Wide-field Cells Research Articles

1104 Differential expressions of calcium-binding proteins in the superior colliculi of developing rats

The cytoarchitecture of the optic tectum of the Japanese quail, Coturnix coturnix japonica, was studied using the Golgi-Kopsch method, parvalbumin, calbindin and GABA immunohistochemistry and nicotinamide adenine dinucleotide phosphate-diaphorase histochemistry. Our results reveal a large number of different types of interneurons in the quail tectum opticum, only part of which are described in the chick or pigeon. Application of parvalbumin and calbindin immunohistochemistry and nicotinamide adenine dinucleotide phosphate-diaphorase histochemistry reveals the following lamination pattern: The stratum opticum, stratum griseum centrale and stratum album centrale remain unstained, while the laminae of the stratum griseum et fibrosum superficiale exhibit a roughly complementary staining pattern of calbindin (laminae c, d, e, f, g, i) and parvalbumin (laminae a, h, i). Nicotinamide adenine dinucleotide phosphate-diaphorase histochemistry yields a dense band in lamina i. The Golgi material reveals the following cell types in the stratum griseum et fibrosum superficiale: marginal cells in the stratum opticum and in lamina h and i, horizontal cells in laminae a and c, large and small radial cells in laminae b, d, h and i, multiform cells in lamina b, bitufted cells in lamina d and e, large pear-shaped cells in lamina g, wide-field cells in lamina j, and stellate cells in lamina j and in the stratum griseum centrale.We consider horizontal cells, bitufted cells, multiform cells and small radial cells to be GABAergic interneurons of the stratum griseum et fibrosum superficiale which seem to be more numerous than in the pigeon tectum opticum. Golgi impregnation and injection of Phaseolus vulgaris leucoagglutinin into the pretectal nucleus lentiformis yielded regularly distributed clusters of telodendra of pretectal axons in lamina d of the stratum griseum et fibrosum superficiale, which are identical in shape and position with axon plexus revealed by Golgi staining.

Responses to light of starburst amacrine cells.

1. Starburst amacrine cells were studied using whole cell patch recording. Displaced starburst cells were labeled in rabbit retinas by intraocular injection of 4,6-diamidino-2-phenylindole. The retinas were isolated and maintained in vitro. The inner limiting membrane and Müller cell endfeet were removed mechanically from small areas above the starburst cell bodies, allowing an unimpeded approach under visual control to the cells. A total of 104 cells was studied. 2. In voltage-clamp recordings, the cells responded to light with slow, graded inward and outward currents on which were superimposed smaller, rapid inward currents. The rapid inward currents appeared to be postsynaptic currents. 3. The receptive fields of the cells were mapped using small spots. They had an on-center, off-surround organization. Visualizing the dendrites by including Lucifer yellow in the patch pipette showed that the receptive fields' centers closely approximated the dendritic spread of the neurons. 4. The cells' responses to movement were tested with smooth movements or with two-spot apparent motion. No directional preference was seen for spots swept across the whole receptive field, for centrifugal movements, or for centripetal movements. 5. Bath-applied tetrodotoxin (TTX) or intracellularly applied lidocaine N-ethyl bromide (QX-314) had no effect on any component of the spontaneous or light-evoked activity. Depolarization of the cell bodies by injected current showed evidence of active conductances, but they were unaffected by TTX or QX-314. 6. 6-Cyano-7-nitroquionxyline-2,3-dione eliminated the small rapid currents, indicating that they depend on alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionic acid/kainate glutamate receptors. 7. Because it is unlikely that we voltage clamped the distalmost dendrites of these wide-field cells, uncertainties remain about rapid electrical events occurring in the dendrites. From a functional point of view, though, the fact that slow responses to distal photic stimulation were recorded at the soma suggests that the starburst cells could in principle integrate inputs across fairly substantial fractions of their total dendritic arbors. The extent to which this actually occurs remains to be learned.

Response characteristics of wide-field non-habituating non-directional motion detecting neurons in the optic lobe of the locust, Locusta migratoria

1. Extracellular recordings from wide-field nonhabituating non-directional (ND) motion detecting neurons in the second optic chiasma of the locust Locusta migratoria are presented. The responses to various types of stepwise moving spot and bar stimuli were monitored (Fig. 1) 2. Stepwise motion in all directions elicited bursts of spikes. The response is inhibited at stimulus velocities above 5°/s. At velocities above 10°/s the ND neurons are slightly more sensitive to motion in the horizontal direction than to motion in the vertical direction (Fig. 2). The ND cells have a preference for small moving stimuli (Fig. 3). 3. The motion response has two peaks. The latency of the second peak depends on stimulus size and stimulus velocity. Increasing the height from 0.1 to 23.5° of a 5°/s moving bar results in a lowering of this latency time from 176 to 130 ms (Fig. 4). When the velocity from a single 0.1° spot is increased from 1 to 16°/s, the latency decreases from 282 to 180 ms (Figs. 5–6). 4. A change-of-direction sensitivity is displayed. Stepwise motion in one particular direction produces a continuous burst of spike discharges. Reversal or change in direction leads to an inhibition of the response (Fig. 7). 5. It shows that non-directional motion perception of the wide-field ND cells can simply be explained by combining self-and lateral inhibition.

Amacrine cell interactions underlying the response to change in the tiger salamander retina

The neural circuitry and pharmacology underlying transient signal formation at the bipolar-amacrine cell interface were studied. Synaptic currents were measured with whole cell patch clamp in retinal slices. Cell types were identified with Lucifer yellow staining. Activity was initiated with puffs of kainate of known time course and spatial spread delivered at bipolar dendrites. OFF bipolar cells responded to kainate with a sustained inward current, but ON bipolar cells were silent. Two types of amacrine cell were found: (1) narrow field cells, with processes that extended laterally less than 200 microns, responding with a sustained inward current, and (2) wide field cells, with processes that extended laterally by up to 1 mm, responding with a brief transient inward current followed by a more sustained outward current. We pharmacologically dissected the synaptic interactions underlying the transient current in the wide field amacrine cell. In the presence of 5-aminovaleric acid (AVA), the time course of this transient current was increased so that it resembled the response of bipolar cells. Because AVA is a GABAB antagonist, it appears to block an opposing signal that truncates the sustained excitatory bipolar input, thereby generating the transient. GABAB specificity is confirmed by (1) block of the transient inward current by baclofen, a GABAB agonist, and (2) block of the baclofen effect by AVA. The site of GABAB action appears to be presynaptic to the amacrine cell membrane because neither baclofen nor AVA, in combination with picrotoxin, had a direct effect at the amacrine cell membrane. GABAB receptors are often found at presynaptic terminals where they modulate calcium or potassium conductances. It has been shown that bipolar cell terminals receive a GABAergic synaptic input (Vaughn et al., 1981; Wu et al., 1981; Tachibana and Kaneko, 1987). The narrow field sustained-responding amacrine cells appear to be GABAergic (Werblin et al., 1988). This suggests that transient activity measured in wide field amacrine cells is formed at a population of bipolar cell terminals by GABAergic feedback from narrow field amacrine cells at GABAB receptors.

On the action of intravenous picrotoxin in the sensorimotor cortex of the cat

The action of topical convulsants, such as strychnine, is not exerted equally on all sets of neurons in the sensorimotor cortex of cats. Small-field neurons near the surface are influenced whereas deeper, wide-field neurons are affected only indirectly. The agent, picrotoxin, was used to test whether or not the deeper neurons are spared the effects of topical convulsants simply because of their location. Picrotoxin, injected intravenously, produced enhancement of the corticofugal reflex discharge evoked by stimulation of any of the four paws and by auditory stimulation. The surface-recorded primary evoked response was also enhanced but only slightly, far less than with topical application. The evoked response in the medial lemniscus was not altered by picrotoxin, but that in the thalamic radiations was enhanced. The drug diazepam, injected intravenously, diminished the enhancements of both the corticofugal reflex discharge and the evoked potential, in some cases reducing the responses to amplitudes smaller than control values. Single-cell recordings in other laboratories have shown that intravenous picrotoxin converts small-field cells to wide-field cells, and that diazepam reverses this effect. The increase in the surface-recorded primary response and the size of the increase in the corticofugal reflex suggest that there is also a direct effect on wide-field neurons or on the pathway leading to them.

Excitability changes along pyramidal tract axons after sensory stimulation

Recordings were made extracellularly of the activity of single pyramidal tract (PT) neurons in the forepaw focus of the cat's postcruciate cerebral cortex. Activity was evoked antidromically by near-threshold stimulation of the contralateral dorsolateral funiculus of the C6 spinal cord (corticospinal tract), the ipsilateral medullary pyramid, the ipsilateral cerebral peduncle, and the ipsilateral internal capsule. Orthodromic activity was initiated by shocks to each of the four paws. The excitability of PT axons at the spinal cord, medullary pyramid, cerebral peduncle, and internal capsule was tested by measuring the threshold to antidromic activation in conditioning-testing interaction. The PT axons with small contralateral receptive fields (small-field cells) showed no change in excitability at any of the four test sites after stimulation of any of the four paws. In contrast, most PT axons with large bilateral receptive fields (wide-field cells) showed increases in excitability after stimulation of the contralateral forepaw at one or more of the test sites, in many cases, at all four sites. Although not tested in all neurons, increases in excitability of wide-field axons were also seen after stimulation of the ipsilateral forepaw and the contralateral and ipsilateral hind paws. The increased excitability was detectable 20 to 25 ms after the contralateral forepaw stimulus, was maximum at 25 to 30 ms, and then returned to baseline by 75 to 100 ms. Maximum changes in excitability varied from 5% to more than 60% in different axons. The time course of the change in excitability was nearly the same at each site, but the magnitude of the change was most often greater at the pyramid and cerebral peduncle than at the internal capsule. In some cells, a period of decreased excitability, in most cases apparent inexcitability, followed the period of increased excitability. This could also be observed at all four test sites. The period of increased excitability most likely resulted from depolarization of terminals of branches of the PT axon near the testing site, whereas the period of decreased excitability may have resulted from strong depolarization or hyperpolarization of such terminals or from hyperpolarization of one or more nodes of Ranvier, the site situated nearer to the soma than the test site.

Neuronal mechanisms subserving directional selectivity in the locust optomotor system

1. The locust optomotor interneurons show velocity-response functions independent of pattern wavelength over a wide range. Thus the conditions for asymmetric direction detecting networks are fulfilled and this type of network can be used as the basis for a model. 2. When the pattern is moved during a short dark period the optomotor interneurons respond on reillumination of the pattern depending on the direction of displacement. These responses appear equivalent to behaviour previously described as optokinetic memory. 3. Experiments where the magnitude of pattern displacement was varied reveal that the type 1 (M1) optomotor interneuron receives inputs from small field cells (field dia. 1.5°). Interactions occur between every fifth cell along a horizontal row. 4. The type 2 (M2) neuron receives inputs from similar small field cells, with every fifth cell along a horizontal row forming an interacting pair. As well, the M2 neuron receives inputs from wider field cells (field dia. 2.5°–4°) and here the receptive fields of interacting pairs are separated by a distance equivalent to six ommatidia. 5. By varying the duration of the dark period it was seen that the lateral interactions of the M1 networks have only a short duration, thus mediating a response to fast movements. A selective facilitation explains the high discharge of these neurons to long slow movements. 6. The excitatory lateral interactions between the wide field cells connecting to the M2 neuron show a double peaked time course which corresponds well with the upper range of the M2 velocity-response function. 7. The experimental data can now be fitted to precise models for the inputs to the M1 and M2 neurons.

On the identification of movement detectors in the fly optic lobe

Intracellular recordings were made in the lobula-lobula plate ganglia of the optic lobes of the blowfliesCalliphora erythrocephala, Phaenicia sericata, and the flesh-flySarcophaga (species unknown) with the following results: 1. This region of the optic lobe is electrically very active. A large variety of response types were encountered. We concentrated upon recording from directionally selective movement detectors (DSMD's). 2. We were able to record from all eight classes of DSMD's reported previously from extracellular recordings. We found that it was possible to impale selectively a vertical or a horizontal DSHD, even though these neurons cannot be seen in the live preparation. Recordings were stable for as long as 40 min in cells that subsequent intracellular staining showed to be 2–10 μm in diameter. 3. Iontophoretic injection of the fluorescent dye procion yellow M4RS works very well in this system. We have achieved 100% recovery of injected cells, with partial fills being a rarity. 4. To date all DSMD's were elements of the lobula plate. 5. DSMD's with preferred directions in the horizontal plane lie in the anterior portion of the lobula plate and project to the ventral periesophageal region. The anatomical “horizontal system” described by Pierantoni (1973) and Strausfeld (1975) are horizontal DSMD's. Smaller cells, mimetic to the “horizontal system” are also horizontal DSMD's. Wide-field cells (Strausfeld, 1970, 1975) may be horizontal DSMD's. 6. DSMD's with preferred directions in the vertical plane lie in the posterior region of the lobula plate and project to the dorsal periesophageal region. These cells are a system of small diameter (2–4 μm) elements that are in close association with a system of larger cells (“vertical system”) described by Pierantoni (1973) and Strausfeld (1975). 7. Intracellular recordings established directly that some horizontal and vertical DSMD's have binocular visual fields.

Relevance of the callosal transfer in defining the peripheral reactivity of somesthetic cortical neurones.

Experiments were performed in 13 chloralose-anaesthetized, curarized cat preparations (monitoring of rectal temperature, heart rate, expired pCO2 and EEG), in order to ascertain whether, and to what extent, the reactivity to ipsilateral skin shocks of the neurones of the anterior ectosylvian and anterior suprasylvian gyri (AEG and ASG, respectively) is dependent on the callosal output of the somatosensory areas of the contralateral hemisphere. Indeed, we knew from previous experiments that a high proportion of AEG and ASG neurones having bilateral peripheral receptive fields (PRFs) can be excited by direct stimulation of the contralateral homonymous areas, and that the callosal fibres originating in the latter carry somesthetic impulses related to contralateral PRFs. A preliminary analysis was carried out on the amplitude and latency relationships between the evoked potentials (EP) recorded simultaneously from the two hemispheres and from the corpus callosum (CC) following stimulation of the forepaw of one side. The results obtained showed good correlations between the onset and development of the EPs picked up from the hemisphere ipsilateral to the stimulated skin, on the one hand, and onset and development of the EPs recorded from the contralateral hemisphere and the corpus callosum, on the other. At a further stage of the experiments, the EPs elicited upon ipsilateral and contralateral skin shocks in the AEG-ASG area have been recorded and averaged before, during and after the reversible inactivation of callosal somesthetic transmission. This was achieved by applying polarizing currents (0.2-1 mA) to the rostral portion of the CC, adequacy and reversibility of this method having been tested by observing, respectively, suppression and prompt restoration of transcallosal EPs and of the asynaptic spiking produced by cortical cells when antidromically invaded from contralateral homotopic cortex. It was seen that during CC blockade the EPs elicited in the AEG-ASG areas did not show any change either in amplitude or time-course if brought about by contralateral peripheral stimulation, whereas those evoked by ipsilateral skin shocks exhibited significant reduction, which was related to the strength of CC polarization and to the reduction of transcallosal EPs. In control experiments similar effects were observed after ablation of somatosensory areas of the hemisphere which send off somesthetic callosal impulses, whereas strychninization of these areas caused effects opposite in sign, i.e., enhancement of the ipsilateral but not of the contralateral EPs in the areas of the untreated hemisphere. By testing the effects of CC polarization on single AEG-ASG neurones, it was observed that the responses of units linked only with contralateral PRFs (Group I; 7 units tested) were unaffected by callosal polarization. The discharges of neurones provided with wide and bilateral PRFs (Group II; 27 units tested) were not affected if elicited by contralateral PRF shocks but were deeply impaired (in 11 neurones out the 27) when provoked by ipsilateral PRF stimulation. The effect consisted chiefly of the disappearance of the first high peak of the PSTHs, and when recording intracellularly graded events, it was mirrored by a large decrease of the postsynaptic excitatory potentials elicited in Group II neurones by ipsilateral PRF shocks. A late scattered histographic component was identified in the PSTHs of such cells, which did not appear to be significantly altered during CC blockade. These effects were observed on the ipsilateral responses of 11 out of the 27 Group II neurones so tested whereas the ipsilateral PSTHs of the remaining 16 Group II neurones either did not undergo significant changes during the callosal blockade or escaped evaluation because of high spontaneous shifts of neural responsiveness. The results are discussed mainly with a view to the possible functional role of the specific somesthetic callosal fibres in defining ipsilateral reactivity for the wide-field cells of the AEG-ASG area.

Congenital Malformations of the Central Nervous System in Scotland

The vertebrate retina has the remarkable ability to support visual function under conditions of limited illumination, including the processing of signals evoked by single photons. Dim-light vision is regulated by several adaptive mechanisms. The mechanism explored in this study is responsible for increasing the light sensitivity and operational range of rod bipolar cells, the retinal neurons operating immediately downstream of rod photoreceptors. This sensitization is achieved through the sustained dopamine-dependent GABA release from other retinal neurons. Our goals were to identify the cell type responsible for the GABA release and the site of its modulation by dopamine. Previous studies have suggested the involvement of amacrine and/or horizontal cells. We now demonstrate, using mice of both sexes, that horizontal cells do not participate in this mechanism. Instead, sustained GABA input is provided by a subpopulation of wide-field amacrine cells, which stimulate the GABA_C receptors at rod bipolar cell axons. We also found that dopamine does not act directly on either of these cells. Rather, it suppresses inhibition imposed on these wide-field cells by another subpopulation of upstream GABAergic amacrine cells, thereby sustaining the GABA_C receptor activation required for rod bipolar cell sensitization. <b>SIGNIFICANCE STATEMENT</b> The vertebrate retina has an exquisite ability to adjust information processing to ever-changing conditions of ambient illumination, from bright sunlight to single-photon counting under dim starlight. Operation under each of these functional regimes requires an engagement of specific adaptation mechanisms. Here, we describe a mechanism optimizing the performance of the dim-light channel of vision, which consists of sensitizing rod bipolar cells by a sustained GABAergic input originating from a population of wide-field amacrine cells. Wide-field amacrine cells span large segments of the retina, making them uniquely equipped to normalize and optimize response sensitivity across distant receptive fields and preclude any bias toward local light-intensity fluctuations.