The AII amacrine cell connectome: a dense network hub

Marc, Robert E.; Anderson, James R.; Jones, Bryan W.; Sigulinsky, Crystal; Lauritzen, J. Scott

doi:10.3389/fncir.2014.00104

Cited by 82 publications

(146 citation statements)

References 59 publications

(110 reference statements)

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“…Our Ca 2+ imaging results in mature AII-ACs are in excellent agreement with previous imaging studies in adult AII-ACs (see Habermann et al, 2003 and Borghuis et al, 2011). Moreover, our developmental studies, together with those of Schubert et al (2008), strongly suggest that glycine release from mature AII-AC occurs mostly from conventional active zones in the lobular appendages, which contain ≈ 0.6 mM glycine (Marc et al, 2014). It thus seems likely that ΔC m reflects the fusion of glycine-containing synaptic vesicles.…”

Section: Discussionsupporting

confidence: 59%

“…Moreover, there is a tonic crossover inhibition to the OFF-alpha ganglion cell from the AII-AC and this implies that the AII-AC must be capable of tonic exocytosis and a continuous release of glycine (Murphy and Rieke, 2006; Münch et al, 2009; van Wyk et al, 2009). Accordingly, the lobular appendages of the AII-AC have a high density of synaptic vesicles that is similar to that of bipolar cell terminals (≈ 1500 vesicles/μm 3 ; Marc et al, 2014). …”

Section: Discussionmentioning

confidence: 93%

“…The AII-AC, in turn, splits the incoming signals into ON and OFF channels by making electrical, gap junction contacts at their arboreal dendrites with ON-type cone bipolar cell terminals and glycinergic synapses at their lobular appendages with OFF-type cone bipolar cell terminals and ganglion cells (Famiglietti & Kolb, 1975; Mills and Massey, 1991). The narrow-field AII-AC thus plays a pivotal role in the mammalian retina (MacNeil, et al, 1999; Marc et al, 2014). …”

Section: Introductionmentioning

confidence: 99%

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Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Balakrishnan

Puthussery

Kim

et al. 2015

Neuron

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Summary Ribbon synapses convey sustained and phasic excitatory drive within retinal microcircuits. However, the properties of retinal inhibitory synapses are less well known. AII-amacrine cells are interneurons in the retina that exhibit large glycinergic synapses at their dendritic lobular appendages. Using membrane capacitance measurements we observe robust exocytosis elicited by the opening of L-type Ca2+ channels located on the lobular appendages. Two pools of synaptic vesicles were detected: a small, rapidly releasable pool and a larger and more slowly releasable pool. Depending on the stimulus, either paired-pulse depression or facilitation could be elicited. During early postnatal maturation, the coupling of the exocytosis Ca2+-sensor to Ca2+ channel becomes tighter. Light-evoked depolarizations of the AII-amacrine cell elicited exocytosis that was graded to light intensity. Our results suggest that AII-amacrine cell synapses are capable of providing both phasic and sustained inhibitory input to their postsynaptic partners without the benefit of synaptic ribbons.

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Section: Discussionsupporting

confidence: 59%

Section: Discussionmentioning

confidence: 93%

Section: Introductionmentioning

confidence: 99%

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Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Balakrishnan

Puthussery

Kim

et al. 2015

Neuron

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“…The latter is an illusion, and the former is the result of joint distribution sampling. The same is true of the synapses of aii amacrine cells onto the dendrites of ganglion cells in the oFF layer [4,73]. again, sources far outnumber targets.…”

Section: New Structuresmentioning

confidence: 77%

High-Resolution Synaptic Connectomics

Marc

Jones

Sigulinsky

et al. 2015

Biological and Medical Physics, Biomedical Engineering

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high-speed, high-resolution connectomics enables unambiguous mapping of synapses, gap junctions, adherens junctions, and other forms of adjacency among neurons in complex neural systems such as brain and retina. This chapter reviews the motivations for generating complete network architectures; the technologies available for large-scale network acquisition, visualization, and analysis; the fusion of molecular markers with a high-resolution ultrastructure; new networks and organelles discovered by ultrastructural connectomics; and new technological advances needed to expand the applications of connectomics. Motivations for Ultrastructural Connectomicsa connectome is the complete set of cellular partners and connections for a neural region. it can be executed on the mesoscale (spatial resolution of magnetic resonance imaging or even conventional optical imaging) to map fiber networks or on the nanoscale (spatial resolution of electron imaging) to map synaptic networks. This review addresses our experience with high-resolution synaptic connectomics based on automated transmission electron microscope (aTeM) imaging.The notion of using computational methods to accelerate ultrastructural analysis is at least three decades old [92]. even so, computational imaging for electron microscopy did not become a mainstream strategy until recently. There were three reasons for this: slow acquisition speed, expensive storage, and weak analytical scale. Film-based imaging followed by high-performance digitization [40] or even digital camera acquisition followed by analysis was so slow that it had no competitive advantage. Second, data storage at the resolution required for synaptic identification and quantification was prohibitively expensive, especially for Nih-funded investigators. The third reason is less obvious: no formal rationale existed to motivate large-scale acquisitions.

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“…With a similar aim, Serrano-Velez et al (2014) apply fluorescent retrograde labeling together with freeze-fracture replica immunogold labeling (FRIL) to understand the synaptic organization of the mosquitofish spinal cord. Marc et al (2014) fully characterized the complete connectome of a retinal cell population using a combination of serial-EM and immunolabeling of small molecules. SoizaReilly and Commons (2014) discuss recent evidence about the complex architecture of the dorsal raphe's synaptic neuropil using the novel high-resolution imaging technique called array tomography.…”

mentioning

confidence: 99%

Neural Circuits Revealed

2015

Frontiers Research Topics

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The appropriate function of the nervous system relies on precise patterns of connectivity among hundreds to billions of neurons across different biological systems. Evolutionarily conserved patterns of neural circuit organization and connectivity between morphologically and functionally diverse sets of neurons emerge from a remarkably robust set of genetic blueprints, uniquely defining circuits responsible for planning and execution of behavioral repertoires (Arenkiel et al., 2004;Dasen, 2009;Pecho-Vrieseling et al., 2009;Sürmeli et al., 2011;White and Sillitoe, 2013;Inamata and Shirasaki, 2014). Although it is well-established that individual neurons represent the elemental building blocks of the brain, understanding the architecture of neural circuits and how neurons functionally "wire up" through synapses, remains one of biology's major challenges. Our current understanding of how interconnected neuronal populations produce perception, memory, and behavior remains nascent. To unravel the details of complex nervous system function, we must consider not only the morphological and physiological properties of individual neurons, but also the structure and function of connections formed between different cell types. In the last decade much effort has been focused on trying to fully characterize "the brain connectome" and to understand how patterns of synaptic connectivity between neurons might help to better inform the underlying defects associated with neurological and psychiatric disorders (Sporns et al., 2005;Lichtman and Sanes, 2008). More recently there is a growing interest in mapping, and eventually classifying, all synapses in the brain to construct a complete "synaptome" (DeFelipe, 2010;O'Rourke et al., 2012). The very nature of these studies, which rely on multidisciplinary research efforts, have thus catalyzed the development of new research tools and technologies. For instance, advances in molecular genetics, viral engineering, and imaging technologies now allow precise labeling, manipulation, and mapping of complex neural circuits, together revealing previously unattainable details about the cellular morphologies and subcellular structures that are unique to the different types of neurons that make up the brain. Such technological advances could not be possible without successful co-evolution of novel computational tools and analytical methods that allow acquisition, management, and interpretation of gigantic and complex datasets. In fact, this last point perhaps represents the main challenge for the future of "connectomics" .This Research Topic comprises a wide variety of articles contributing to current views and understanding of different neural circuits, how they are organized in neural networks, and what are the functional outputs of this organization. Additionally, pioneering researchers in the field review novel high-throughput tools and analytical approaches, further describing how these methods have evolved to better explore neural circuits at different levels, covering a wide spectrum of ana...

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The AII amacrine cell connectome: a dense network hub

Cited by 82 publications

References 59 publications

Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

Synaptic Vesicle Exocytosis at the Dendritic Lobules of an Inhibitory Interneuron in the Mammalian Retina

High-Resolution Synaptic Connectomics

Neural Circuits Revealed

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