Calcium accumulation in visual interneurons of the fly: stimulus dependence and relationship to membrane potential (original) (raw)
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In vivo imaging of calcium accumulation in fly interneurons as elicited by visual motion stimulation
Proceedings of the National Academy of Sciences, 1992
The computation of motion plays a central role in visual orientation. The fly has been successfully used as a model system for analyzing the mechanisms underlying motion detection. Thereby, much attention has been paid to a neuronal circuit of individually identifiable neurons in the third visual ganglion that extracts different types of retinal motion patterns and converts these patterns into specific components of visual orientation behavior. The extended dendritic trees of these large cells are the sites of convergence of numerous spatially distributed local motion-sensitive elements. As is revealed by in vivo microfluorometric imaging, these cells accumulate calcium during activation by visual motion stimulation. The spatiotemporal pattern of calcium distribution shows the following characteristics: (i) calcium accumulation is first spatially restricted to those dendritic branches that are depolarized by the retinotopic input, (ii) during ongoing motion stimulation calcium may a...
Journal of Neurobiology, 2001
Neurons exploit both membrane biophysics and biochemical pathways of the cytoplasm for dendritic integration of synaptic input. Here we quantify the tuning discrepancy of electrical and chemical response properties in two kinds of neurons using in vivo visual stimulation. Dendritic calcium concentration changes and membrane potential of visual interneurons of the fly were measured in response to visual motion stimuli. Two classes of tangential cells of the lobula plate were compared, HS-cells and CH-cells. Both neuronal classes are known to receive retinotopic input with similar properties, yet they differ in morphology, physiology, and computational context. Velocity tuning and directional selectivity of the electrical and calcium responses were investigated. In both cell classes, motioninduced calcium accumulation did not follow the early transient of the membrane potential. Rather, the amplitude of the calcium signal seemed to be related to the late component of the depolarization, where it was close to a steady state. Electrical and calcium responses differed with respect to their velocity tuning in CH-cells, but not in HS-cells. Furthermore, velocity tuning of the calcium response, but not of the electrical response differed between neuronal classes. While null-direction motion caused hyperpolarization in both classes, this led to a calcium decrement in CH-cells, but had no effect on the calcium signal in HS-cells, not even when calcium levels had been raised by a preceding excitatory motion stimulus. Finally, the voltage-[Ca 2؉ ] i-relationship for motion-induced, transient potential changes was steeper and less rectifying in CH-cells than in HS-cells. These results represent an example of dendritic information processing in vivo, where two neuronal classes respond to identical stimuli with a similar electrical response, but differing calcium response. This highlights the capacity of neurons to segregate two response components.
Journal of Neurophysiology
Motion adaptation in directionally selective tangential cells (TC) of the fly visual system has previously been explained as a presynaptic mechanism. Based on the observation that adaptation is in part direction selective, which is not accounted for by the former models of motion adaptation, we investigated whether physiological changes located in the TC dendrite can contribute to motion adaptation. Visual motion in the neuron's preferred direction (PD) induced stronger adaptation than motion in the opposite direction and was followed by an afterhyperpolarization (AHP). The AHP subsides in the same time as adaptation recovers. By combining in vivo calcium fluorescence imaging with intracellular recording, we show that dendritic calcium accumulation following motion in the PD is correlated with the AHP. These results are consistent with a calcium-dependent physiological change in TCs underlying adaptation during continuous stimulation with PD motion, expressing itself as an AHP a...
Mechanisms of Dendritic Calcium Signaling in Fly Neurons
2000
Mechanisms of dendritic calcium signaling in fly neurons. J Neuro- physiol 85: 439 - 447, 2001. We examined the mechanisms underlying dendritic calcium accumulation in lobula plate tangential cells of the fly visual system using an in vitro preparation of the fly brain. Local visual stimulation evokes a localized calcium signal in the dendrites of these cells in vivo. Here
Dendritic integration of motion information in visual interneurons of the blowfly
Neuroscience Letters, 1992
Dendritic integration plays a key role in the way information is processed by nerve cells. The large motion-sensitive interneurons of the fly appear to be most appropriate for an investigation of this process. These cells are known to receive input from numerous local motion-sensitive elements and to control visually-guided optomotor responses (e.g., Trends Neurosci., 11 (1988) 351-358; Stavenga and Hardie, Facets of Vision, Springer, 1989). The retinotopic input organization of these cells allows for in vivo stimulation of selected parts of their dendritic tree with their natural excitatory and inhibitory synaptic input signals. By displaying motion in either the cells' preferred or null direction in different regions of the receptive field we found: (i) Responses to combinations of excitatory and inhibitory motion stimuli can be described as the sum of the two response components. (ii) Responses to combination of excitatory stimuli show saturation effects. The deviation from linear superposition depends on the distance and relative position of the activated synaptic sites on the dendrite and makes the responses almost insensitive to the number of activated input channels. (iii) The saturation level depends on different stimulus parameters, e.g. the velocity of the moving pattern. The cell still encodes velocity under conditions of spatial saturation. The results can be understood on the basis of passive dendritic integration of the signals of retinotopically organized local motion-detecting elements with opposite polarity.
Localized direction selective responses in the dendrites of visual interneurons of the fly
BMC Biology, 2010
Background: The various tasks of visual systems, including course control, collision avoidance and the detection of small objects, require at the neuronal level the dendritic integration and subsequent processing of many spatially distributed visual motion inputs. While much is known about the pooled output in these systems, as in the medial superior temporal cortex of monkeys or in the lobula plate of the insect visual system, the motion tuning of the elements that provide the input has yet received little attention. In order to visualize the motion tuning of these inputs we examined the dendritic activation patterns of neurons that are selective for the characteristic patterns of wide-field motion, the lobula-plate tangential cells (LPTCs) of the blowfly. These neurons are known to sample direction-selective motion information from large parts of the visual field and combine these signals into axonal and dendro-dendritic outputs. Results: Fluorescence imaging of intracellular calcium concentration allowed us to take a direct look at the local dendritic activity and the resulting local preferred directions in LPTC dendrites during activation by wide-field motion in different directions. These 'calcium response fields' resembled a retinotopic dendritic map of local preferred directions in the receptive field, the layout of which is a distinguishing feature of different LPTCs. Conclusions: Our study reveals how neurons acquire selectivity for distinct visual motion patterns by dendritic integration of the local inputs with different preferred directions. With their spatial layout of directional responses, the dendrites of the LPTCs we investigated thus served as matched filters for wide-field motion patterns.
2003
Synaptic transmission is usually studied in vitro with electrical stimulation replacing the natural input of the system. In contrast, we analyzed in vivo transfer of visual motion information from graded-potential presynaptic to spiking postsynaptic neurons in the fly. Motion in the null direction leads to hyperpolarization of the presynaptic neuron but does not much influence the postsynaptic cell, because its firing rate is already low during rest, giving only little scope for further reductions. In contrast, preferred-direction motion leads to presynaptic depolarizations and increases the postsynaptic spike rate. Signal transfer to the postsynaptic cell is linear and reliable for presynaptic graded membrane potential fluctuations of up to approximately 10 Hz. This frequency range covers the dynamic range of velocities that is encoded with a high gain by visual motion-sensitive neurons. Hence, information about preferred-direction motion is transmitted largely undistorted ensuring a consistent dependency of neuronal signals on stimulus parameters, such as motion velocity. Postsynaptic spikes are often elicited by rapid presynaptic spike-like depolarizations which superimpose the graded membrane potential. Although the timing of most of these spike-like depolarizations is set by noise and not by the motion stimulus, it is preserved at the synapse with millisecond precision.
Journal of Computational Neuroscience, 1999
In this last paper in a series (Borst and Haag, 1996; Haag et al., 1997) about the lobula plate tangential cells of the fly visual system (CH, HS, and VS cells), the visual response properties were examined using intracellular recordings and computer simulations. In response to visual motion stimuli, all cells responded mainly by a graded shift of their axonal membrane potential. While ipsilateral motion resulted in a graded membrane potential shift, contralateral motion led to distinct EPSPs. For HS cells, simultaneous extracellular recorded action potentials of a spiking interneuron, presumably the H2 cell, corresponded to the EPSPs in the HS cell in a one-to-one fashion. When HS cells were hyperpolarized during ipsilateral motion, they mainly produced action potentials, but when they were hyperpolarized during contralateral motion only a slight increase of EPSP amplitude, could be observed. Intracellular application of the sodium channel blocker QX 314 abolished action potentials of HS cells while having little effect on the graded membrane response to ipsilateral motion. HS and CH cells were also studied with respect to their spatial integration properties. For both cell types, their graded membrane response was found to increase less than linearly with the size of the ipsilateral motion pattern. However, while for HS cells various amounts of hyperpolarizing current injected during motion stimulation led to different saturation levels, this was not the case for CH cells. In response to a sinusoidal velocity modulation, CH cells followed pattern motion only up to 10 Hz modulation frequency, but HS cells still revealed significant membrane depolarizations up to about 40 Hz. In the computer simulations, the compartmental models of tangential cells, as derived in the previous papers, were linked to an array of local motion detectors. The model cells revealed the same basic response features as their natural counterparts. They showed a response saturation as a function of stimulus size. In CH-models, however, the saturation was less pronounced than in real CH-cells, indicating spatially nonuniform membrane resistances with higher values in the dendrite. As in the experiments, HS models responded to high-frequency velocity modulation with a higher amplitude than did CH models.
Biochemical and biophysical research communications, 2015
The spatial dynamics of action potentials, including their propagation and the location of spike initiation zone (SIZ), are crucial for the computation of a single neuron. Compared with mammalian central neurons, the spike dynamics of invertebrate neurons remain relatively unknown. Thus, we examined the spike dynamics based on single spike-induced Ca(2+) signals in the dendrites of cricket mechanosensory projection neurons, known as giant interneurons (GIs). The Ca(2+) transients induced by a synaptically evoked single spike were larger than those induced by an antidromic spike, whereas subthreshold synaptic potentials caused no elevation of Ca(2+). These results indicate that synaptic activity enhances the dendritic Ca(2+) influx through voltage-gated Ca(2+) channels. Stimulation of the presynaptic sensory afferents ipsilateral to the recording site evoked a dendritic spike with higher amplitude than contralateral stimulation, thereby suggesting that alteration of the spike wavefor...