OMR-Arena: Automated Measurement and Stimulation System to Determine Mouse Visual Thresholds Based on Optomotor Responses

Measurement of the optomotor response is a common way to determine thresholds of the visual system in animals. Particularly in mice, it is frequently used to characterize the visual performance of different genetically modified strains or to test the effect of various drugs on visual performance. Several methods have been developed to facilitate the presentation of stimuli using computer screens or projectors. Common methods are either based on the measurement of eye movement during optokinetic reflex behavior or rely on the measurement of head and/or body-movements during optomotor responses. Eye-movements can easily and objectively be quantified, but their measurement requires invasive fixation of the animals. Head movements can be observed in freely moving animals, but until now depended on the judgment of a human observer who reported the counted tracking movements of the animal during an experiment. In this study we present a novel measurement and stimulation system based on open source building plans and software. This system presents appropriate 360 stimuli while simultaneously video-tracking the animal''s head-movements without fixation. The on-line determined head gaze is used to adjust the stimulus to the head position, as well as to automatically calculate visual acuity. Exemplary, we show that automatically measured visual response curves of mice match the results obtained by a human observer very well. The spatial acuity thresholds yielded by the automatic analysis are also consistent with the human observer approach and with published results. Hence, OMR-arena provides an affordable, convenient and objective way to measure mouse visual performance.     

Sensitivity of the Goldfish Motion Detection System Revealed by Incoherent Random Dot Stimuli: Comparison of Behavioural and Neuronal Data

Background

Global motion detection is one of the most important abilities in the animal kingdom to navigate through a 3-dimensional environment. In the visual system of teleost fish direction-selective neurons in the pretectal area (APT) are most important for global motion detection. As in all other vertebrates these neurons are involved in the control of slow phase eye movements during gaze stabilization. In contrast to mammals cortical pathways that might influence motion detection abilities of the optokinetic system are missing in teleost fish.

Results

To test global motion detection in goldfish we first measured the coherence threshold of random dot patterns to elicit horizontal slow phase eye movements. In addition, the coherence threshold of the optomotor response was determined by the same random dot patterns. In a second approach the coherence threshold to elicit a direction selective response in neurons of the APT was assessed from a neurometric function. Behavioural thresholds and neuronal thresholds to elicit slow phase eye movements were very similar, and ranged between 10% and 20% coherence. In contrast to these low thresholds for the optokinetic reaction and APT neurons the optomotor response could only be elicited by random dot patterns with coherences above 40%.

Conclusion

Our findings suggest a high sensitivity for global motion in the goldfish optokinetic system. Comparison of neuronal and behavioural thresholds implies a nearly one-to-one transformation of visual neuron performance to the visuo-motor output. In addition, we assume that the optomotor response is not mediated by the optokinetic system, but instead by other motion detection systems with higher coherence thresholds.     

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.     

Convergence of visual,haltere, and prosternai inputs at neck motor neurons of Calliphora erythrocephala

Summary Neck muscles of Calliphora erythrocephala, situated in the anterior prothorax, are innervated on each side by 8 motor neurons arising in the brain (cervical nerve neurons, CN1–8) and at least 13 motor neurons arising in the prothoracic ganglion (anterior dorsal and frontal nerve neurons, ADN1,2 and FN1-11). Three prominent motor neurons (CN6 and FN1,2) are described in detail with special emphasis on their relationships with giant visual interneurons from the lobula plate, haltere interneurons, and primary afferents from the prosternal organs and halteres. These sensory organs detect head movement and body yaw, respectively. Neuronal relationships indicate that head movement is under multimodal sensory control that includes giant motion-sensitive neurons previously supposed to mediate the optomotor response in flying flies. The described pathways provide anatomical substrates for the control of optokinetic and yaw-incurred head movements that behavioural studies have shown must exist.     

Adaptation accentuates responses of fly motion-sensitive visual neurons to sudden stimulus changes

Adaptation in sensory and neuronal systems usually leads to reduced responses to persistent or frequently presented stimuli. In contrast to simple fatigue, adapted neurons often retain their ability to encode changes in stimulus intensity and to respond when novel stimuli appear. We investigated how the level of adaptation of a fly visual motion-sensitive neuron affects its responses to discontinuities in the stimulus, i.e. sudden brief changes in one of the stimulus parameters (velocity, contrast, grating orientation and spatial frequency). Although the neuron''s overall response decreased gradually during ongoing motion stimulation, the response transients elicited by stimulus discontinuities were preserved or even enhanced with adaptation. Moreover, the enhanced sensitivity to velocity changes by adaptation was not restricted to a certain velocity range, but was present regardless of whether the neuron was adapted to a baseline velocity below or above its steady-state velocity optimum. Our results suggest that motion adaptation helps motion-sensitive neurons to preserve their sensitivity to novel stimuli even in the presence of strong tonic stimulation, for example during self-motion.     

A Normalization Model of Attentional Modulation of Single Unit Responses

Although many studies have shown that attention to a stimulus can enhance the responses of individual cortical sensory neurons, little is known about how attention accomplishes this change in response. Here, we propose that attention-based changes in neuronal responses depend on the same response normalization mechanism that adjusts sensory responses whenever multiple stimuli are present. We have implemented a model of attention that assumes that attention works only through this normalization mechanism, and show that it can replicate key effects of attention. The model successfully explains how attention changes the gain of responses to individual stimuli and also why modulation by attention is more robust and not a simple gain change when multiple stimuli are present inside a neuron''s receptive field. Additionally, the model accounts well for physiological data that measure separately attentional modulation and sensory normalization of the responses of individual neurons in area MT in visual cortex. The proposal that attention works through a normalization mechanism sheds new light a broad range of observations on how attention alters the representation of sensory information in cerebral cortex.     

Haltere and visual inputs sum linearly to predict wing (but not gaze) motor output in tethered flying Drosophila

In the true flies (Diptera), the hind wings have evolved into specialized mechanosensory organs known as halteres, which are sensitive to gyroscopic and other inertial forces. Together with the fly''s visual system, the halteres direct head and wing movements through a suite of equilibrium reflexes that are crucial to the fly''s ability to maintain stable flight. As in other animals (including humans), this presents challenges to the nervous system as equilibrium reflexes driven by the inertial sensory system must be integrated with those driven by the visual system in order to control an overlapping pool of motor outputs shared between the two of them. Here, we introduce an experimental paradigm for reproducibly altering haltere stroke kinematics and use it to quantify multisensory integration of wing and gaze equilibrium reflexes. We show that multisensory wing-steering responses reflect a linear superposition of haltere-driven and visually driven responses, but that multisensory gaze responses are not well predicted by this framework. These models, based on populations, extend also to the responses of individual flies.     

Visual response properties of neck motor neurons in the honeybee

Recent behavioural studies have demonstrated that honeybees use visual feedback to stabilize their gaze. However, little is known about the neural circuits that perform the visual motor computations that underlie this ability. We investigated the motor neurons that innervate two neck muscles (m44 and m51), which produce stabilizing yaw movements of the head. Intracellular recordings were made from five (out of eight) identified neuron types in the first cervical nerve (IK1) of honeybees. Two motor neurons that innervate muscle 51 were found to be direction-selective, with a preference for horizontal image motion from the contralateral to the ipsilateral side of the head. Three neurons that innervate muscle 44 were tuned to detect motion in the opposite direction (from ipsilateral to contralateral). These cells were binocularly sensitive and responded optimally to frontal stimulation. By combining the directional tuning of the motor neurons in an opponent manner, the neck motor system would be able to mediate reflexive optomotor head turns in the direction of image motion, thus stabilising the retinal image. When the dorsal ocelli were covered, the spontaneous activity of neck motor neurons increased and visual responses were modified, suggesting an ocellar input in addition to that from the compound eyes.     

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.     

Modification of the courtship song by visual stimuli in the grasshopper Gomphocerus rufus (Acrididae)

ABSTRACT. Males of Gomphocerus rufus L. perform a courtship song consisting of repetitive units, each of which is composed of three subunits (S1, S2, S3). S1 is characterized mainly by slow and fast head rolling; S2 and S3 are distinguished by different types of leg-stridulation. These movements and the associated sounds were recorded during presentation of visual stimuli, either linear displacement of a living female or optomotor stimuli generated by a striped drum. Females moved artificially through the binocular visual field of a courting male with a velocity of 1 cm/s or more are mounted by the male from any subunit S1, S2 or S3, although under natural conditions mounting occurs only from S2. Thus above a critical velocity the courtship programme can be modified. Rotation of a striped drum about the yaw axis of the male during the slow S1 induces asymmetrical leg position, following movements of the head, and prolongation of S1. During S2 the male is especially sensitive to optomotor stimuli and responds with marked changes in body position. In S3 the intensity of the song is reduced, and its duration shortened. Fast drum movements interrupt the courtship programme. Rotation of the drum about the roll axis elicits optomotor head turning that interferes with the head rolling of S1. The fast phase of S1 and the frequency of head-rolling during S1 cannot be modified by optomotor stimulation. The results can be interpreted by assuming certain interactions between three central nervous elements: a calling-song generator, a head-rolling generator, and an optomotor centre.     

Persistent activity in limbic system neurons: neurophysiological and modeling perspectives

Neural activity persisting for one to hundreds of seconds has been postulated to be a substrate of memory. This review article illustrates examples of such activity in limbic system structures including the hippocampus, postsubiculum, and the anterodorsal thalamus. These neuronal responses include better known correlates with the spatial position as well as with head direction of the animal relative to its environment as well as other lesser known examples. Since head direction responses are greater when the animal is actively moving than when passively rotated, it has been proposed that there might be a general mechanism where the behavioral state of the animal can provide modulatory gating of such persistent signals. This would regulate the relative influence of these signals on downstream structures. Neural network attractor models of the head direction cell system are presented to demonstrate how these responses might originate, as well as the dynamics by which they are updated during movements.     

Rapid dynamics of contrast responses in the cat primary visual cortex

The visual information we receive during natural vision changes rapidly and continuously. The visual system must adapt to the spatiotemporal contents of the environment in order to efficiently process the dynamic signals. However, neuronal responses to luminance contrast are usually measured using drifting or stationary gratings presented for a prolonged duration. Since motion in our visual field is continuous, the signals received by the visual system contain an abundance of transient components in the contrast domain. Here using a modified reverse correlation method, we studied the properties of responses of neurons in the cat primary visual cortex to different contrasts of grating stimuli presented statically and transiently for 40 ms, and showed that neurons can effectively discriminate the rapidly changing contrasts. The change in the contrast response function (CRF) over time mainly consisted of an increment in contrast gain (CRF shifts to left) in the developing phase of temporal responses and a decrement in response gain (CRF shifts downward) in the decay phase. When the distribution range of stimulus contrasts was increased, neurons demonstrated decrement in contrast gain and response gain. Our results suggest that contrast gain control (contrast adaptation) and response gain control mechanisms are well established during the first tens of milliseconds after stimulus onset and may cooperatively mediate the rapid dynamic responses of visual cortical neurons to the continuously changing contrast. This fast contrast adaptation may play a role in detecting contrast contours in the context of visual scenes that are varying rapidly.     

The three-dimensional optomotor torque system ofDrosophila melanogaster

Summary The well known optomotor yaw torque response in flies is part of a 3-dimensional system. Optomotor responses around the longitudinal and transversal body axes (roll and pitch) with strinkingly similar properties to the optomotor yaw response are described here forDrosophila melanogaster. Stimulated by visual motion from a striped drum rotating around an axis aligned with the measuring axis, a fly responds with torque of the same polarity as that of the rotation of the pattern. In this stimulus situation the optomotor responses for yaw, pitch and roll torque have about the same amplitudes and dynamic properties (Fig. 2). Pronounced negative responses are measured with periodic gratings of low pattern wavelengths due to geometrical interference (Fig. 3). The responses depend upon the contrast frequency rather than the angular velocity of the pattern (Fig. 4). Like the optomotor yaw response, roll and pitch responses can be elicited by small field motion in most parts of the visual field; only for motion below and behind the fly roll and pitch responses have low sensitivity.The mutantoptomotor-blind ^H31 (omb ^H31) in which the giant neurones of the lobula plate are missing or severely reduced, is impaired in all 3 optomotor torque responses (Fig. 5) whereas other visual responses like the optomotor lift/thrust response and the landing response (elicited by horizontal front-to-back motion) are not affected (Heisenberg et al. 1978).We propose that the lobula plate giant neurons mediate optomotor torque responses and that the VS-cells in particular are involved in roll and pitch but not in lift/thrust control. This hypothesis accommodates various electrophysiological and anatomical observations about these neurons in large flies.Abbreviation EMD elementary movement detector     

Face-infringement space: the frame of reference of the ventral intraparietal area

Experimental studies have shown that responses of ventral intraparietal area (VIP) neurons specialize in head movements and the environment near the head. VIP neurons respond to visual, auditory, and tactile stimuli, smooth pursuit eye movements, and passive and active movements of the head. This study demonstrates mathematical structure on a higher organizational level created within VIP by the integration of a complete set of variables covering face-infringement. Rather than positing dynamics in an a priori defined coordinate system such as those of physical space, we assemble neuronal receptive fields to find out what space of variables VIP neurons together cover. Section 1 presents a view of neurons as multidimensional mathematical objects. Each VIP neuron occupies or is responsive to a region in a sensorimotor phase space, thus unifying variables relevant to the disparate sensory modalities and movements. Convergence on one neuron joins variables functionally, as space and time are joined in relativistic physics to form a unified spacetime. The space of position and motion together forms a neuronal phase space, bridging neurophysiology and the physics of face-infringement. After a brief review of the experimental literature, the neuronal phase space natural to VIP is sequentially characterized, based on experimental data. Responses of neurons indicate variables that may serve as axes of neural reference frames, and neuronal responses have been so used in this study. The space of sensory and movement variables covered by VIP receptive fields joins visual and auditory space to body-bound sensory modalities: somatosensation and the inertial senses. This joining of allocentric and egocentric modalities is in keeping with the known relationship of the parietal lobe to the sense of self in space and to hemineglect, in both humans and monkeys. Following this inductive step, variables are formalized in terms of the mathematics of graph theory to deduce which combinations are complete as a multidimensional neural structure that provides the organism with a complete set of options regarding objects impacting the face, such as acceptance, pursuit, and avoidance. We consider four basic variable types: position and motion of the face and of an external object. Formalizing the four types of variables allows us to generalize to any sensory system and to determine the necessary and sufficient conditions for a neural center (for example, a cortical region) to provide a face-infringement space. We demonstrate that VIP includes at least one such face-infringement space.     

Responses of Neurons of the Extrastriate Area 21b of the Cat Brain Cortex to Changes in Orientation of Moving Visual Stimuli

We studied the responses of neurons of the extrastriate cortical area 21b of the cat to changes in orientation of the movements of visual stimuli within the receptive field (RF) of the neuron under study. Our experiments demonstrated that 24 of 108 cells (22%) responded differentially to a certain extent to orientation of the movements of visual stimuli. As a whole, neurons of the area 21b did not demonstrate fine tuning on the optimum angle of orientation. In many cases, neuronal responses to different orientations of the movement of visual stimulus depended significantly on specific parameters of this stimulus (its shape, dimensions, and contrast). Some directionally sensitive neurons responded to a change in orientation of the movement of visual stimuli by modification of the index of directionality. We also studied spatial organization of the RF of neurons with the presentation of stationary visual stimuli. Comparison of the neuronal responses to a change in orientation of the movements of stimuli and to presentation of stationary stimuli showed that the correlation between the orientation sensitivity of the neuron under study and the stationary functional organization of its RF was insignificant. We hypothesize that inhibitory processes and subthreshold influences from a space surrounding the RF play a special role in the formation of the neuronal responses generated in the associative visual cortical regions to visual stimulation.     

Forward genetic analysis of visual behavior in zebrafish

The visual system converts the distribution and wavelengths of photons entering the eye into patterns of neuronal activity, which then drive motor and endocrine behavioral responses. The gene products important for visual processing by a living and behaving vertebrate animal have not been identified in an unbiased fashion. Likewise, the genes that affect development of the nervous system to shape visual function later in life are largely unknown. Here we have set out to close this gap in our understanding by using a forward genetic approach in zebrafish. Moving stimuli evoke two innate reflexes in zebrafish larvae, the optomotor and the optokinetic response, providing two rapid and quantitative tests to assess visual function in wild-type (WT) and mutant animals. These behavioral assays were used in a high-throughput screen, encompassing over half a million fish. In almost 2,000 F2 families mutagenized with ethylnitrosourea, we discovered 53 recessive mutations in 41 genes. These new mutations have generated a broad spectrum of phenotypes, which vary in specificity and severity, but can be placed into only a handful of classes. Developmental phenotypes include complete absence or abnormal morphogenesis of photoreceptors, and deficits in ganglion cell differentiation or axon targeting. Other mutations evidently leave neuronal circuits intact, but disrupt phototransduction, light adaptation, or behavior-specific responses. Almost all of the mutants are morphologically indistinguishable from WT, and many survive to adulthood. Genetic linkage mapping and initial molecular analyses show that our approach was effective in identifying genes with functions specific to the visual system. This collection of zebrafish behavioral mutants provides a novel resource for the study of normal vision and its genetic disorders.     

An analog VLSI implementation of a visual interneuron: enhanced sensory processing through biophysical modeling

Flies are capable of rapid, coordinated flight through unstructured environments. This flight is guided by visual motion information that is extracted from photoreceptors in a robust manner. One feature of the fly's visual processing that adds to this robustness is the saturation of wide-field motion-sensitive neuron responses with increasing pattern size. This makes the cell's responses less dependent on the sparseness of the optical flow field while retaining motion information. By implementing a compartmental neuronal model in silicon, we add this "gain control" to an existing analog VLSI model of fly vision. This results in enhanced performance in a compact, low-power CMOS motion sensor. Our silicon system also demonstrates that modern, biophysically-detailed models of neural sensory processing systems can be instantiated in VLSI hardware.     

Monkey and humans exhibit similar motion-processing mechanisms

Single cell recording studies have resulted in a detailed understanding of motion-sensitive neurons in non-human primate visual cortex. However, it is not known to what extent response properties of motion-sensitive neurons in the non-human primate brain mirror response characteristics of motion-sensitive neurons in the human brain. Using a motion adaptation paradigm, the direction aftereffect, we show that changes in the activity of human motion-sensitive neurons to moving dot patterns that differ in dot density bear a strong resemblance to data from macaque monkey. We also show a division-like inhibition between neural populations tuned to opposite directions, which also mirrors neural-inhibitory behaviour in macaque. These findings strongly suggest that motion-sensitive neurons in human and non-human primates share common response and inhibitory characteristics.     

Attention to stimulus features shifts spectral tuning of V4 neurons during natural vision

Previous neurophysiological studies suggest that attention can alter the baseline or gain of neurons in extrastriate visual areas but that it cannot change tuning. This suggests that neurons in visual cortex function as labeled lines whose meaning does not depend on task demands. To test this common assumption, we used a system identification approach to measure spatial frequency and orientation tuning in area V4 during two attentionally demanding visual search tasks, one that required fixation and one that allowed free viewing during search. We found that spatial attention modulates response baseline and gain but does not alter tuning, consistent with previous reports. In contrast, feature-based attention often shifts neuronal tuning. These tuning shifts are inconsistent with the labeled-line model and tend to enhance responses to stimulus features that distinguish the search target. Our data suggest that V4 neurons behave as matched filters that are dynamically tuned to optimize visual search.     

Distinct Acute Zones for Visual Stimuli in Different Visual Tasks in Drosophila

The fruit fly Drosophila melanogaster has a sophisticated visual system and exhibits complex visual behaviors. Visual responses, vision processing and higher cognitive processes in Drosophila have been studied extensively. However, little is known about whether the retinal location of visual stimuli can affect fruit fly performance in various visual tasks. We tested the response of wild-type Berlin flies to visual stimuli at several vertical locations. Three paradigms were used in our study: visual operant conditioning, visual object fixation and optomotor response. We observed an acute zone for visual feature memorization in the upper visual field when visual patterns were presented with a black background. However, when a white background was used, the acute zone was in the lower visual field. Similar to visual feature memorization, the best locations for visual object fixation and optomotor response to a single moving stripe were in the lower visual field with a white background and the upper visual field with a black background. The preferred location for the optomotor response to moving gratings was around the equator of the visual field. Our results suggest that different visual processing pathways are involved in different visual tasks and that there is a certain degree of overlap between the pathways for visual feature memorization, visual object fixation and optomotor response.