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      Visual Stimuli Evoked Action Potentials Trigger Rapidly Propagating Dendritic Calcium Transients in the Frog Optic Tectum Layer 6 Neurons

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          Abstract

          The superior colliculus in mammals or the optic tectum in amphibians is a major visual information processing center responsible for generation of orientating responses such as saccades in monkeys or prey catching avoidance behavior in frogs. The conserved structure function of the superior colliculus the optic tectum across distant species such as frogs, birds monkeys permits to draw rather general conclusions after studying a single species. We chose the frog optic tectum because we are able to perform whole-cell voltage-clamp recordings fluorescence imaging of tectal neurons while they respond to a visual stimulus. In the optic tectum of amphibians most visual information is processed by pear-shaped neurons possessing long dendritic branches, which receive the majority of synapses originating from the retinal ganglion cells. Since the first step of the retinal input integration is performed on these dendrites, it is important to know whether this integration is enhanced by active dendritic properties. We demonstrate that rapid calcium transients coinciding with the visual stimulus evoked action potentials in the somatic recordings can be readily detected up to the fine branches of these dendrites. These transients were blocked by calcium channel blockers nifedipine CdCl 2 indicating that calcium entered dendrites via voltage-activated L-type calcium channels. The high speed of calcium transient propagation, >300 μm in <10 ms, is consistent with the notion that action potentials, actively propagating along dendrites, open voltage-gated L-type calcium channels causing rapid calcium concentration transients in the dendrites. We conclude that such activation by somatic action potentials of the dendritic voltage gated calcium channels in the close vicinity to the synapses formed by axons of the retinal ganglion cells may facilitate visual information processing in the principal neurons of the frog optic tectum.

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          The mammalian superior colliculus: laminar structure and connections.

          The superior colliculus is a laminated midbrain structure that acts as one of the centers organizing gaze movements. This review will concentrate on sensory and motor inputs to the superior colliculus, on its internal circuitry, and on its connections with other brainstem gaze centers, as well as its extensive outputs to those structures with which it is reciprocally connected. This will be done in the context of its laminar arrangement. Specifically, the superficial layers receive direct retinal input, and are primarily visual sensory in nature. They project upon the visual thalamus and pretectum to influence visual perception. These visual layers also project upon the deeper layers, which are both multimodal, and premotor in nature. Thus, the deep layers receive input from both somatosensory and auditory sources, as well as from the basal ganglia and cerebellum. Sensory, association, and motor areas of cerebral cortex provide another major source of collicular input, particularly in more encephalized species. For example, visual sensory cortex terminates superficially, while the eye fields target the deeper layers. The deeper layers are themselves the source of a major projection by way of the predorsal bundle which contributes collicular target information to the brainstem structures containing gaze-related burst neurons, and the spinal cord and medullary reticular formation regions that produce head turning.
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            Action potential initiation and backpropagation in neurons of the mammalian CNS.

            Most neurons in the mammalian CNS encode and transmit information via action potentials. Knowledge of where these electrical events are initiated and how they propagate within neurons is therefore fundamental to an understanding of neuronal function. While work from the 1950s suggested that action potentials are initiated in the axon, many subsequent investigations have suggested that action potentials can also be initiated in the dendrites. Recently, experiments using simultaneous patch-pipette recordings from different locations on the same neuron have been used to address this issue directly. These studies show that the site of action potential initiation is in the axon, even when synaptic activation is powerful enough to elicit dendritic electrogenesis. Furthermore, these and other studies also show that following initiation, action potentials actively backpropagate into the dendrites of many neuronal types, providing a retrograde signal of neuronal output to the dendritic tree.
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              Event or emergency? Two response systems in the mammalian superior colliculus.

              Recent studies of the effects of stimulating the superior colliculus (SC) in rodents suggest that this structure mediates at least two classes of response to novel sensory stimuli. One class contains the familiar orienting response, together with movements resembling tracking or pursuit, and appears appropriate for undefined sensory 'events'. The second class contains defensive movements such as avoidance or flight, together with cardiovascular changes, that would be appropriate for a sudden emergency such as the appearance of a predator, or of an object on collision course. The two response systems appear to depend on separate output projections, and are probably subject to different sensory and forebrain influences. These findings (1) suggest an explanation for the complex anatomical organization of the SC, with multiple output pathways differentially accessed by a very wide variety of inputs, (2) emphasize the similarities between the SC and the optic tectum in non-mammalian species, and (3) suggest that the SC may be useful as a model for studying both the sensory control of defensive responses, and how intelligent decisions can be taken about relatively simple sensory inputs.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                28 September 2015
                2015
                : 10
                : 9
                : e0139472
                Affiliations
                [001]Neurophysiology laboratory, Neuroscience Institute, Lithuanian University of Health Sciences, Kaunas, Lithuania
                Institut Curie, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GS GB. Performed the experiments: GS NS. Analyzed the data: GB. Contributed reagents/materials/analysis tools: GS. Wrote the paper: GB GS TT.

                Article
                PONE-D-15-29438
                10.1371/journal.pone.0139472
                4586134
                26414356
                1b15b693-d788-4d63-bee9-98c4ba77319d
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 5 July 2015
                : 13 September 2015
                Page count
                Figures: 4, Tables: 0, Pages: 13
                Funding
                This work was supported by the Lithuanian Research Council grant No. VP1-3.1-ŠMM-07-K-02-059 to TT that is a part of the Global Grant measure of the European Social Fund.
                Categories
                Research Article
                Custom metadata
                Data are available from Figshare. Corresponding links are: http://figshare.com/s/f6815c645ca611e5940506ec4bbcf141 and http://figshare.com/s/9257945a5ca711e5bcd806ec4bbcf141.

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