type and position. Properties known or inferred from physiological and anatomical studies of neurons contributing to motion detection are incorporated into the model: broad tuning to local motion direction and the representation of each visual sampling unit by a quartet of small-field T5-like neurons with orthogonal preferred directions. The model predicts hitherto untested response properties of optic flow selective collators, and predicts that selectivity for a given flow field can be highly sensitive to perturbations in physiological properties of the motion detectors.     

End-stopping and the aperture problem: two-dimensional motion signals in macaque V1

Our perception of fine visual detail relies on small receptive fields at early stages of visual processing. However, small receptive fields tend to confound the orientation and velocity of moving edges, leading to ambiguous or inaccurate motion measurements (the aperture problem). Thus, it is often assumed that neurons in primary visual cortex (V1) carry only ambiguous motion information. Here we show that a subpopulation of V1 neurons is capable of signaling motion direction in a manner that is independent of contour orientation. Specifically, end-stopped V1 neurons obtain accurate motion measurements by responding only to the endpoints of long contours, a strategy which renders them largely immune to the aperture problem. Furthermore, the time course of end-stopping is similar to the time course of motion integration by MT neurons. These results suggest that cortical neurons might represent object motion by responding selectively to two-dimensional discontinuities in the visual scene.     

Orientation sensitive properties of visually driven neurons in extrastriate area 21a of cat cortex

Orientation sensitive properties of extrastriate area 21a neurons were investigated. Special attention was paid to the qualitative characteristics of neuron responses to the different orientations of visual stimulus motion across neuron classical receptive fields (CRF). The results of experiments have shown that a group of neurons (31%) in area 21a with specialized responses to moving visual stimuli changed their direction selective (DS) characteristics depending on the orientation of the stimulus movement. Some neurons reveal an abrupt drop of the direction sensitivity index (DI) to certain orientation (58%), and some show significant increase of DI at one of applied orientations of stimulus motion (22%). Detailed investigation of response patterns of non-directional neurons to different orientations of stimulus motion have revealed clear-cut qualitative differences, such as different regularities in the distribution of inter-peak inhibitory intervals in the response pattern in dependence of the orientation of stimulus motion. The investigation of neuron CRF stationary functional organization did not reveal correlations between RF's spatial functional organization, and that of qualitative modulations of neuron response patterns. A suggestion was put forward, that visual information central processing of orientation discrimination is a complex integrative process that includes quantitative as well as qualitative transformations of neuron activity.     

Distribution of auditory motion-direction sensitive neurons in the barn owl's midbrain

Barn owls have neurons sensitive to acoustic motion-direction in the midbrain. We report here that acoustic motion-direction sensitive neurons with receptive-field centres in frontal auditory space are not randomly distributed. In the inferior colliculus and optic tectum in the left (right) brain, the responses of about two-thirds of the motion-direction sensitive neurons were sensitive to clockwise (counter-clockwise) motion. The midbrain contains maps of auditory space that represent about 15 degrees of ipsilateral and all of contralateral space. Since a similar bias in motion-direction sensitivity was observed for neurons with receptive-field centres in ipsilateral as well as for neurons with receptive fields centres in contralateral auditory space, the brain side at which a motion-direction sensitive neuron was recorded was a more important predictor for the preferred direction of a cell than the spatial direction of the centre of the receptive field. Within one dorso-ventral electrode pass motion-direction sensitivity typically stayed constant suggesting a clustered or even a columnar-like organization. We hypothesize from these distributions that the right brain is important for orientating movements to the left hemisphere and vice versa.     

Visuomotor transformation in the fly gaze stabilization system

For sensory signals to control an animal's behavior, they must first be transformed into a format appropriate for use by its motor systems. This fundamental problem is faced by all animals, including humans. Beyond simple reflexes, little is known about how such sensorimotor transformations take place. Here we describe how the outputs of a well-characterized population of fly visual interneurons, lobula plate tangential cells (LPTCs), are used by the animal's gaze-stabilizing neck motor system. The LPTCs respond to visual input arising from both self-rotations and translations of the fly. The neck motor system however is involved in gaze stabilization and thus mainly controls compensatory head rotations. We investigated how the neck motor system is able to selectively extract rotation information from the mixed responses of the LPTCs. We recorded extracellularly from fly neck motor neurons (NMNs) and mapped the directional preferences across their extended visual receptive fields. Our results suggest that-like the tangential cells-NMNs are tuned to panoramic retinal image shifts, or optic flow fields, which occur when the fly rotates about particular body axes. In many cases, tangential cells and motor neurons appear to be tuned to similar axes of rotation, resulting in a correlation between the coordinate systems the two neural populations employ. However, in contrast to the primarily monocular receptive fields of the tangential cells, most NMNs are sensitive to visual motion presented to either eye. This results in the NMNs being more selective for rotation than the LPTCs. Thus, the neck motor system increases its rotation selectivity by a comparatively simple mechanism: the integration of binocular visual motion information.     

Global versus local adaptation in fly motion-sensitive neurons

Flies, like humans, experience a well-known consequence of adaptation to visual motion, the waterfall illusion. Direction-selective neurons in the fly lobula plate permit a detailed analysis of the mechanisms responsible for motion adaptation and their function. Most of these neurons are spatially non-opponent, they sum responses to motion in the preferred direction across their entire receptive field, and adaptation depresses responses by subtraction and by reducing contrast gain. When we adapted a small area of the receptive field to motion in its anti-preferred direction, we discovered that directional gain at unadapted regions was enhanced. This novel phenomenon shows that neuronal responses to the direction of stimulation in one area of the receptive field are dynamically adjusted to the history of stimulation both within and outside that area.     

Two-dimensional substructure of MT receptive fields.

Neurons at progressively higher levels of the visual system have progressively larger, more complicated receptive fields, presumably constructed from simpler antecedent receptive fields. To study this hierarchical organization, we used sparse white noise to map receptive-field substructure (second order Wiener-like kernels) in an extrastriate motion processing area (MT) of alert monkeys. The maps revealed a clear substructure, on a spatial scale comparable to the receptive fields of the V1 inputs. There were both facilitatory and suppressive interactions that differed in spatial organization and time course. Directional interactions were remarkably precise over a very small spatial range, and reversed when successive stimuli reversed contrast--a neural correlate of "reverse phi" motion perception. The maps of some cells had an unexpected, curved shape, which challenges existing models for direction selectivity.     

Segregation of object and background motion in visual area MT: effects of microstimulation on eye movements

To track a moving object, its motion must first be distinguished from that of the background. The center-surround properties of neurons in the middle temporal visual area (MT) may be important for signaling the relative motion between object and background. To test this, we microstimulated within MT and measured the effects on monkeys' eye movements to moving targets. We found that stimulation at "local motion" sites, where receptive fields possessed antagonistic surrounds, shifted pursuit in the preferred direction of the neurons, whereas stimulation at "wide-field motion" sites shifted pursuit in the opposite, or null, direction. We propose that activating wide-field sites simulated background motion, thus inducing a target motion signal in the opposite direction. Our results support the hypothesis that neuronal center-surround mechanisms contribute to the behavioral segregation of objects from the background.     

Response properties of visual interneurons to motion stimuli in the praying mantis,Tenodera aridifolia

Intracellular responses of motion-sensitive visual interneurons were recorded from the lobula complex of the mantis, Tenodera aridifolia. The interneurons were divided into four classes according to the response polarity, spatial tuning, and directional selectivity. Neurons of the first class had small, medium, or large receptive fields and showed a strong excitation in response to a small-field motion such as a small square moving in any direction (SF neurons). The second class neurons showed non-directionally selective responses: an excitation to a large-field motion of gratings in any direction (ND neurons). Most ND neurons had small or medium-size receptive fields. Neurons of the third class had large receptive fields and exhibited directionally selective responses: an excitation to a large-field motion of gratings in preferred direction and an inhibition to a motion in opposite, null direction (DS neurons). The last class neurons had small receptive fields and showed inhibitory responses to a moving square and gratings (I neurons). The functional roles of these neurons in prey recognition and optomotor response were discussed.