Information processing by graded-potential transmission through tonically active synapses

Juusola, Mikko; French, Andrew S.; Uusitalo, R. O.; Weckström, Matti

doi:10.1016/s0166-2236(96)10028-x

Cited by 138 publications

(119 citation statements)

References 51 publications

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“…There was a zone of binocular overlap in the frontal visual field extending for each eye by 18.75 • into the contralateral visual field. To mimic the phasic response properties of output cells of the fly's first visual neuropile (Juusola et al 1996, Laughlin 1994, the photoreceptor output was temporally filtered with a firstorder high-pass filter (time constant 35 ms). The resulting signals were fed into correlationtype motion detectors, which have been shown to explain many aspects of the local motion detector (EMD) responses in the fly's visual system (for a review see Egelhaaf and Borst 1993b).…”

Section: Model Simulationsmentioning

confidence: 99%

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Kern¹,

Lutterklas²,

Petereit³

et al. 2001

Network: Computation in Neural Systems

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The stimuli traditionally used for analysing visual information processing are much simpler than what an animal sees when moving in its natural environment. Therefore, we analysed in a previous study the performance of an identified neuron in the optomotor system of the fly by using as visual stimuli image sequences that were experienced by the animal while walking in a structured environment. These electrophysiological experiments revealed that the fly visual system computes from behaviourally generated optic flow a rather unambiguous representation of the animal's self-motion. In contrast to conclusions based on simple stimuli, the directions of turns are represented by an interneuron, the HSE cell, quite independent of the spatial layout of the environment and its textural properties when the cell is stimulated with behaviourally generated optic flow. This conclusion is substantiated here by further experimental evidence. Moreover, it is shown that the largely unambiguous responses of the HSE cell to behaviourally generated optic flow can be replicated to a large extent by a network model of the fly's visual motion pathway. These results stress the significance of naturalistic stimuli for analysing what is encoded by neuronal circuits under natural operating conditions.

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Section: Model Simulationsmentioning

confidence: 99%

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Kern¹,

Lutterklas²,

Petereit³

et al. 2001

Network: Computation in Neural Systems

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“…Many graded synapses release neurotransmitter tonically, such that hyperpolarization reduces neurotransmitter release and depolarization increases neurotransmitter release (8). One possible mechanism that has been put forward for graded release is that the resting membrane potential of the neuron might lie in the middle of the activation curve of the voltage-gated calcium channel, so that small changes in the membrane potential could lead to increases or decreases in calcium influx (28). This model suggests that the mini frequencies should decrease if the motor neuron is hyperpolarized.…”

mentioning

confidence: 99%

Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction

Liu

Hollopeter

Jørgensen

2009

Proc. Natl. Acad. Sci. U.S.A.

144

168

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Most neurotransmission is mediated by action potentials, whereas sensory neurons propagate electrical signals passively and release neurotransmitter in a graded manner. Here, we demonstrate that Caenorhabditis elegans neuromuscular junctions release neurotransmitter in a graded fashion. When motor neurons were depolarized by light-activation of channelrhodopsin-2, the evoked postsynaptic current scaled with the strength of the stimulation. When motor neurons were hyperpolarized by light-activation of halorhodopsin, tonic release of synaptic vesicles was decreased. These data suggest that both evoked and tonic neurotransmitter release is graded in response to membrane potential. Acetylcholine synapses are depressed by highfrequency stimulation, in part due to desensitization of the nicotinesensitve ACR-16 receptor. By contrast, GABA synapses facilitate before becoming depressed. Graded transmission and plasticity confer a broad dynamic range to these synapses. Graded release precisely transmits stimulation intensity, even hyperpolarizing inputs. Synaptic plasticity alters the balance of excitatory and inhibitory inputs into the muscle in a use-dependent manner.channelrhodopsin-2 ͉ graded release ͉ halorhodopsin ͉ synaptic depression ͉ synaptic facilitation I n most neurons, propagation of an electrical signal occurs via all-or-none action potentials. These regenerative depolarizations ensure that signal transmission is robust and reliable over long distances. Conversely, some neurons lack action potentials, and rely instead on passive propagation and graded release of neurotransmitter. Graded synaptic transmission depends on two attributes: passive propagation of membrane depolarization along the axon, and non-saturating calcium influx at the synaptic bouton. Thus, graded transmission is associated with a paucity or absence of the voltage-gated ion channels in the axon, and incomplete activation of voltage-gated calcium channels at the synapse. Graded release of neurotransmitter underlies synaptic transmission in spiking neurons as well: if action potentials are blocked by tetrodotoxin neurotransmitter, release varies linearly with membrane potential (1, 2). The action potential simply fixes the size of the depolarization of the bouton.The most well studied graded synapses are the ribbon synapses of the vertebrate retina, either those of the photoreceptor or the bipolar cells (3). These neurons exhibit tonic release of neurotransmitter at rest. Evoked responses scale with the presynaptic stimulus (4) and thereby increase the information content at synapses. Sustained depolarization of the presynaptic cell results in increased neurotransmitter release (presumably by increasing miniature postsynaptic currents), and hyperpolarization results in decreased neurotransmitter release. These synapses show marked depression when stimulated but are also capable of high levels of sustained transmission under continuous stimulation (5, 6).

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“…Error bars represent mean ± SEM. efficient form for transmitting information (Juusola et al, 1996). The short cytoplasmic processes and high input resistance in NG2 cells may permit these cells even more effective electrotonic spread of local potentials than neurons.…”

Section: Discussionmentioning

confidence: 99%

“…Nonspiking neurons are also found in primary sensory systems and in the CNS of invertebrates, where electrotonic spread of local potentials is used effectively for signal transmission (Juusola et al, 1996). The graded membrane depolarization causes graded and continuous transmitter release by increased [Ca 2+ ] i through activation of VGCCs (Juusola et al, 1996;Wilson, 2004), and has been found to be an (E) Averaged total migration distance of NG2 cells (summed migration distance from all the migrated NG2 cells in one side) starting from the edge of the DiI-stained area under various conditions. Data were analyzed from the same brain slices as shown in D. *, P < 0.05; **, P < 0.01 compared between the two groups indicated.…”

Section: Discussionmentioning

confidence: 99%

Ca²⁺signaling evoked by activation of Na⁺channels and Na⁺/Ca²⁺exchangers is required for GABA-induced NG2 cell migration

Tong¹,

Li²,

Zhou³

et al. 2009

J Gen Physiol

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Information processing by graded-potential transmission through tonically active synapses

Cited by 138 publications

References 51 publications

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction

Ca²⁺signaling evoked by activation of Na⁺channels and Na⁺/Ca²⁺exchangers is required for GABA-induced NG2 cell migration

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Information processing by graded-potential transmission through tonically active synapses

Cited by 138 publications

References 51 publications

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Neuronal processing of behaviourally generated optic flow: experiments and model simulations

Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction

Ca2+signaling evoked by activation of Na+channels and Na+/Ca2+exchangers is required for GABA-induced NG2 cell migration

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Ca²⁺signaling evoked by activation of Na⁺channels and Na⁺/Ca²⁺exchangers is required for GABA-induced NG2 cell migration