Response latency of a motion-sensitive neuron in the fly visual system: dependence on stimulus parameters and physiological conditions

Warzecha A-K, Egelhaaf M. Response latency of a motion-sensitive neuron in the fly visual system: dependence on stimulus parameters and physiological conditions. Vision research. 2000;40(21):2973-2983

Temporal precision of the encoding of motion information by visual interneurons

Warzecha A-K, Kretzberg J, Egelhaaf M. Temporal precision of the encoding of motion information by visual interneurons. Current Biology. 1998;8(7):359-368.BACKGROUND: There is much controversy about the timescale on which neurons process and transmit information. On the one hand, a vast amount of information can be processed by the nervous system if the precise timing of individual spikes on a millisecond timescale is important. On the other hand, neuronal responses to identical stimuli often vary considerably and stochastic response fluctuations can exceed the mean response amplitude. Here, we examined the timescale on which neural responses could be locked to visual motion stimuli. RESULTS: Spikes of motion-sensitive neurons in the visual system of the blowfly are time-locked to visual motion with a precision in the range of several tens of milliseconds. Nevertheless, different motion-sensitive neurons with largely overlapping receptive fields generate a large proportion of spikes almost synchronously. This precision is brought about by stochastic rather than by motion-induced membrane-potential fluctuations elicited by the common peripheral input. The stochastic membrane-potential fluctuations contain more power at frequencies above 30-40 Hz than the motion-induced potential changes. A model of spike generation indicates that such fast membrane-potential changes are a major determinant of the precise timing of spikes. CONCLUSIONS: The timing of spikes in neurons of the motion pathway of the blowfly is controlled on a millisecond timescale by fast membrane-potential fluctuations. Despite this precision, spikes do not lock to motion stimuli on this timescale because visual motion does not induce sufficiently rapid changes in the membrane potential

Membrane potential fluctuations determine the precision of spike timing and synchronous activity: a model study

Kretzberg J, Egelhaaf M, Warzecha A-K. Membrane potential fluctuations determine the precision of spike timing and synchronous activity: a model study. Journal of computational neuroscience. 2001;10(1):79-97.It is much debated on what time scale information is encoded by neuronal spike activity. With a phenomenological model that transforms time-dependent membrane potential fluctuations into spike trains, we investigate constraints for the timing of spikes and for synchronous activity of neurons with common input. The model of spike generation has a variable threshold that depends on the time elapsed since the previous action potential and on the preceding membrane potential changes. To ensure that the model operates in a biologically meaningful range, the model was adjusted to fit the responses of a fly visual interneuron to motion stimuli. The dependence of spike timing on the membrane potential dynamics was analyzed. Fast membrane potential fluctuations are needed to trigger spikes with a high temporal precision. Slow fluctuations lead to spike activity with a rate about proportional to the membrane potential. Thus, for a given level of stochastic input, the frequency range of membrane potential fluctuations induced by a stimulus determines whether a neuron can use a rate code or a temporal code. The relationship between the steepness of membrane potential fluctuations and the timing of spikes has also implications for synchronous activity in neurons with common input. Fast membrane potential changes must be shared by the neurons to produce synchronous activity

Neural coding with graded membrane potential changes and spikes

Kretzberg J, Warzecha A-K, Egelhaaf M. Neural coding with graded membrane potential changes and spikes. Journal of computational neuroscience. 2001;11(2):153-164.The neural encoding of sensory stimuli is usually investigated for spike responses, although many neurons are known to convey information by graded membrane potential changes. We compare by model simulations how well different dynamical stimuli can be discriminated on the basis of spiking or graded responses. Although a continuously varying membrane potential contains more information than binary spike trains, we find situations where different stimuli can be better discriminated on the basis of spike responses than on the basis of graded responses. Spikes can be superior to graded membrane potential fluctuations if spikes sharpen the temporal structure of neuronal responses by amplifying fast transients of the membrane potential. Such fast membrane potential changes can be induced deterministically by the stimulus or can be due to membrane potential noise that is influenced in its statistical properties by the stimulus. The graded response mode is superior for discrimination between stimuli on a fine time scale

Impact of photon noise on the reliability of a motion-sensitive neuron in the fly's visual system

Grewe J, Kretzberg J, Warzecha A-K, Egelhaaf M. Impact of photon noise on the reliability of a motion-sensitive neuron in the fly's visual system. The journal of neuroscience. 2003;23(34):10776-10783.Variable behavioral responses to identical visual stimuli can, in part, be traced back to variable neuronal signals that provide unreliable information about the outside world. This unreliability in encoding of visual information is caused by several noise sources such as photon noise, synaptic noise, or the stochastic nature of ion channels. Neurons of the fly's visual motion pathway have been claimed to represent perfect encoders, with photon noise as the main noise source limiting their performance. Other studies on the fly's visual system suggest, however, that internal noise emerging within the nervous system also affects the reliability of motion vision. To resolve these contradictory interpretations, we performed an electrophysiological investigation, inspired by the "equivalent noise" paradigm applied in psychophysics, on the fly's motion-sensitive H1 neuron. Noise-like brightness fluctuations of different strength were superimposed on the motion stimuli. Because the noise level found to affect the temporal properties of the spike responses is much larger than the estimate of photon noise under the experimental conditions, our results indicate that motion vision is more likely to be limited by internal sources of variability than by photon noise

Outdoor performance of a motion-sensitive neuron in the blowfly

Egelhaaf M, Grewe J, Kern R, Warzecha A-K. Outdoor performance of a motion-sensitive neuron in the blowfly. Vision research. 2001;41(27):3627-3637.We studied an identified motion-sensitive neuron of the blowfly under outdoor conditions. The neuron was stimulated by oscillating the fly in a rural environment. We analysed whether the motion-induced neuronal activity is affected by brightness changes ranging between bright sunlight and dusk, In addition, the relationship between spike rate and ambient temperature was determined. The main results are: (1) The mean spike rate elicited by visual motion is largely independent of brightness changes over several orders of magnitude as they occur as a consequence of positional changes of the sun. Even during dusk the neuron responds strongly and directionally selective to motion. (2) The neuronal spike rate is not significantly affected by short-term brightness changes caused by clouds temporarily occluding the sun. (3) In contrast, the neuronal activity is much affected by changes in ambient temperature. (C) 2001 Elsevier Science Ltd. All rights reserved

Neural encoding of behaviourally relevant visual-motion information in the fly

Egelhaaf M, Kern R, Krapp HG, Kretzberg J, Kurtz R, Warzecha A-K. Neural encoding of behaviourally relevant visual-motion information in the fly. Trends in Neurosciences. 2002;25(2):96-102.Information processing in visual systems is constrained by the spatial and temporal characteristics of the sensory input and by the biophysical properties of the neuronal circuits. Hence, to understand how visual systems encode behaviourally relevant information, we need to know about both the computational capabilities of the nervous system and the natural conditions under which animals normally operate. By combining behavioural, neurophysiological and computational approaches, it is now possible in the fly to assess adaptations that process visual-motion information under the constraints of its natural input. It is concluded that neuronal operating ranges and coding strategies appear to be closely matched to the inputs the animal encounters under behaviourally relevant conditions

Relating Neuronal to Behavioral Performance: Variability of Optomotor Responses in the Blowfly

Behavioral responses of an animal vary even when they are elicited by the same stimulus. This variability is due to stochastic processes within the nervous system and to the changing internal states of the animal. To what extent does the variability of neuronal responses account for the overall variability at the behavioral level? To address this question we evaluate the neuronal variability at the output stage of the blowfly's (Calliphora vicina) visual system by recording from motion-sensitive interneurons mediating head optomotor responses. By means of a simple modelling approach representing the sensory-motor transformation, we predict head movements on the basis of the recorded responses of motion-sensitive neurons and compare the variability of the predicted head movements with that of the observed ones. Large gain changes of optomotor head movements have previously been shown to go along with changes in the animals' activity state. Our modelling approach substantiates that these gain changes are imposed downstream of the motion-sensitive neurons of the visual system. Moreover, since predicted head movements are clearly more reliable than those actually observed, we conclude that substantial variability is introduced downstream of the visual system

Information and Discriminability as Measures of Reliability of Sensory Coding

Response variability is a fundamental issue in neural coding because it limits all information processing. The reliability of neuronal coding is quantified by various approaches in different studies. In most cases it is largely unclear to what extent the conclusions depend on the applied reliability measure, making a comparison across studies almost impossible. We demonstrate that different reliability measures can lead to very different conclusions even if applied to the same set of data: in particular, we applied information theoretical measures (Shannon information capacity and Kullback-Leibler divergence) as well as a discrimination measure derived from signal-detection theory to the responses of blowfly photoreceptors which represent a well established model system for sensory information processing. We stimulated the photoreceptors with white noise modulated light intensity fluctuations of different contrasts. Surprisingly, the signal-detection approach leads to a safe discrimination of the photoreceptor response even when the response signal-to-noise ratio (SNR) is well below unity whereas Shannon information capacity and also Kullback-Leibler divergence indicate a very low performance. Applying different measures, can, therefore, lead to very different interpretations concerning the system's coding performance. As a consequence of the lower sensitivity compared to the signal-detection approach, the information theoretical measures overestimate internal noise sources and underestimate the importance of photon shot noise. We stress that none of the used measures and, most likely no other measure alone, allows for an unbiased estimation of a neuron's coding properties. Therefore the applied measure needs to be selected with respect to the scientific question and the analyzed neuron's functional context

Temperature-dependence of neuronal performance in the motion pathway of the blowfly *Calliphora erythrocephala*

Warzecha A-K, Horstmann W, Egelhaaf M. Temperature-dependence of neuronal performance in the motion pathway of the blowfly *Calliphora erythrocephala*. The journal of experimental biology. 1999;202(22):3161-3170.Raising the head temperature within a behaviourally relevant range has strong effects on the performance of an identified neuron, the H1 neuron, in the visual motion pathway of blowflies. The effect is seen as an increase in the mean amplitude of the responses to motion under both transient and steady-state conditions, a considerable decrease in the response latency and an improvement in the reliability of the responses to motion. These temperature-dependent effects are independent of whether the animal is exposed to transient temperature changes or is maintained continuously at the same temperature for its entire life. The changes in the neuronal response properties with temperature may be of immediate functional significance for the animal under its normal operating conditions. In particular, the decrease in latency and the improvement in the reliability with increasing temperature may be relevant for the fly when executing its extremely virtuosic flight manoeuvres