Optic flow representation in the optic lobes of Diptera: modeling innervation matrices onto collators and their evolutionary implications

A network model of optic flow processing, based on physiological and anatomical features of motion-processing neurons, is used to investigate the role of small-field motion detectors emulating T5 cells in producing optic flow selective properties in wide-field collator neurons. The imposition of different connectivities can mimic variations observed in comparative studies of lobula plate architecture across the Diptera. The results identify two features that are crucial for optic flow selectivity: the broadness of the spatial patterns of synaptic connections from motion detectors to collators, and the relative contributions of excitatory and inhibitory synaptic outputs. If these two aspects of the innervation matrix are balanced appropriately, the network's sensitivity to perturbations in physiological properties of the small-field motion detectors is dramatically reduced, suggesting that sensory systems can evolve robust mechanisms that do not rely upon precise control of network parameters. These results also suggest that alternative lobula plate architectures observed in insects are consistent in allowing optic flow selective properties in wide-field neurons. The implications for the evolution of optic flow selective neurons are discussed.     

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.     

The functional organization of male-specific visual neurons in flies

Summary Intracellular recording and Lucifer yellow dye filling of male fleshflies, Sarcophaga bullata, have revealed male-specific neurons in the lobula, the axons of which project to the origin of premotor channels supplying flight motor neurons. Dendrites of male-specific neurons visit areas of the retinotopic mosaic supplied by the retina's acute zone, which is used by males to keep the image of a conspecific female centered during aerial pursuit. Only males engage in high-speed acrobatic chases, and male-specific neurons are suspected to under-lie this behavior. Physiological determination of receptive fields of male-specific neurons substantiates the fields predicted from anatomical studies and demonstrates that they subtend the acute zone. Male-specific neurons respond in a manner predicted on theoretical grounds from observations of tracking behavior. Such properties include directional selectivity to visual motion and higher sensitivity to motion of small images than to wide-field motion. The present account substantiates and extends neuroanatomical evidence that predicts that male-specific lobula neurons comprise a distinct circuit mediating conspecific tracking.     

Subcellular mapping of dendritic activity in optic flow processing neurons

Dendritic integration is a fundamental element of neuronal information processing. So far, few studies have provided a detailed spatial picture of this process, describing the properties of local dendritic activity and its subcellular organization. Here, we used 2-photon calcium imaging in optic flow processing neurons of the fly Calliphora vicina to determine the preferred location and direction of local motion cues for small branchlets throughout the entire dendrite. We found a pronounced retinotopic mapping on both the subcellular and the cell population level. In addition, dendritic branchlets residing in different layers of the neuropil were tuned to distinct directions of motion. Summing the local receptive fields of all dendritic branchlets reproduced the characteristic properties of these neurons’ axonal output receptive fields. Our results corroborate the notion that the dendritic morphology of vertical system cells allows them to selectively collect local motion inputs with particular directional preferences from a spatially organized input repertoire, thus forming filters that match global patterns of optic flow. Furthermore, we suggest that the facet arrangement across the fly’s eye shapes the subcellular direction tuning to local motion stimuli. These data illustrate a highly structured circuit organization as an efficient way to hard-wire a complex sensory task.     

Representation of motion onset and offset in an augmented Barlow-Levick model of motion detection

Kinetic occlusion produces discontinuities in the optic flow field, whose perception requires the detection of an unexpected onset or offset of otherwise predictably moving or stationary contrast patches. Many cells in primate visual cortex are directionally selective for moving contrasts, and recent reports suggest that this selectivity arises through the inhibition of contrast signals moving in the cells’ null direction, as in the rabbit retina. This nulling inhibition circuit (Barlow-Levick) is here extended to also detect motion onsets and offsets. The selectivity of extended circuit units, measured as a peak evidence accumulation response to motion onset/offset compared to the peak response to constant motion, is analyzed as a function of stimulus speed. Model onset cells are quiet during constant motion, but model offset cells activate during constant motion at slow speeds. Consequently, model offset cell speed tuning is biased towards higher speeds than onset cell tuning, similarly to the speed tuning of cells in the middle temporal area when exposed to speed ramps. Given a population of neurons with different preferred speeds, this asymmetry addresses a behavioral paradox—why human subjects in a simple reaction time task respond more slowly to motion offsets than onsets for low speeds, even though monkey neuron firing rates react more quickly to the offset of a preferred stimulus than to its onset.     

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.     

A multi-stage model for fundamental functional properties in primary visual cortex

Many neurons in mammalian primary visual cortex have properties such as sharp tuning for contour orientation, strong selectivity for motion direction, and insensitivity to stimulus polarity, that are not shared with their sub-cortical counterparts. Successful models have been developed for a number of these properties but in one case, direction selectivity, there is no consensus about underlying mechanisms. We here define a model that accounts for many of the empirical observations concerning direction selectivity. The model describes a single column of cat primary visual cortex and comprises a series of processing stages. Each neuron in the first cortical stage receives input from a small number of on-centre and off-centre relay cells in the lateral geniculate nucleus. Consistent with recent physiological evidence, the off-centre inputs to cortex precede the on-centre inputs by a small (～4 ms) interval, and it is this difference that confers direction selectivity on model neurons. We show that the resulting model successfully matches the following empirical data: the proportion of cells that are direction selective; tilted spatiotemporal receptive fields; phase advance in the response to a stationary contrast-reversing grating stepped across the receptive field. The model also accounts for several other fundamental properties. Receptive fields have elongated subregions, orientation selectivity is strong, and the distribution of orientation tuning bandwidth across neurons is similar to that seen in the laboratory. Finally, neurons in the first stage have properties corresponding to simple cells, and more complex-like cells emerge in later stages. The results therefore show that a simple feed-forward model can account for a number of the fundamental properties of primary visual cortex.     

Two classes of visual motion sensitive interneurons differ in direction and velocity dependency of in vivo calcium dynamics

Neurons exploit both membrane biophysics and biochemical pathways of the cytoplasm for dendritic integration of synaptic input. Here we quantify the tuning discrepancy of electrical and chemical response properties in two kinds of neurons using in vivo visual stimulation. Dendritic calcium concentration changes and membrane potential of visual interneurons of the fly were measured in response to visual motion stimuli. Two classes of tangential cells of the lobula plate were compared, HS-cells and CH-cells. Both neuronal classes are known to receive retinotopic input with similar properties, yet they differ in morphology, physiology, and computational context. Velocity tuning and directional selectivity of the electrical and calcium responses were investigated. In both cell classes, motion-induced calcium accumulation did not follow the early transient of the membrane potential. Rather, the amplitude of the calcium signal seemed to be related to the late component of the depolarization, where it was close to a steady state. Electrical and calcium responses differed with respect to their velocity tuning in CH-cells, but not in HS-cells. Furthermore, velocity tuning of the calcium response, but not of the electrical response differed between neuronal classes. While null-direction motion caused hyperpolarization in both classes, this led to a calcium decrement in CH-cells, but had no effect on the calcium signal in HS-cells, not even when calcium levels had been raised by a preceding excitatory motion stimulus. Finally, the voltage-[Ca2+]i-relationship for motion-induced, transient potential changes was steeper and less rectifying in CH-cells than in HS-cells. These results represent an example of dendritic information processing in vivo, where two neuronal classes respond to identical stimuli with a similar electrical response, but differing calcium response. This highlights the capacity of neurons to segregate two response components.     

Response properties of cat AMLS neurons to optic flow stimuli

Spiral and translation stimuli were used to investigate the response properties of cat AMLS (anteromedial lateral suprasylvian area) neurons to optic flow. The overwhelming majority of cells could be significantly excited by the two modes of stimuli and most responsive cells displayed obvious direction selectivity. It is the first time to find a visual area in mammalian brain preferring rotation stimuli. Two representative hypotheses are discussed here on the neural mechanism of optic flow analysis in visual cortex, and some new viewpoints are proposed to explain the experimental results.     

Response properties of cat AMLS neurons to optic flow stimuli

Spiral and translation stimuli were used to investigate the response properties of cat AMLS (anteromedial lateral suprasylvian area) neurons to optic flow. The overwhelming majority of cells could be significantly excited by the two modes of stimuli and most responsive cells displayed obvious direction selectivity. It is the first time to find a visual area in mammalian brain preferring rotation stimuli. Two representative hypotheses are discussed here on the neural mechanism of optic flow analysis in visual cortex, and some new viewpoints are proposed to explain the experimental results.     

Neural specializations for small target detection in insects

Despite being equipped with low-resolution eyes and tiny brains, many insects show exquisite abilities to detect and pursue targets even in highly textured surrounds. Target tracking behavior is subserved by neurons that are sharply tuned to the motion of small high-contrast targets. These neurons respond robustly to target motion, even against self-generated optic flow. A recent model, supported by neurophysiology, generates target selectivity by being sharply tuned to the unique spatiotemporal profile associated with target motion. Target neurons are likely connected in a complex network where some provide more direct output to behavior, whereas others serve an inter-regulatory role. These interactions may regulate attention and aid in the robust detection of targets in clutter observed in behavior.     

A comparison of models for sharpening of the frequency selectivity in the coachlea

The mechanical tuning of the basilar membrane has not been shown to be sharp enough to explain the very narrow tuning curves observed in primary auditory fibers. A mechanism for sharpening of the frequency selectivity or an unknown second filter is therefore assumed to exist in the cochlea. In the present paper, several theories for frequency selectivity sharpening in the cochlea are studied with the aid of a basilar membrane model. It is shown that the model proposed by Zwislocki (1974) for interaction between inner and outer hair cells results in the greatest increase in selectivity. It is also shown that nonlinear basilar membrane motion may very well explain the discrepancy between mechanical and neural tuning. Besides an increased selectivity at low sound intensities due to an increased low-frequency cut-off slope in the frequency transfer function, nonlinear basilar membrane motion also results in an increased high-frequency cut-off slope not present in other models for frequency selectivity sharpening.     

Visual Receptive Field Properties of Neurons in the Mouse Lateral Geniculate Nucleus

The lateral geniculate nucleus (LGN) is increasingly regarded as a “smart-gating” operator for processing visual information. Therefore, characterizing the response properties of LGN neurons will enable us to better understand how neurons encode and transfer visual signals. Efforts have been devoted to study its anatomical and functional features, and recent advances have highlighted the existence in rodents of complex features such as direction/orientation selectivity. However, unlike well-researched higher-order mammals such as primates, the full array of response characteristics vis-à-vis its morphological features have remained relatively unexplored in the mouse LGN. To address the issue, we recorded from mouse LGN neurons using multisite-electrode-arrays (MEAs) and analysed their discharge patterns in relation to their location under a series of visual stimulation paradigms. Several response properties paralleled results from earlier studies in the field and these include centre-surround organization, size of receptive field, spontaneous firing rate and linearity of spatial summation. However, our results also revealed “high-pass” and “low-pass” features in the temporal frequency tuning of some cells, and greater average contrast gain than reported by earlier studies. In addition, a small proportion of cells had direction/orientation selectivity. Both “high-pass” and “low-pass” cells, as well as direction and orientation selective cells, were found only in small numbers, supporting the notion that these properties emerge in the cortex. ON- and OFF-cells showed distinct contrast sensitivity and temporal frequency tuning properties, suggesting parallel projections from the retina. Incorporating a novel histological technique, we created a 3-D LGN volume model explicitly capturing the morphological features of mouse LGN and localising individual cells into anterior/middle/posterior LGN. Based on this categorization, we show that the ON/OFF, DS/OS and linear response properties are not regionally restricted. Our study confirms earlier findings of spatial pattern selectivity in the LGN, and builds on it to demonstrate that relatively elaborate features are computed early in the visual pathway.     

Integration of binocular optic flow in cervical neck motor neurons of the fly

Global visual motion elicits an optomotor response of the eye that stabilizes the visual input on the retina. Here, we analyzed the neck motor system of the blowfly to understand binocular integration of visual motion information underlying a head optomotor response. We identified and characterized two cervical nerve motor neurons (called CNMN6 and CNMN7) tuned precisely to an optic flow corresponding to pitch movements of the head. By means of double recordings and dye coupling, we determined that these neurons are connected ipsilaterally to two vertical system cells (VS2 and VS3), and contralaterally to one horizontal system cell (HSS). In addition, CNMN7 turned out to be connected to the ipsilateral CNMN6 and to its contralateral counterpart. To analyze a potential function of this circuit, we performed behavioral experiments and found that the optomotor pitch response of the fly head was only observable when both eyes were intact. Thus, this neural circuit performs two visuomotor transformations: first, by integrating binocular visual information it enhances the tuning to the optic flow resulting from pitch movements of the head, and second it could assure an even head declination by coordinating the activity of the CNMN7 neurons on both sides.     

A model for the detection of moving targets in visual clutter inspired by insect physiology

We present a computational model for target discrimination based on intracellular recordings from neurons in the fly visual system. Determining how insects detect and track small moving features, often against cluttered moving backgrounds, is an intriguing challenge, both from a physiological and a computational perspective. Previous research has characterized higher-order neurons within the fly brain, known as 'small target motion detectors' (STMD), that respond robustly to moving features, even when the velocity of the target is matched to the background (i.e. with no relative motion cues). We recorded from intermediate-order neurons in the fly visual system that are well suited as a component along the target detection pathway. This full-wave rectifying, transient cell (RTC) reveals independent adaptation to luminance changes of opposite signs (suggesting separate ON and OFF channels) and fast adaptive temporal mechanisms, similar to other cell types previously described. From this physiological data we have created a numerical model for target discrimination. This model includes nonlinear filtering based on the fly optics, the photoreceptors, the 1(st) order interneurons (Large Monopolar Cells), and the newly derived parameters for the RTC. We show that our RTC-based target detection model is well matched to properties described for the STMDs, such as contrast sensitivity, height tuning and velocity tuning. The model output shows that the spatiotemporal profile of small targets is sufficiently rare within natural scene imagery to allow our highly nonlinear 'matched filter' to successfully detect most targets from the background. Importantly, this model can explain this type of feature discrimination without the need for relative motion cues.     

Descending pathways connecting the male-specific visual system of flies to the neck and flight motor

Summary During sexual pursuit, male flies Sarcophaga bullata, stabilize the image of a pursued target on the dorso-frontal acute zone of their compound eyes. By retinotopic projection, this region is represented in the upper frontal part of the lobula where it is sampled by ensembles of male-specific motion- and flicker-sensitive interneurons. Intracellular recordings of descending neurons, followed by biocytin injection, demonstrate that male-specific neurons are dye-coupled to specific descending neurons and that the response characteristics of these descending neurons closely resemble those of male-specific lobula neurons. Such descending neurons are biocytin-coupled in the thoracic ganglia, revealing their connections with ipsilateral frontal nerve motor neurons supplying muscles that move the head and with contralateral basalar muscle motor neurons that control wing beat amplitude. Recordings from neck muscle motor neurons demonstrate that although they respond to movement of panoramic motion, they also selectively respond to movement of small targets presented to the male-specific acute zone. The present results are discussed with respect to anatomical and physiological studies of sex-specific interneurons and with respect to sex-specific visual behavior. The present study, and those of the two preceding papers, provide a revision of Land and Collett's hypothetical circuit underlying target localization and motor control in males pursuing females.     

Responses of blowfly motion-sensitive neurons to reconstructed optic flow along outdoor flight paths

The retinal image flow a blowfly experiences in its daily life on the wing is determined by both the structure of the environment and the animal’s own movements. To understand the design of visual processing mechanisms, there is thus a need to analyse the performance of neurons under natural operating conditions. To this end, we recorded flight paths of flies outdoors and reconstructed what they had seen, by moving a panoramic camera along exactly the same paths. The reconstructed image sequences were later replayed on a fast, panoramic flight simulator to identified, motion sensitive neurons of the so-called horizontal system (HS) in the lobula plate of the blowfly, which are assumed to extract self-motion parameters from optic flow. We show that under real life conditions HS-cells not only encode information about self-rotation, but are also sensitive to translational optic flow and, thus, indirectly signal information about the depth structure of the environment. These properties do not require an elaboration of the known model of these neurons, because the natural optic flow sequences generate—at least qualitatively—the same depth-related response properties when used as input to a computational HS-cell model and to real neurons.     

Parietal area VIP neuronal responses to heading stimuli are encoded in head-centered coordinates

The ventral intraparietal area (VIP) is a multimodal parietal area, where visual responses are brisk, directional, and typically selective for complex optic flow patterns. VIP thus could provide signals useful for visual estimation of heading (self-motion direction). A central problem in heading estimation is how observers compensate for eye velocity, which distorts the retinal motion cues upon which perception depends. To find out if VIP could be useful for heading, we measured its responses to simulated trajectories, both with and without eye movements. Our results showed that most VIP neurons very strongly signal heading direction. Furthermore, the tuning of most VIP neurons was remarkably stable in the presence of eye movements. This stability was such that the population of VIP neurons represented heading very nearly in head-centered coordinates. This makes VIP the most robust source of such signals yet described, with properties ideal for supporting perception.     

Human V6: Functional Characterisation and Localisation

Human visual area V6, in the parieto-occipital sulcus, is thought to have an important role in the extraction of optic flow for the monitoring and guidance of self-motion (egomotion) because it responds differentially to egomotion-compatible optic flow when compared to: (a) coherent but egomotion-incompatible flow (Cardin & Smith, 2010), and (b) incoherent motion (Pitzalis et al., 2010). It is not clear, however, whether V6 responds more strongly to egomotion-incompatible global motion than to incoherent motion. This is relevant not only for determining the functional properties of V6, but also in order to choose optimal stimuli for localising V6 accurately with fMRI. Localisation with retinotopic mapping is difficult and there is a need for a simple, reliable method. We conducted an event-related 3T fMRI experiment in which participants viewed a display of dots which either: a) followed a time-varying optic flow trajectory in a single, egomotion-compatible (EC) display; b) formed an egomotion-incompatible (EI) 3×3 array of optic flow patches; or c) moved randomly (RM). Results from V6 show an ordering of response magnitudes: EC > EI > RM. Neighbouring areas V3A and V7 responded more strongly to EC than to RM, but about equally to EC and EI. Our results suggest that although V6 may have a general role in the extraction of global motion, in clear contrast to neighbouring motion areas it is especially concerned with encoding EC stimuli. They suggest two strategies for localising V6: (1) contrasting EC and EI; or (2) contrasting EC and RM, which is more sensitive but carries a risk of including voxels from neighbouring regions that also show a EC > RM preference.     

A model of visual detection of angular speed for bees

A fly or bee's responses to widefield image motion depend on two basic parameters: temporal frequency and angular speed. Rotational optic flow is monitored using temporal frequency analysers, whereas translational optic flow seems to be monitored in terms of angular speed. Here we present a possible model of an angular speed detector which processes input signals through two parallel channels. The output of the detector is taken as the ratio of the two channels’ outputs. This operation amplifies angular speed sensitivity and depresses temporal frequency tuning. We analyse the behaviour of two versions of this model with different filtering properties in response to a variety of input signals. We then embody the detector in a simulated agent's visual system and explore its behaviour in experiments on speed control and odometry. The latter leads us to suggest a new algorithm for optic flow driven odometry.