Adaptation of transient responses of a movement-sensitive neuron in the visual system of the blowfly Calliphora erythrocephala

We studied temporal response properties of the H1 neuron by extracellular recording. This neuron is a wide-field movement-sensitive element in the visual system of the blowfly (Calliphora erythrocephala). If the neuron is stimulated with a stepwise pattern displacement in its preferred direction, it responds with a burst of action potentials. By repeating the stimulus step one obtains the average of the step response: a 20ms latency time followed by a sharp increase in average firing rate and a slower decay to the resting activity. We report that the characteristic decay time of the step response depends on the stimulus history. If the stimulus moved prior to the step, the higher the pattern velocity, the faster was the decay of the step response to the resting level. In quantitative terms, for velocities in the range 0.4–100°/s, the decay time-constant varies from 300–10ms and is smaller for higher velocities. The time-constant is only weakly affected by other stimulus parameters such as modulation depth or spatial wavelength, and is set independently in different areas of the visual field where it is tuned to the local velocity. We discuss a possible advantage of this form of adaptation for the processing of visual signals: The performance of the nolinear operations that extract information from the visual input can be optimized by prefiltering signals in the individual visual columns with a time-constant that decreases with stimulus velocity. It will be shown that both the test step response and the response to continuous movement can be described reasonably well by a correlation model with input filters that adapt their time-constants.     

Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli

The pursuit system controlling chasing behaviour in male blowflies has to cope with extremely fast and dynamically changing visual input. An identified male-specific visual neuron called Male Lobula Giant 1 (MLG1) is presumably one major element of this pursuit system. Previous behavioural and modelling analyses have indicated that angular target size, retinal target position and target velocity are relevant input variables of the pursuit system. To investigate whether MLG1 specifically represents any of these visual parameters we obtained in vivo intracellular recordings while replaying optical stimuli that simulate the visual signals received by a male fly during chasing manoeuvres. On the basis of these naturalistic stimuli we find that MLG1 shows distinct direction sensitivity and is depolarised if the target motion contains an upward component. The responses of MLG1 are jointly determined by the retinal position, the speed and direction, and the duration of target motimotion. Coherence analysis reveals that although retinal target size and position are in some way inherent in the responses of MLG1, we find no confirmation of the hypothesis that MLG1 encodes any of these parameters exclusively.     

On spiking units in the first optic chiasm of the blowfly

We recorded from the spiking sustaining unit in the optic chiasm between lamina and medulla in the brain of the blowfly Calliphora vicina, and investigated both temporal and spatial properties of the light-adapted cell. The sustaining unit fails to follow the highest temporal frequencies followed by the photoreceptor, but its temporal resolution is substantially better than that of the on-off unit. The sustaining unit does not display the fast temporal adaptation as previously described in the on-off unit. As compared with the on-off unit, the sustaining unit has a high sensitivity to small contrasts. Although the sustaining unit continues spiking as long as the light is on, its response is also transient as it adapts rapidly after a change of intensity. The receptive field and the line spread function of the sustaining unit have a similar size and profile: a central lobe with a half-width of approximately 2° surrounded by a circular inhibitory zone located at about 3° off-axis.     

Circadian control of spontaneous flight activity in the blowfly, Lucilia cuprina

ABSTRACT. Under laboratory light: dark cycles, the flight activity of adult Lucilia cuprina (Wied.) was low during darkness and uniformity high during light. This pattern persisted as a rhythm both in constant darkness and in constant light of intensity up to 1lx, with a period of approximately 22 h in each. Light pulses of 15 min at l00lx applied to the free-running rhythm in constant darkness generated phase shifts of up to 60°, 12-h light pulses of the same intensity generated maximal (180°) phase shifts. The phase response curves had shapes similar to those of a number of other insect rhythms. When exposed to light periods (70 lx) of greater than 12 h followed by constant darkness, the rhythm reinitiated at the light-dark transition from a constant phase equivalent to that at the time of the light-dark transition in the LD 12:12 cycle.     

Circadian rhythms in the blowfly, Phormia terraenovae: the period in constant light

ABSTRACT. Locomotor activity of individual blowflies, Phormia (=Protophormia) terraenovae R.D. (Diptera, Calliphoridae), was recorded by means of running wheels made of Perspex (plexiglass). At various intervals after hatching, flies were placed in the wheel in continuous light (120 lx). The period of the free-running rhythm was often shorter than 24 h initially, but lengthened later and stabilized after 15–20 days at values around or above 25 h. The mean period was independent of age in both sexes. Within a range from 2 to 2000lx the period did not depend in a systematic way on intensity of illumination; no activity could be recorded below 1 lx.     

Resolution of complex neuronal arrangements in the blowfly visual system using triple fluorescence staining

Summary Consecutive application of the fluorescent dyes, Texas Red and Lucifer Yellow, followed by nuclear staining with Bisbenzimide, reveals spatial relationships between individual neurons and relationships between their cell bodies and the perikaryal rind. The method is particularly useful for light-microscopical studies of complex interrelationships between identified neurons. The method has specific advantages over intraneuropil staining with cobalt or with HRP. These advantages are: simplicity, speed, information content, and aesthetic considerations.     

Steering a virtual blowfly: simulation of visual pursuit

The behavioural repertoire of male flies includes visually guided chasing after moving targets. The visuomotor control system for these pursuits belongs to the fastest found in the animal kingdom. We simulated a virtual fly, to test whether or not experimentally established hypotheses on the underlying control system are sufficient to explain chasing behaviour. Two operating instructions for steering the chasing virtual fly were derived from behavioural experiments: (i) the retinal size of the target controls the fly's forward speed and, thus, indirectly its distance to the target; and (ii) a smooth pursuit system uses the retinal position of the target to regulate the fly's flight direction. Low-pass filters implement neuronal processing time. Treating the virtual fly as a point mass, its kinematics are modelled in consideration of the effects of translatory inertia and air friction. Despite its simplicity, the model shows behaviour similar to that of real flies. Depending on its starting position and orientation as well as on target size and speed, the virtual fly either catches the target or follows it indefinitely without capture. These two behavioural modes of the virtual fly emerge from the control system for flight steering without implementation of an explicit decision maker.     

Renewal of visual pigment in photoreceptors of the blowfly

Summary Spectrophotometric measurements of photoreceptors 1–6 in the blowfly demonstrate that rhodopsin undergoes a continuous renewal. This involves, in the dark, the slow degradation of rhodopsin whereas metarhodopsin is degraded at a much faster rate. The effect of light is to reduce the rate at which metarhodopsin is degraded, i.e. the rate is inversely related to the intensity of the light. Rhodopsin synthesis is dependent on the presence of 11-cis retinal which is formed via a photoreaction from all-trans retinal resulting from the breakdown of rhodopsin and/or metarhodopsin: the biosynthesis of rhodopsin is therefore a light dependent process. Light of the blue/violet spectral range was found to mediate the isomerization of all-trans retinal into the 11-cis form. It is proposed that this stereospecificity is the result of all-trans retinal being bound to a protein. On the basis of the results a visual pigment cycle is proposed.     

Circadian variation in swim performance.

Previous findings of time-of-day differences in athletic performance could be confounded by diurnal fluctuations in environmental and behavioral "masking" factors (e.g., sleep, ambient temperature, and energy intake). The purpose of this study was to examine whether there is a circadian rhythm in swim performance that is independent of these masking factors. Experienced swimmers (n = 25) were assessed for 50-55 consecutive hours in the laboratory. The swimmers followed a 3-h "ultra-short" sleep-wake cycle, involving 1 h of sleep in darkness and 2 h of wakefulness in dim light, that was repeated throughout the observation. The protocol distributes behavioral and environmental masking factors equally across the 24-h period. Each swimmer was scheduled to perform six maximal-effort 200-m swim trials that were distributed equally across eight times of day (n = 147 trials). Each trial was separated by 9 h. A cosine fit of intra-aural temperature data established the time of the lowest body temperature (Tmin). Swim performances were z-transformed and compared across the eight times of day and across twelve 2-h intervals relative to Tmin. Analysis of covariance, controlling for trial number, revealed a significant (P < 0.001) pattern in swim performance relative to environmental and circadian times of day. Performance peaked 5-7 h before Tmin (approximately 2300) and was worst from 1 h before to 1 h after Tmin (approximately 0500). Mean swim performance was 169.5 s; circadian variation from peak to worst performance was 5.8 s. These data suggest a circadian rhythm in athletic performance independent of environmental and behavioral masking effects.     

Circadian rhythms in the blowfly, Phormia terraenovae: control of phase within the range of entrainment

ABSTRACT Locomotor activity of individual blowflies, Phormia (= Protophormia) terraenovae R.D. (Diptera, Calliphoridae) was recorded by means of running wheels. A few days after emergence, adult flies were placed in the wheels and exposed to at least two of four light-dark cycles (LD) differing in cycle duration T (LD 11:11, 12:12, 13:13 and 14:14 h). The intensity of illumination was 400 lux in L and 2 lux in D. From the actograms, phase-angle differences were read off between onset of activity and light-on (ψ/_onset), and between end of activity and light-off (ψend)- Within the range of entrainment, ψ changed systematically from negative values in T =22 h to positive values in T =28 h: the mean change in ψ per hour change in T , expressed in degree of the full circadian cycles, was 20^o. Standard deviations of ψ around its mean were computed for ten-cycle intervals; in ψ_onset and in ψ_end standard deviation was minimal when 4ψ was close to zero, and increased steadily with increasing negative or positive ψ -values.     

Response characteristics of the BVP neuron model to periodic pulse inputs.

The characteristics of the BVP neuron model response to periodic pulse stimuli are investigated. Temporal patterns of the output of the model are analyzed as a function of the stimulus intensity and period. The BVP model exhibits the same chaotic behavior, and a Cantor function-like graph of the response frequency (mean firing rate) as in electrophysiological experiments. This shows that the BVP model describes the complicated response characteristics of the neuron at least qualitatively.     

Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowfly Calliphora

Summary Hyperpolarizing potentials were recorded from second order monopolar neurons of the ganglion opticum I of Calliphora by means of glass microcapillaries. The eye was stimulated with a spotlike light source. Potentials were recorded in relation to the intensity of the light stimulus. The recording site was identified by marking the cell with a dye and by localizing the tip of the electrode.This work was supported by the Deutsche Forschungsgemeinschaft.     

Location-dependent effects of inhibition on local spiking in pyramidal neuron dendrites

Cortical computations are critically dependent on interactions between pyramidal neurons (PNs) and a menagerie of inhibitory interneuron types. A key feature distinguishing interneuron types is the spatial distribution of their synaptic contacts onto PNs, but the location-dependent effects of inhibition are mostly unknown, especially under conditions involving active dendritic responses. We studied the effect of somatic vs. dendritic inhibition on local spike generation in basal dendrites of layer 5 PNs both in neocortical slices and in simple and detailed compartmental models, with equivalent results: somatic inhibition divisively suppressed the amplitude of dendritic spikes recorded at the soma while minimally affecting dendritic spike thresholds. In contrast, distal dendritic inhibition raised dendritic spike thresholds while minimally affecting their amplitudes. On-the-path dendritic inhibition modulated both the gain and threshold of dendritic spikes depending on its distance from the spike initiation zone. Our findings suggest that cortical circuits could assign different mixtures of gain vs. threshold inhibition to different neural pathways, and thus tailor their local computations, by managing their relative activation of soma- vs. dendrite-targeting interneurons.     

Improving the performance of the amblyopic visual system

Experience-dependent plasticity is closely linked with the development of sensory function; however, there is also growing evidence for plasticity in the adult visual system. This review re-examines the notion of a sensitive period for the treatment of amblyopia in the light of recent experimental and clinical evidence for neural plasticity. One recently proposed method for improving the effectiveness and efficiency of treatment that has received considerable attention is ‘perceptual learning’. Specifically, both children and adults with amblyopia can improve their perceptual performance through extensive practice on a challenging visual task. The results suggest that perceptual learning may be effective in improving a range of visual performance and, importantly, the improvements may transfer to visual acuity. Recent studies have sought to explore the limits and time course of perceptual learning as an adjunct to occlusion and to investigate the neural mechanisms underlying the visual improvement. These findings, along with the results of new clinical trials, suggest that it might be time to reconsider our notions about neural plasticity in amblyopia.     

Pigment-dispersing hormone-immunoreactive neurons and their relation to serotonergic neurons in the blowfly and cockroach visual system

Summary The pigment-dispersing hormone (PDH) family of neuropeptides comprises a series of closely related octadecapeptides, isolated from different species of crustaceans and insects, which can be demonstrated immunocytochemically in neurons in the central nervous system and optic lobes of some representatives of these groups (Rao and Riehm 1989). In this investigation we have extended these immunocytochemical studies to include the blowfly Phormia terraenovae and the cockroach Leucophaea maderae. In the former species tissue extracts were also tested in a bioassay: extracts of blowfly brains exhibited PDH-like biological activity, causing melanophore pigment dispersion in destalked (eyestalkless) specimens of the fiddler crab Uca pugilator. Using standard immunocytochemical techniques, we could demonstrate a small number of pigment-dispersing hormone-immunoreactive (PDH-IR) neurons innervating optic lobe neuropil in the blowfly and the cockroach. In the blowfly the cell bodies of these neurons are located at the anterior base of the medulla. At least eight PDH-IR cell bodies of two size classes can be distinguished: 4 larger and 4 smaller. Branching immunoreactive fibers invade three layers in the medulla neuropil, and one stratum distal and one proximal to the lamina synaptic layer. A few fibers can also be seen invading the basal lobula and the lobula plate. The fibers distal to the lamina appear to be derived from two of the large PDH-IR cell bodies which also send processes into the medulla. These neurons share many features in their laminamedulla morphology with the serotonin immunoreactive neurons LBO-5HT described earlier (see Nässel 1988). It could be demonstrated by immunocytochemical double labeling that the serotonin and PDH immunoreactivities are located in two separate sets of neurons. In the cockroach optic lobe PDH-IR processes were found to invade the lamina synaptic region and form a diffuse distribution in the medulla. The numerous cell bodies of the lamina-medulla cells in the cockroach are located basal to the lamina in two clusters. Additional PDH-IR cell bodies could be found at the anterior base of the medulla. The distribution and morphology of serotonin-immunoreactive neurons in the cockroach lamina was found to be very similar to the PDH-IR ones. It is hence tempting to speculate that in both species the PDH-and serotonin-immunoreactive neurons are functionally coupled with common follower neurons. These neurons may be candidates for regulating large numbers of units in the visual system. In the flies photoreceptor properties may be regulated by action of the two set of neurons at sites peripheral to the lamina synaptic layer, possibly by paracrine release of messengers.     

Determination of the fraction of active inputs required by a neuron to fire

What fraction of the inputs to a neuron in the primary visual cortex (V1) need to be active for that neuron to reach its firing threshold? The paper describes a numerical method for estimating the selectivity of visual neurons, in terms of the required fraction of active excitatory inputs, from standard data produced by intracellular electro-physiological recordings. The method also provides an estimate of the relative strength of the feedforward inhibition in a push-pull model of the inputs to V1 simple cells. The method is tested on two V1 cells described in Carandini and Ferster [Carandini, M., Ferster, D., 2000. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470-484]. The results indicate that the maximum strength of feedforward inhibition is around 30% of the maximum strength of feedforward excitation. The two V1 neurons investigated fire if more than around 40% of their excitatory LGN inputs are active.     

Stochastic constancy,variability and adaptation of spike generation: Performance of a giant neuron in the visual system of the fly

The stochastic structure of the spike activity generated by a movement processing wide-field element in the visual system of the fly has been studied over the whole performance area of the neuron. The structure of this discharge is described in terms of an Adaptive Integrate-to-Threshold model for a wide variety of spatio-temporal stimuli as well as steady-state stimuli. In order to reproduce the experimental results it is shown that the source of randomness in the model (e.g. the threshold) behaves like a random variable which is distributed according to a two-state Markov renewal process. In the case of stationary discharges generated by moving sinewave patterns the shape of the interspike interval distribution (which, in the Integrate-to-Threshold model, reflects the shape of the threshold distribution) changes continuously from a two-state distribution at low firing rates to a one-state distribution at high firing rates. In dynamic conditions of the discharge, generated by temporal dynamic stimuli, the experimental results show that the shape of the (demodulated) interval distribution of the discharge is determined by the highest instantaneous firing rate with an adaptation time constant of a few seconds. The physioligical origin of this intriguing behaviour remains — up till now — out of the picture.