Gamma-aminobutyric acid and GABA_A receptors are involved in directional selectivity of pretectal neurons in pigeons

The present study describes the effects of gamma-aminobutyric acid (GABA) and its antagonists, bicuculline and 2-hydroxysaclofen, on visual responses of neurons in the pigeon nucleus lentiformis mesencephali (nLM). The results indicate that GABA significantly reduces both spontaneous activity and visual responsiveness, and GABAA antagonist bicuculline but not GABAB antagonist 2-hydroxysaclofen enhances visual responses of nLM cells examined. Furthermore, inhibition produced by motion in the null-direction of pretectal neurons is diminished by bicuculline but not by 2-hydroxysaclofen. It is therefore concluded that the null-direction inhibition of directional cells in the pigeon nLM is predominantly mediated by GABA and GABAA receptors. This inhibition may at least in part underlie directional asymmetry of optokinetic responses.     

Neural mechanisms of tactile motion integration in somatosensory cortex

How are local motion signals integrated to form a global motion percept? We investigate the neural mechanisms of tactile motion integration by presenting tactile gratings and plaids to the fingertips of monkeys, using the tactile analogue of a visual monitor and recording the responses evoked in somatosensory cortical neurons. The perceived directions of the gratings and plaids are measured in parallel psychophysical experiments. We identify a population of somatosensory neurons that exhibit integration properties comparable to those induced by analogous visual stimuli in area MT and find that these neural responses account for the perceived direction of the stimuli across all stimulus conditions tested. The preferred direction of the neurons and the perceived direction of the stimuli can be predicted from the weighted average of the directions of the individual stimulus features, highlighting that the somatosensory system implements a vector average mechanism to compute tactile motion direction that bears striking similarities to its visual counterpart.     

Gamma-aminobutyric acid and GABAA receptors are involved in directional selectivity of pretectal neurons in pigeons

The present study describes the effects of gamma-aminobutyric acid (GABA) and its antagonists, bicuculline and 2-hydroxysaclofen, on visual responses of neurons in the pigeon nucleus lentiformis mesencephali (nLM). The results indicate that GABA significantly reduces both spontaneous activity and visual responsiveness, and GABA_A antagonist bicuculline but not GABA_B antagonist 2-hydroxysaclofen enhances visual responses of nLM cells examined. Furthermore, inhibition produced by motion in the null-direction of pretectal neurons is diminished by bicuculline but not by 2-hydroxysaclofen. It is therefore concluded that the null-direction inhibition of directional cells in the pigeon nLM is predominantly mediated by GABA and GABA_A receptors. This inhibition may at least in part underlie directional asymmetry of optokinetic responses.     

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.     

蛤蚧豆状核的结构及其与顶盖前端的纤维联系

运用Nissl法和辣根过氧化物酶(horseradish peroxidase,HRP)追踪标记技术,研究蛤蚧(Gekko gecko)豆状核的结构及其与顶盖前端的纤维联系。Nissl染色显示,蛤蚧豆状核细胞大小没有明显差别,由背内侧细胞密集部和腹外侧细胞稀疏部组成。将HRP注射于顶盖前端,结果豆状核背内侧部和腹外侧部分别接受同侧顶盖前端脑室内、外侧纤维的传入,核内标记有浓密的神经丛和大量纤维末梢,并在该核腹外侧部及其邻近区域发现少量大胞体标记细胞。推测豆状核腹外侧部的大胞体细胞及其邻近区域的大胞体细胞可能具有相同的功能,且该核可能形成离顶盖通路和副视系统相联系的交通要道。     

Rats spontaneously perceive global motion direction of drifting plaids

Computing global motion direction of extended visual objects is a hallmark of primate high-level vision. Although neurons selective for global motion have also been found in mouse visual cortex, it remains unknown whether rodents can combine multiple motion signals into global, integrated percepts. To address this question, we trained two groups of rats to discriminate either gratings (G group) or plaids (i.e., superpositions of gratings with different orientations; P group) drifting horizontally along opposite directions. After the animals learned the task, we applied a visual priming paradigm, where presentation of the target stimulus was preceded by the brief presentation of either a grating or a plaid. The extent to which rat responses to the targets were biased by such prime stimuli provided a measure of the spontaneous, perceived similarity between primes and targets. We found that gratings and plaids, when used as primes, were equally effective at biasing the perception of plaid direction for the rats of the P group. Conversely, for the G group, only the gratings acted as effective prime stimuli, while the plaids failed to alter the perception of grating direction. To interpret these observations, we simulated a decision neuron reading out the representations of gratings and plaids, as conveyed by populations of either component or pattern cells (i.e., local or global motion detectors). We concluded that the findings for the P group are highly consistent with the existence of a population of pattern cells, playing a functional role similar to that demonstrated in primates. We also explored different scenarios that could explain the failure of the plaid stimuli to elicit a sizable priming magnitude for the G group. These simulations yielded testable predictions about the properties of motion representations in rodent visual cortex at the single-cell and circuitry level, thus paving the way to future neurophysiology experiments.     

Retinal projections in the Northern Water snake Natrix sipedon sipedon (L.)

Retinal projections were studied experimentally in the Northern water snake using modifications of the Nauta silver impregnation technique. Contralaterally, the retina projects to nucleus geniculatus lateralis pars dorsalis and pars ventralis, nucleus lentiformis mesencephali and nucleus geniculatus pretectalis. A sparse projection was also observed to nucleus ovalis. An additional afferent thalamic projection to nucleus ventrolateralis was found in two cases. The retina projects ipsilaterally to the dorsolateral portion of nucleus geniculatus lateralis pars dorsalis, and sparsely to nucleus lentiformis mesencephali and nucleus geniculatus pretectalis. Nucleus posterodorsalis receives dense bilateral retinal projections. Contralaterally, the retina also projects to the superficial layers of the tectum (layers 8–13 of Ramón) and to nucleus opticus tegmenti. Armstrong's findings that the retinal projections in Natrix are qualittatively similar to those in lizards were confirmed. However there are marked quantitative differences among the various pathways and their corresponding nuclei. These differences are particularly striking in comparing the visual projections to the dorsal thalamus, the retino-tecto-rotundal and the retino-geniculate systems. The first is reduced in volume and the second is markedly increased in volume in comparison with lizards. These data lend support to the theories of Walls that snakes evolved from fossorial lizards and of Underwood that the eyes of these lizards underwent reduction but not complete degeneration. Qualitatively the retinal projections are conservative among lizards and snakes, but a history of reduction of these pathways in ancestral snakes with a selective increase in the retino-geniculate system as a surface niche was reattained is reflected in the anatomy of this ophidian visual system.     

Dichoptic plaids may rival, but their motions can integrate

When the eyes view incompatible images, binocular rivalry usually results: image constituents in corresponding parts of the monocular visual fields are not perceived simultaneously. We asked naive undergraduates to view dichoptic, dioptic, and monoptic plaids. The dichoptic images evoked strong binocular rivalry when contrast was high, especially if the component gratings were set in motion. Nevertheless, the subjects' visual systems integrated the motion information across the two eyes, producing a unitary motion percept that did not reflect the image in either eye alone. By manipulating the relative spatial scale of the gratings, we affected how well the motion cohered: the results were remarkably similar between dichoptic and traditional dioptic plaids. By manipulating the relative speed of the gratings, we systematically affected the perceived direction of motion of the plaids; these results were also remarkably similar for dichoptic and dioptic plaids. Thus, the motion analysis of dichoptic and dioptic plaids is proceeding according to very similar rules, even though the dichoptic images are incompatible and evoke binocular rivalry.     

Internuclear connections between the pretectum and the accessory optic system in Salamandra salamandra

Summary Application of horseradish peroxidase into the posterior thalamic and basal optic neuropils of Salamandra salamandra (L.) revealed strong reciprocal connections between the pretectum and the accessory optic system. Pretectal neurons located within the periventricular gray matter project to the basal optic neuropil distributing their terminals over the whole extent of this neuropil. A well developed nucleus of the basal optic neuropil, with its neurons within and medial to this neuropil, projects to the posterior thalamic neuropil. Its terminals appear to be located selectively within the core of the posterior thalamic neuropil which receives no ipsilateral retinal afferents.The pretectum and the accessory optic system are reciprocally connected to a ventral tegmental nucleus, which has not previously been described in urodeles. This nucleus is located immediately dorsal to the oculomotor and trochlear nuclei and extends from the oculomotor root to the middle of the trochlear nucleus.Dendrites of the nucleus of Darkschewitsch reach the posterior thalamic neuropil but mainly enter the rostral tegmental neuropil, while the dendrites of the nucleus of the medial longitudinal fasciculus ramify within the basal optic neuropil and the anterior tegmental neuropil with minor branches in the caudal posterior thalamic neuropil.     

Retinal projections in a snake, Thamnophis sirtalis

The retinofugal projections of the snake Thamnophis sirtalis were studied by the method of experimentally induced Wallerian degeneration stained by the Fink-Heimer method. The retinal ganglion cells project to all parts of the contralateral lateral geniculate complex, nucleus lentiformis mesencephali, nucleus geniculatus pretectalis, nucleus posterodorsalis, basal optic nucleus and superficial layers of the optic tectum. In addition, the retinofugal projections were observed terminating in portions of the ipsilateral lateral geniculate complex and nucleus posterodorsalis. Examination of the morphology of the retinal terminal areas stained for Nissl substance with cresyl violet led to the conclusion that these regions are well differentiated and should not be considered poorly developed when compared with other reptilian forms such as turtles.     

Identification of Retinal Ganglion Cells and Their Projections Involved in Central Transmission of Information about Upward and Downward Image Motion

The direction of image motion is coded by direction-selective (DS) ganglion cells in the retina. Particularly, the ON DS ganglion cells project their axons specifically to terminal nuclei of the accessory optic system (AOS) responsible for optokinetic reflex (OKR). We recently generated a knock-in mouse in which SPIG1 (SPARC-related protein containing immunoglobulin domains 1)-expressing cells are visualized with GFP, and found that retinal ganglion cells projecting to the medial terminal nucleus (MTN), the principal nucleus of the AOS, are comprised of SPIG1⁺ and SPIG1⁻ ganglion cells distributed in distinct mosaic patterns in the retina. Here we examined light responses of these two subtypes of MTN-projecting cells by targeted electrophysiological recordings. SPIG1⁺ and SPIG1⁻ ganglion cells respond preferentially to upward motion and downward motion, respectively, in the visual field. The direction selectivity of SPIG1⁺ ganglion cells develops normally in dark-reared mice. The MTN neurons are activated by optokinetic stimuli only of the vertical motion as shown by Fos expression analysis. Combination of genetic labeling and conventional retrograde labeling revealed that axons of SPIG1⁺ and SPIG1⁻ ganglion cells project to the MTN via different pathways. The axon terminals of the two subtypes are organized into discrete clusters in the MTN. These results suggest that information about upward and downward image motion transmitted by distinct ON DS cells is separately processed in the MTN, if not independently. Our findings provide insights into the neural mechanisms of OKR, how information about the direction of image motion is deciphered by the AOS.     

The optokinetic response in wild type and white zebra finches

Optic flow is a main source of information about self movement and the three-dimensional composition of the environment during locomotion. It is processed by the accessory optic system in all vertebrates. The optokinetic response is elicited by rotational optic flow, e.g. in a rotating drum lined with vertical stripes. We investigated here the effect of rotational optic flow on the optokinetic response in wild type and white zebra finches. The highest stimulus velocity eliciting an optokinetic response (upper velocity threshold) was dependent on stimulus direction and illumination level, but was not different between the colour morphs. The upper velocity threshold was higher with temporal to nasal movements in monocularly exposed birds and symmetrical with binocular exposure. Its increase with illumination level followed Fechner's law and reached a plateau at about 560 Lux. In bright daylight, white birds did not show optokinetic responses. We conclude that the altered wiring of the visual system of white birds has no influence on accessory optic system function. The unwillingness of white birds to respond with optokinetic response in bright daylight may be due to a substantial lack of inhibition within the visual system as demonstrated earlier, which may enhance the sensibility to glare.     

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.     

Neural organization of the circadian system of the cockroach Leucophaea maderae

The cockroach Leucophaea maderae was the first animal in which lesion experiments localized an endogenous circadian clock to a particular brain area, the optic lobe. The neural organization of the circadian system, however, including entrainment pathways, coupling elements of the bilaterally distributed internal clock, and output pathways controlling circadian locomotor rhythms are only recently beginning to be elucidated. As in flies and other insect species, pigment-dispersing hormone (PDH)-immunoreac- tive neurons of the accessory medulla of the cockroach are crucial elements of the circadian system. Lesions and transplantation experiments showed that the endogeneous circadian clock of the brain resides in neurons associated with the accessory medulla. The accessory medulla is organized into a nodular core receiving photic input, and into internodular and peripheral neuropil involved in efferent output and coupling input. Photic entrainment of the clock through compound eye photoreceptors appears to occur via parallel, indirect pathways through the medulla. Light-like phase shifts in circadian locomotor activity after injections of γ-aminobutyric acid (GABA)- or Mas-allatotropin into the vicinity of the accessory medulla suggest that both substances are involved in photic entrainment. Extraocular, cryptochrome-based photoreceptors appear to be present in the optic lobe, but their role in photic entrainment has not been examined. Pigment-dispersing hormone-immunoreactive neurons provide efferent output from the accessory medulla to several brain areas and to the peripheral visual system. Pigment-dispersing hormone-immunoreactive neurons, and additional heterolateral neurons are, furthermore, involved in bilateral coupling of the two pacemakers. The neuronal organization, as well as the prominent involvement of GABA and neuropeptides, shows striking similarities to the organization of the suprachiasmatic nucleus, the circadian clock of the mammalian brain.     

Gamma-aminobutyric acid and GABAA receptors are involved in directional selectivity of pretectal neurons in pigeons

The present study describes the effects of gamma-aminobutyric acid (GABA) and itsantagonists, bicuculline and 2-hydroxysaclofen, on visual responses of neurons in the pigeon nucleuslentiformis mesencephali (nLM). The results indicate that GABA significantly reduces bothspontaneous activity and visual responsiveness, and GABAA antagonist bicuculline but not GABABantagonist 2-hydroxysaclofen enhances visual responses of nLM cells examined. Furthermore,inhibition produced by motion in the null-direction of pretectal neurons is diminished by bicucullinebut not by 2-hydroxysaclofen. It is therefore concluded that the null-direction inhibition of directionalcells in the pigeon nLM is predominantly mediated by GABA and GABAA receptors. This inhibitionmay at least in part underlie directional asymmetry of optokinetic responses.     

The intrinsic neuronal organisation of the nucleus of the basal optic root in the domestic chicken; a light and electron microscopic study using anterograde tracers and postembedding GABA-immunostaining

The intrinsic neuronal organisation in the nucleus of the basal optic root of chickens was investigated. The divergent connections with various areas and the functional complexity of the nucleus require a complex intrinsic structural arrangement. Therefore, an analysis of Golgi impregnated material, ultrastructure, GABA-immunocytochemistry and biotinylated dextran-amine anterograde tracer analysis of the nucleus was carried out. In the Golgi analysis, a characteristic dendritic ramification pattern of two types of putative projection neurons was observed. These neurons form dendritic nests with their overlapping dendritic terminal sections, that develop synaptic fields with the optic fibre terminals. These synaptic fields were confirmed by electron microscopy. GABA-immunopositive terminals synapse with distinct loci of the dendritic trees of projection neurons; they may therefore play an important role in the inhibitory-modulatory system of the nucleus of the basal optic root. The GABA-immunopositive terminals derive from small and/or elongated local circuit neurons which receive retinal afferents, and from myelinated fibres afferents to the nucleus of unknown origin.     

Development of optokinetic neuronal responses in the pretectum and horizontal optokinetic nystagmus in unilaterally enucleated rats

Responses of single units to constant-velocity rotations of the visual surround (0.25-10 degrees/s) were studied in the pretectum of unilateral enucleated rats at different ages. Enucleation was performed either in the first postnatal week ("early" enucleated rats) or in the adult stage ("late" enucleated rats). Pretectal unitary responses were recorded in early enucleated animals at postnatal day 20-21, 36-49 and, in both experimental groups, in the adult stage. Optokinetic ocular nystagmus was studied in early and late enucleated rats in the adult stage. Gain of optokinetic nystagmus in temporo-nasal stimulus direction was not changed for visual surround rotations of up to 20 degrees/s compared to controls in monocular viewing conditions. At higher stimulus velocities, however, the gain dropped. In naso-temporal stimulus direction, optokinetic nystagmus was improved in gain for optokinetic pattern motions of up to 5-10 degrees/s. There were only minor differences in the gain behaviour of optokinetic nystagmus obtained from early or late enucleated rats. The optokinetic responses of pretectal neurons obtained from early and late enucleated rats were reduced in sensitivity by more than 50%. The response patterns of neurons recorded in the contralateral pretectum relative to the intact eye were shifted by a large amount from directional selective to directional nonselective response types. No such changes were obtained in the ipsilateral pretectum. In contrast to normal rats, there were very few directional selective units responding to temporo-nasal pattern motion. On the other hand, a large proportion of directional selective units responded to naso-temporal pattern motion. These latter units were found in both early and late enucleated rats. A similar response type has previously been described for intact young rats but not for adult rats. The velocity tuning curve of pretectal units studied in the adult stage was similar in shape in early and late enucleated rats and resembled that obtained from enucleated or intact young animals. Our results show that response sensitivity, direction and velocity tuning of pretectal units depend crucially on retinal afferent input originating from both eyes. The data suggest that the response characteristics of many of the pretectal units that are considered to be important for mediating optokinetic reflexes depend on interpretectal signal processing using commissural connections. There is very little evidence for an adaptative structural plasticity of the optokinetic system following loss of one eye. The reduced asymmetry observed in gain of optokinetic responses correlated in both early and late enucleated rats with the shifts observed in the distribution of pretectal unitary response patterns.     

Neural basis of the magnetic compass: interactions of visual,magnetic and vestibular inputs in the pigeon's brain

Summary Single unit electrical activity was recorded extracellularly in the lateral and superior vestibular nuclei, the vestibulo-cerebellum and the nucleus of the basal optic root (nBOR) under earth-strength magnetic stimulation. Units in the vestibular system responded with either inhibition or excitation to the magnetic stimuli only if the animal was moved out of the horizontal plane. No responses to the artificial magnetic field were observed when enucleation was performed contralateral to the recording site or when magnetic stimuli were applied in total darkness.Most of the units in the nBOR responded to slow direction changes in the magnetic field with a gradual augmentation of activity. The responses were generally weak but nevertheless statistically significant and seemed to be direction selective, i.e. different cells responded to a different distinct direction change of the magnetic field.The results indicate, that information provided by magnetic cues in the earth's strength range may be conveyed from the visual to the vestibular system via a projection from the nBOR and then related to active movements of the animal.Abbreviation nBOR nucleus of the basal optic root     

A Model of Binocular Rivalry and Cross-orientation Suppression

Binocular rivalry and cross-orientation suppression are well-studied forms of competition in visual cortex, but models of these two types of competition are in tension with one another. Binocular rivalry occurs during the presentation of dichoptic grating stimuli, where two orthogonal gratings presented separately to the two eyes evoke strong alternations in perceptual dominance. Cross-orientation suppression occurs during the presentation of plaid stimuli, where the responses to a component grating presented to both eyes is weakened by the presence of a superimposed orthogonal grating. Conventional models of rivalry that rely on strong competition between orientation-selective neurons incorrectly predict rivalry between the components of plaids. Lowering the inhibitory weights in such models reduces rivalry for plaids, but also reduces it for dichoptic gratings. Using an exhaustive grid search, we show that this problem cannot be solved simply by adjusting the parameters of the model. Instead, we propose a robust class of models that rely on ocular opponency neurons, previously proposed as a mechanism for efficient stereo coding, to yield rivalry only for dichoptic gratings, not for plaids. This class of models reconciles models of binocular rivalry with the divisive normalization framework that has been used to explain cross-orientation. Our model makes novel predictions that we confirmed with psychophysical tests.     

On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly

A new class of large-field tangential neurones (Figure Detection (FD-) cells) has been found and analysed in the lobula plate, the posterior part of the third visual ganglion, of the fly by combined extra-and intracellular recording as well as Lucifer Yellow injection. The FD-cells are likely to play a prominent role in figure-ground discrimination. Together with the Horizontal Cells, the output elements of the neuronal network underlying the optomotor course control reaction, they seem to be appropriate to account for the characteristic yaw torque response to relative motion. The FD-cells might thus compensate for the deficits of the Horizontal Cells with respect to figureground discrimination (see Egelhaaf, 1985a).The FD-cells are directionally selective for either front-to-back (FD 1, FD 4) or back-to-front motion (FD 2, FD 3). Their excitatory receptive fields cover part of (FD 1, FD 2, FD 3) or the entire horizontal extent (FD 4) of the visual field of one eye. Their most important common property in the context of figureground discrimination is that they are more sensitive to relatively small objects than to spatially extended patterns. Their response to a small figure is much reduced by simultaneous large-field motion in front of the ipsi-as well as the contralateral eye. This large-field inhibition is either directionally selective or bidirectional, depending on the FD-cell under consideration. The main dendritic arborization of all FD-cells resides in the lobula plate. Their axonal projections lie in either the ipsi-or contralateral posterior optic foci and, thus, in the same area as the terminals of the Horizontal Cells. The FD-cells are, therefore, appropriate candidates for output elements of the optic lobes involved in figure-ground discrimination.