Dynamic relationship between the slow potential and spikes in cockroach ocellar neurons

The relationship between the slow potential and spikes of second-order ocellar neurons of the cockroach, Periplaneta americana, was studied. The stimulus was a sinusoidally modulated light with various mean illuminances. A solitary spike was generated at the depolarizing phase of the modulation response. Analysis of the relationship between the amplitude/frequency of voltage modulation and the rate of spike generation showed that (a) the spike initiation process was bandpass at approximately 0.5-5 Hz, (b) the process contained a dynamic linearity and a static nonlinearity, and (c) the spike threshold at optimal frequencies (0.5-5 Hz) remained unchanged over a mean illuminance range of 3.6 log units, whereas (d) the spike threshold at frequencies of less than 0.5 Hz was lower at a dimmer mean illuminance. The voltage noise in the response was larger and the mean membrane potential level was more positive at a dimmer mean illuminance. Steady or noise current injection during sinusoidal light stimulation showed that (a) the decrease in the spike threshold at a dimmer mean illuminance was due to the increase in the noise variance: the noise had facilitatory effects on the spike initiation; and (b) the change in the mean potential level had little effect on the spike threshold. We conclude that fundamental signal modifications occur during the spike initiation in the cockroach ocellar neuron, a finding that differs from the spike initiation process in other visual systems, including Limulus eye and vertebrate retina, in which it is presumed that little signal modification occurs at the analog-to-digital conversion process.     

Rectification and spike synchronization in the Limulus lateral eye

The encoding of light stimuli into spike trains in the Limulus lateral eye is shown to be markedly nonlinear in our conditions of stimulation. Our experimental results support the conclusion that nonlinearities are enhanced by lateral inhibition but arise within the single ommatidium, and are due to the high gain in the transduction from generator potential to spike rate. This high gain is in turn related to the existence, in the steady relation between generator potential and spike rate, of a positive threshold on the generator potential.     

Dynamics of Excitation and Inhibition in the Light-Adapted Limulus Eye in situ

The dynamics of spike discharge in eccentric cell axons from the in situ lateral eye of Limulus, under small sinusoidal modulation of light to which the eye is adapted, are described over two decades of light intensity and nearly three decades of frequency. Steady-state lateral inhibition coefficients, derived from the very low-frequency response, average 0.04 at three interommatidial spacings. The gain vs. frequency of a singly illuminated ommatidium is described closely from 0.004 to 0.4 cps by the linear transfer function s^0.25; this function also accounts approximately for the measured phase leads, the small signal adaptation following small step inputs, and for Pinter's (1966) earlier low-frequency generator potential data. We suggest that such dynamics could arise from a summation in the generator potential of distributed intensity-dependent relaxation processes along the dendrite and rhabdome. Analysis of the dynamic responses of an eccentric cell with and without simultaneously modulated illumination of particular neighbors indicates an effect equivalent to self-inhibition acting via a first-order low-pass filter with time constant 0.42 sec, and steady-state gain near 4.0. The corresponding filters for lateral inhibition required time constants from 0.35 to 1 sec and effective finite delay of 50–90 msec.     

Non-linear Membrane Properties in Entorhinal Cortical Stellate Cells Reduce Modulation of Input-Output Responses by Voltage Fluctuations

The presence of voltage fluctuations arising from synaptic activity is a critical component in models of gain control, neuronal output gating, and spike rate coding. The degree to which individual neuronal input-output functions are modulated by voltage fluctuations, however, is not well established across different cortical areas. Additionally, the extent and mechanisms of input-output modulation through fluctuations have been explored largely in simplified models of spike generation, and with limited consideration for the role of non-linear and voltage-dependent membrane properties. To address these issues, we studied fluctuation-based modulation of input-output responses in medial entorhinal cortical (MEC) stellate cells of rats, which express strong sub-threshold non-linear membrane properties. Using in vitro recordings, dynamic clamp and modeling, we show that the modulation of input-output responses by random voltage fluctuations in stellate cells is significantly limited. In stellate cells, a voltage-dependent increase in membrane resistance at sub-threshold voltages mediated by Na⁺ conductance activation limits the ability of fluctuations to elicit spikes. Similarly, in exponential leaky integrate-and-fire models using a shallow voltage-dependence for the exponential term that matches stellate cell membrane properties, a low degree of fluctuation-based modulation of input-output responses can be attained. These results demonstrate that fluctuation-based modulation of input-output responses is not a universal feature of neurons and can be significantly limited by subthreshold voltage-gated conductances.     

Light-induced responses of slow oscillatory neurons of the rat olivary pretectal nucleus

Background

The olivary pretectal nucleus (OPN) is a small midbrain structure responsible for pupil constriction in response to eye illumination. Previous electrophysiological studies have shown that OPN neurons code light intensity levels and therefore are called luminance detectors. Recently, we described an additional population of OPN neurons, characterized by a slow rhythmic pattern of action potentials in light-on conditions. Rhythmic patterns generated by these cells last for a period of approximately 2 minutes.

Methodology

To answer whether oscillatory OPN cells are light responsive and whether oscillatory activity depends on retinal afferents, we performed in vivo electrophysiology experiments on urethane anaesthetized Wistar rats. Extracellular recordings were combined with changes in light conditions (light-dark-light transitions), brief light stimulations of the contralateral eye (diverse illuminances) or intraocular injections of tetrodotoxin (TTX).

Conclusions

We found that oscillatory neurons were able to fire rhythmically in darkness and were responsive to eye illumination in a manner resembling that of luminance detectors. Their firing rate increased together with the strength of the light stimulation. In addition, during the train of light pulses, we observed two profiles of responses: oscillation-preserving and oscillation-disrupting, which occurred during low- and high-illuminance stimuli presentation respectively. Moreover, we have shown that contralateral retina inactivation eliminated oscillation and significantly reduced the firing rate of oscillatory cells. These results suggest that contralateral retinal innervation is crucial for the generation of an oscillatory pattern in addition to its role in driving responses to visual stimuli.     

Slow and Spike Potentials Recorded from Retinula Cells of the Honeybee Drone in Response to Light

Responses to light recorded by means of intracellular microelectrodes in isolated heads kept in oxygenated Ringer solution consist of a slow depolarization. Light adaptation increases the rates of depolarization and repolarization and decreases the amplitude of the response. Qualitatively these changes are similar to those observed in Limulus by Fuortes and Hodgkin. They are rapidly reversible during dark adaptation. In retinula cells of the drone eye a large single spike is recorded superimposed on the rising phase of the slow potential. The spike is a regenerative phenomenon; it can be triggered with electric current and is markedly reduced, sometimes abolished by tetrodotoxin. In rare cases cells were found which responded to light with a train of spikes. This behavior was only found under "unusual" experimental conditions; i.e., towards the end of a long experiment, during impalement, or at the beginning of responses to steps of strongly light-adapted preparations.     

Responses to object approach by a wide field visual neurone, the LGMD2 of the locust: Characterization and image cues

The LGMD2 belongs to a group of giant movement-detecting neurones which have fan-shaped arbors in the lobula of the locust optic lobe and respond to movements of objects. One of these neurones, the LGMD1, has been shown to respond directionally to movements of objects in depth, generating vigorous, maintained spike discharges during object approach. Here we compare the responses of the LGMD2 neurone with those of the LGMD1 to simulated movements of objects in depth and examine different image cues which could allow the LGMD2 to distinguish approaching from receding objects. In the absence of stimulation, the LGMD2 has a resting discharge of 10–40 spikes s⁻¹ compared with <1 spike s⁻¹ for the LGMD1. The most powerful excitatory stimulus for the LGMD2 is a dark object approaching the eye. Responses to approaching objects are suppressed by wide field movements of the background. Unlike the LGMD1, the LGMD2 is not excited by the approach of light objects; it specifically responds to movement of edges in the light to dark direction. Both neurones rely on the same monocular image cues to distinguish approaching from receding objects: an increase in the velocity with which edges of images travel over the eye; and an increase in the extent of edges in the image during approach. Accepted: 23 October 1996     

Electroretinogram components of the ocellus of the adult cabbage looper moth Trichoplusia ni

The electroretinogram (ERG) of the adult cabbage looper (Trichoplusia ni) ocellus has been studied by extracellular recording methods. Using white light stimulation, the ERG was found to have four components, two of which differ from those of ocelli previously studied. Here component 3 is an excitatory post-synaptic potential (EPSP) and component 4 is an excitatory spike discharge from the ocellar second-order neurons. The excitatory nature of these components has been verified by two experiments. In a light adaptation experiment decreased stimulus intervals caused a reduction in the number of excitatory spikes. In an experiment with the anticholinesterase tetraethylpyrophosphate (TEPP), treatment of the preparation abolished the excitatory spike discharge and reduced the magnitude of the EPSP.     

Performance of blue- and green-sensitive photoreceptors of the cricket Gryllus bimaculatus

The compound eye of the cricket Gryllus bimaculatus contains a specialized dorsal rim area (DRA) populated by distinct blue-sensitive photoreceptors responsible for perception of polarized light. The rest of the eye is dominated by green-sensitive photoreceptors. Using patch clamp we studied dissociated ommatidia of nocturnal adults and diurnal eight-instar nymphs with the goals (1) of characterizing the biophysical properties of cricket photoreceptors in general and (2) describing the functionally dissimilar blue- and green-sensitive photoreceptors in terms of voltage-gated channel composition and signal coding. Despite different lifestyles, adult and nymph photoreceptors were indistinguishable. No significant circadian changes were observed in K⁺ currents. In contrast, prominent differences were seen between blue- and green-sensitive photoreceptors. The former were characterized by relatively low absolute sensitivity, high input resistance, slow quantum bumps with long latencies, small light-induced and K⁺ currents and low steady-state depolarization. Information rate, a measure of photoreceptor performance calculated from voltage responses to bandwidth-limited white noise-modulated light contrast, was 87 ± 8 bits s^?1 in green-sensitive photoreceptors vs. 59 ± 14 bits s^?1 in blue-sensitive photoreceptors, implying a limited role of DRA in the perception of visual contrasts. In addition, evidence of electrical coupling between photoreceptors is presented.     

Light-initiated responses of retinula and eccentric cells in the Limulus lateral eye

The relationship between retinula and eccentric cells in the lateral eye of Limulus polyphemus was studied using a double electrode technique which permitted simultaneous recording of light-initiated responses in two sense cells and the labeling of the cells for subsequent histological examination and identification. The following results were obtained: (a) light-initiated slow responses with and without superimposed spike potentials were recorded from retinula cells and from eccentric cells (only one eccentric cell yielded responses without superimposed spike potentials); (b) spike potentials recorded in different cells within the same ommatidium were always synchronous; (c) a complete absence of spike potentials was observed in two experiments in which no eccentric cells could be found in the ommatidia containing the labeled retinula cells; (d) the greatest differences in the characteristics of responses recorded simultaneously occurred in those recorded from retinula-eccentric combinations. The results indicate that there is only one source of spike potential activity within an ommatidium (presumably the eccentric cell) and that the light-initiated response of retinula cells may be independent of the eccentric cell response. The suggestion is advanced that the response of the retinula cell may "trigger" the eccentric cell response.     

Biophysical mechanism of spike threshold dependence on the rate of rise of the membrane potential by sodium channel inactivation or subthreshold axonal potassium current

Spike threshold filters incoming inputs and thus gates activity flow through neuronal networks. Threshold is variable, and in many types of neurons there is a relationship between the threshold voltage and the rate of rise of the membrane potential (dVm/dt) leading to the spike. In primary sensory cortex this relationship enhances the sensitivity of neurons to a particular stimulus feature. While Na⁺ channel inactivation may contribute to this relationship, recent evidence indicates that K⁺ currents located in the spike initiation zone are crucial. Here we used a simple Hodgkin-Huxley biophysical model to systematically investigate the role of K⁺ and Na⁺ current parameters (activation voltages and kinetics) in regulating spike threshold as a function of dVm/dt. Threshold was determined empirically and not estimated from the shape of the Vm prior to a spike. This allowed us to investigate intrinsic currents and values of gating variables at the precise voltage threshold. We found that Na⁺ inactivation is sufficient to produce the relationship provided it occurs at hyperpolarized voltages combined with slow kinetics. Alternatively, hyperpolarization of the K⁺ current activation voltage, even in the absence of Na⁺ inactivation, is also sufficient to produce the relationship. This hyperpolarized shift of K⁺ activation allows an outward current prior to spike initiation to antagonize the Na⁺ inward current such that it becomes self-sustaining at a more depolarized voltage. Our simulations demonstrate parameter constraints on Na⁺ inactivation and the biophysical mechanism by which an outward current regulates spike threshold as a function of dVm/dt.     

VolPy: Automated and scalable analysis pipelines for voltage imaging datasets

Voltage imaging enables monitoring neural activity at sub-millisecond and sub-cellular scale, unlocking the study of subthreshold activity, synchrony, and network dynamics with unprecedented spatio-temporal resolution. However, high data rates (>800MB/s) and low signal-to-noise ratios create bottlenecks for analyzing such datasets. Here we present VolPy, an automated and scalable pipeline to pre-process voltage imaging datasets. VolPy features motion correction, memory mapping, automated segmentation, denoising and spike extraction, all built on a highly parallelizable, modular, and extensible framework optimized for memory and speed. To aid automated segmentation, we introduce a corpus of 24 manually annotated datasets from different preparations, brain areas and voltage indicators. We benchmark VolPy against ground truth segmentation, simulations and electrophysiology recordings, and we compare its performance with existing algorithms in detecting spikes. Our results indicate that VolPy’s performance in spike extraction and scalability are state-of-the-art.     

Sexual Dimorphism in the Compound Eye of Rhagophthalmus ohbai (Coleoptera: Rhagophthalmidae): II. Physiology and Function of the Eye of the Male

The eyes of male and female Rhagophthalmus ohbai are of very different sizes and possess approximately 3000 and 35 facets, respectively. In the male eye one can distinguish a smaller dorsal region with 500 facets and a larger ventral one with ca. 1800. Ultrastructural differences between them have been described earlier in this journal (Lau and Meyer-Rochow, 2006). Electrophysiological recordings from the two eye areas have now revealed that the ventral region is maximally sensitive to light of 600 nm wavelength, while the dorsal eye region responds maximally to light of 540–560 nm wavelengths. In the dorsal eye region sensitivity to UV-radiation at around 360 nm wavelength, being twice as high as that of the ventral eye region, amounted to ca. one quarter of peak wavelength sensitivity. The regional differences in spectral sensitivity seem to be a reflection of the different tasks of the two eye regions: looking downward to see the yellow light emitted by a female, sensitivity towards longer wavelengths would be advantageous, but looking upward into the twilight sky, sensitivity to shorter wavelength would be a more appropriate adaptation.     

The voltage-dependent step of the chloride transporter of Valonia utricularis encounters a Nernst-Planck and not an Eyring type of potential energy barrier

Voltage-clamp experiments were performed on cells of the giant marine alga Valonia utricularis to study the voltage dependence of the previously postulated chloride transporter (Wang, J., G. Wehner, R. Benz, and U. Zimmermann. 1991. Biophys. J. 59:235-248). Only one exponential current relaxation (apart from the capacitive spike) could be resolved up to a clamp voltage of ~120 mV within the time resolution of our experimental instrumentation (100 μs). This means that the rate constants of the heterogeneous complexation, k_R (association) and k_D (dissociation), were too fast to be resolved. Therefore, the “Läuger” model for carrier-mediated ion transport with equilibrium heterogeneous surface reaction was used to fit the experimental results. The voltage dependence of the initial membrane conductance was used for the evaluation of the voltage dependence of the translocation rate constant of the complexed carriers, k_AS. The initial conductance was found to be independent on the clamp voltage, which means that the translocation rate constant k_AS is a linear function of the applied voltage and that the voltage dependence of the translocation of charged carriers through the plasmalemma could be explained by a square-type Nernst-Planck barrier. The movement of the complexed form of the carrier through the membrane may be explained by a diffusion process rather than by simple first-order kinetic jump across an Eyring-type potential well. The current relaxation after a voltage clamp was studied as a function of the external chloride concentration. The results allowed an estimation of the stability constant, K, of the heterogeneous complexation reaction and a calculation of the translocation rate constants of the free and the complexed carriers, k_s and k_AS, respectively.     

Social recognition and approach in the chick: lateralization and effect of visual experience

Chicks, Gallus gallus domesticus, tested monocularly on day 3 after hatching recognize familiar versus unfamiliar conspecifics and choose to approach one or other when they use the left eye, whereas they approach familiar and unfamiliar chicks at random when they use the right eye. In experiment 1 we investigated the effects of light exposure of embryos prior to hatching on this particular form of lateralization. Irrespective of whether they hatched from eggs incubated in the dark or from eggs exposed to light during the final days of incubation, chicks using the left eye had higher choice scores (meaning they chose to approach either a familiar or an unfamiliar chick) than chicks using the right eye or both eyes. Therefore, light experience prior to hatching did not influence the lateralization of individual recognition or choice behaviour, although it did affect latency to move out of, and time spent in, the centre of the runway. Experiment 2 showed that visual/social experience posthatching influences choice behaviour: chicks housed in a group in the light for 12 h on day 1 posthatching made a clear choice between familiar and unfamiliar chicks when tested on day 3, but chicks kept in a group in the dark on day 1 did not make a choice, instead alternating between the two stimuli. In experiment 3 we found that posthatching visual/social experience increased the choice scores of chicks using the right eye and thereby removed any lateralization of choice behaviour. The results suggest that visual experience of a social group is required before chicks using their right eye (and left hemisphere) will pay attention to the cues that distinguish one chick from another. Chicks using their left eye (and right hemisphere) recognize the difference between individuals without requiring visual experience with other chicks. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Increased noise level of purkinje cell activities minimizes impact of their modulation during sensorimotor control

While firing rate is well established as a relevant parameter for encoding information exchanged between neurons, the significance of other parameters is more conjectural. Here, we show that regularity of neuronal spike activities affects sensorimotor processing in tottering mutants, which suffer from a mutation in P/Q-type voltage-gated calcium channels. While the modulation amplitude of the simple spike firing rate of their floccular Purkinje cells during optokinetic stimulation is indistinguishable from that of wild-types, the regularity of their firing is markedly disrupted. The gain and phase values of tottering's compensatory eye movements are indistinguishable from those of flocculectomized wild-types or from totterings with the flocculus treated with P/Q-type calcium channel blockers. Moreover, normal eye movements can be evoked in tottering when the flocculus is electrically stimulated with regular spike trains mimicking the firing pattern of normal simple spikes. This study demonstrates the importance of regularity of firing in Purkinje cells for neuronal information processing.     

The pineal eye inXenopus laevis embryos and larvae: A photoreceptor with a direct excitatory effect on behaviour

Summary Behavioural experiments demonstrate that embryos and young larval stages ofXenopus laevis when exposed to a sudden drop in light intensity may show locomotor activity. Recordings from motoneurone axons demonstrate that the integrity of the pineal eye photoreceptors are essential for this response to occur. Thus the pineal has a direct excitatory effect on behaviour.The pineal eye arises embryologically as a single dorsal vesicular evagination of the diencephalon and anatomically it is very similar to that of other developing amphibians.Recording from the pineal eye using a suction electrode demonstrates that suddenly lowering the light intensity evokes a burst of impulses followed by a raised firing frequency. Conversely, increasing the light intensity leads to a lowered firing frequency. With prolonged exposure to white light at a range of intensities, the frequency of spike discharge is dependent upon the light intensity. The pineal eye can therefore act as a luminance detector.The pineal photoreceptors are most sensitive to light of a wavelength near 520 nm, this probably enables maximum sensitivity to the wavelengths of light that penetrate the freshwater environment.The possible role of the pineal eye in controlling locomotor activity is discussed.Abbreviations HRP horse raddish peroxidase - SEM scanning electron microscopy     

Relative spike timing in stochastic oscillator networks of the Hermissenda eye

The role of relative spike timing on sensory coding and stochastic dynamics of small pulse-coupled oscillator networks is investigated physiologically and mathematically, based on the small biological eye network of the marine invertebrate Hermissenda. Without network interactions, the five inhibitory photoreceptors of the eye network exhibit quasi-regular rhythmic spiking; in contrast, within the active network, they display more irregular spiking but collective network rhythmicity. We investigate the source of this emergent network behavior first analyzing the role of relative input to spike–timing relationships in individual cells. We use a stochastic phase oscillator equation to model photoreceptor spike sequences in response to sequences of inhibitory current pulses. Although spike sequences can be complex and irregular in response to inputs, we show that spike timing is better predicted if relative timing of spikes to inputs is accounted for in the model. Further, we establish that greater noise levels in the model serve to destroy network phase-locked states that induce non-monotonic stimulus rate-coding, as predicted in Butson and Clark (J Neurophysiol 99:146–154, 2008a; J Neurophysiol 99:155–165, 2008b). Hence, rate-coding can function better in noisy spiking cells relative to non-noisy cells. We then study how relative input to spike–timing dynamics of single oscillators contribute to network-level dynamics. Relative timing interactions in the network sharpen the stimulus window that can trigger a spike, affecting stimulus encoding. Also, we derive analytical inter-spike interval distributions of cells in the model network, revealing that irregular Poisson-like spike emission and collective network rhythmicity are emergent properties of network dynamics, consistent with experimental observations. Our theoretical results generate experimental predictions about the nature of spike patterns in the Hermissenda eye.     

Vision in the edible snail. The morphology and total electrical activity of the retina]

Recording of the integrative electrical activity of the retina of the snail and electron microscopic study of its eye have shown the following. The electrical activity of the photoreceptors is a source of the retinogram (ERG) of the snail. ERG reaction form is characterized by two phases of a response: the initial spike and the following slow fading. For each given value of the photometric brightness of a light signal there exists a low limit of its length, beginning from which the ERG reaction of the snail assumes the form described. The value of the ERG response is a logarithmic function of brightness of the light stimulus.