Spinules: a case for retinal synaptic plasticity

doi:10.1016/0166-2236(93)90155-F

Trends in Neurosciences

Volume 16, Issue 6, June 1993, Pages 201-206

https://doi.org/10.1016/0166-2236(93)90155-F Get rights and content

Abstract

In both vertebrate and invertebrate nervous systems, a population of synapses is characterized by having finger-like indentations of the postsynaptic membrane that project into the presynaptic terminal. These ‘spinules’ are often transitory structures, and their presence has been associated with increased synaptic activity. We have studied the functional role of spinules in the fish retina, where they are observed in horizontal cells invaginating cone pedicles, and in synaptic terminals of bipolar cells. In the cone—horizontal cell synaptic complex, spinules are present during light adaptation; their formation is triggered by external light stimuli as well as by endogenous factors. Pharmacologically, spinules are degraded following an increase, and formed in response to a decrease of the transmitter glutamate released by the cone cells. Dopamine, released by interplexiform cells and acting via a D₁ receptor-mediated increase in cAMP, and a protein-kinase-C-based mechanism are also capable of inducing spinule formation. Functionally, the presence and absence, as well as the timecourse, of spinule formation during light adaptation is closely correlated with the development of biphasic chromatic responses in a class of cone horizontal cells and the manifestation of colour-opponency in ganglion cells. This suggests that in the outer retina of fish, spinules are mediating feedback activity essential for the coding of antagonistic colour information.

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Circadian clock organization in the retina: From clock components to rod and cone pathways and visual function
2023, Progress in Retinal and Eye Research
Citation Excerpt :
Spinules substantially increase the contact area between the cone membrane and cHC dendrites within the cone pedicle. Evidence suggests that spinules play a role in shaping the chromatic response properties of cHCs (Wagner and Djamgoz, 1993; De Juan and Garcia, 2001). It has also been proposed that spinules mediate feedback from cHCs to cones (Wagner and Djamgoz, 1993; De Juan and Garcia, 2001) but this idea has been questioned (Thoreson and Mangel, 2012).
Circadian (24-h) clocks are cell-autonomous biological oscillators that orchestrate many aspects of our physiology on a daily basis. Numerous circadian rhythms in mammalian and non-mammalian retinas have been observed and the presence of an endogenous circadian clock has been demonstrated. However, how the clock and associated rhythms assemble into pathways that support and control retina function remains largely unknown. Our goal here is to review the current status of our knowledge and evaluate recent advances. We describe many previously-observed retinal rhythms, including circadian rhythms of morphology, biochemistry, physiology, and gene expression. We evaluate evidence concerning the location and molecular machinery of the retinal circadian clock, as well as consider findings that suggest the presence of multiple clocks. Our primary focus though is to describe in depth circadian rhythms in the light responses of retinal neurons with an emphasis on clock control of rod and cone pathways. We examine evidence that specific biochemical mechanisms produce these daily light response changes. We also discuss evidence for the presence of multiple circadian retinal pathways involving rhythms in neurotransmitter activity, transmitter receptors, metabolism, and pH. We focus on distinct actions of two dopamine receptor systems in the outer retina, a dopamine D₄ receptor system that mediates circadian control of rod/cone gap junction coupling and a dopamine D₁ receptor system that mediates non-circadian, light/dark adaptive regulation of gap junction coupling between horizontal cells. Finally, we evaluate the role of circadian rhythmicity in retinal degeneration and suggest future directions for the field of retinal circadian biology.
Neuromodulatory role of melatonin in retinal information processing
2013, Progress in Retinal and Eye Research
The neurohormone melatonin is implicated in a variety of physiological processes. In the retina, a major source for melatonin production, melatonin is involved in modulation of neuronal activities. In this article we review recent advances in this research field, which is preceded by a concise account of general information about melatonin, melatonin receptors and intracellular signaling pathways for melatonin actions.
Melatonin is mainly synthesized in and released from photoreceptors in the retina. Different subtypes of melatonin receptors are present on major types of retinal neurons, and the expression of these receptors is highly species- and neuron subtype-dependent. By activating different melatonin receptor subtypes, melatonin modulates activities of retinal neurons. In the outer retina, melatonin regulates the activity of photoreceptors. In addition, melatonin reduces the light responsiveness of cone-driven horizontal cells, but potentiates rod signal to rod-dominant ON type bipolar cells in teleost fish or inhibits the TEA-sensitive potassium channel of rod-driven ON type bipolar cells in rats. In the inner retina, melatonin potentiates inputs from glycinergic amacrine cells to ganglion cells in rats. These actions of melatonin on retinal neurons are mediated by distinct intracellular signaling pathways via different subtypes of melatonin receptors and all serve to improve visual performance in a world of changing ambient illumination. The topics, concerning allosteric action of melatonin, interplay between melatonin and dopamine systems, and potential interaction between melatonin and melanopsin systems, are also discussed. An in-depth discussion of future directions in this research field is presented.
Lateral interactions in the outer retina
2012, Progress in Retinal and Eye Research
Citation Excerpt :
Following spinule retraction, color-opponent responses of ganglion cells (Raynauld et al., 1979) and horizontal cells (Weiler and Wagner, 1984) are abolished and responses of luminosity horizontal cells to high temporal frequency stimulation are diminished (Djamgoz et al., 1988). These effects are consistent with elimination of horizontal cell to cone feedback (Wagner and Djamgoz, 1993). The evidence that physical retraction of horizontal cell spinules from cone pedicles diminishes feedback effects is consistent with both unconventional (e.g., ephaptic interactions considered in Section 3.1.2) and conventional synaptic interactions between horizontal cells and cones.
Lateral interactions in the outer retina, particularly negative feedback from horizontal cells to cones and direct feed-forward input from horizontal cells to bipolar cells, play a number of important roles in early visual processing, such as generating center-surround receptive fields that enhance spatial discrimination. These circuits may also contribute to post-receptoral light adaptation and the generation of color opponency. In this review, we examine the contributions of horizontal cell feedback and feed-forward pathways to early visual processing. We begin by reviewing the properties of bipolar cell receptive fields, especially with respect to modulation of the bipolar receptive field surround by the ambient light level and to the contribution of horizontal cells to the surround. We then review evidence for and against three proposed mechanisms for negative feedback from horizontal cells to cones: 1) GABA release by horizontal cells, 2) ephaptic modulation of the cone pedicle membrane potential generated by currents flowing through hemigap junctions in horizontal cell dendrites, and 3) modulation of cone calcium currents (I_Ca) by changes in synaptic cleft proton levels. We also consider evidence for the presence of direct horizontal cell feed-forward input to bipolar cells and discuss a possible role for GABA at this synapse. We summarize proposed functions of horizontal cell feedback and feed-forward pathways. Finally, we examine the mechanisms and functions of two other forms of lateral interaction in the outer retina: negative feedback from horizontal cells to rods and positive feedback from horizontal cells to cones.
Ultrastructure of the distal retina of the adult zebrafish, Danio rerio
2012, Tissue and Cell
The organization, morphological characteristics, and synaptic structure of photoreceptors in the adult zebrafish retina were studied using light and electron microscopy. Adult photoreceptors show a typical ordered tier arrangement with rods easily distinguished from cones based on outer segment (OS) morphology. Both rods and cones contain mitochondria within the inner segments (IS), including the large, electron-dense megamitochondria previously described (Kim et al.) Four major ultrastructural differences were observed between zebrafish rods and cones: (1) the membranes of cone lamellar disks showed a wider variety of relationships to the plasma membrane than those of rods, (2) cone pedicles typically had multiple synaptic ribbons, while rod spherules had 1–2 ribbons, (3) synaptic ribbons in rod spherules were ∼2 times longer than ribbons in cone pedicles, and (4) rod spherules had a more electron-dense cytoplasm than cone pedicles. Examination of photoreceptor terminals identified four synaptic relationships at cone pedicles: (1) invaginating contacts postsynaptic to cone ribbons forming dyad, triad, and quadrad synapses, (2) presumed gap junctions connecting adjacent postsynaptic processes invaginating into cone terminals, (3) basal junctions away from synaptic ribbons, and (4) gap junctions between adjacent photoreceptor terminals. More vitread and slightly farther removed from photoreceptor terminals, extracellular microtubule-like structures were identified in association with presumed horizontal cell processes in the OPL. These findings, the first to document the ultrastructure of the distal retina in adult zebrafish, indicate that zebrafish photoreceptors have many characteristics similar to other species, further supporting the use of zebrafish as a model for the vertebrate visual system.
Zebrafish vision: Structure and function of the zebrafish visual system
2010, Fish Physiology
Citation Excerpt :
These are transient structures that retract in the dark-adapted retina (Wagner 1980). Their formation is triggered by decreased glutamate release from photoreceptors and increased dopamine release from interplexiform cells (Kohler et al. 1990; Wagner and Djamgoz 1993). This process is well documented in the zebrafish retina and can be observed as early as 5 days post fertilization, although the number and complexity of spinules increases with ensuing maturation of the retina (Biehlmaier et al. 2003).
This chapter discusses the structure and function of the zebrafish visual system. The development, structure, and function of the zebrafish visual system are shaped by its ecology. The visual system of the zebrafish can be loosely grouped into three parts—namely, the eye (including the retina), retinofugal projections connecting the retina to visual centers in the rest of the brain, and visual centers in the brain receiving and processing visual information. The anterior segment of the eye contains the cornea and the lens. They help in projecting a focused image onto the retina. The retina, as an outpocketing of the diencephalon, has long enjoyed the status of one of the most intensely studied parts of the central nervous system. Because of its position in the body it is an approachable part of the brain with clearly demarcated layers and a clear association among stimulus input, structure, and behavioral and physiological output. The main retinofugal projections terminate in the optic tecta of the dorsal midbrain, apart from a number of additional retinofugal areas. The zebrafish larva expresses a number of visually mediated behaviors that make it possible to screen for mutant strains deficient in these behaviors. The first emerging visually mediated behavioral response is the visual startle response, where the larvae respond with a rapid increase in body movements to sudden decrease in brightness.
Combinatorial morphogenesis of dendritic spines and filopodia by SPAR and α-actinin2
2009, Biochemical and Biophysical Research Communications
Rap small GTPases regulate excitatory synaptic strength and morphological plasticity of dendritic spines. Changes in spine structure are mediated by the F-actin cytoskeleton, but the link between Rap activity and actin dynamics is unclear. Here, we report a novel interaction between SPAR, a postsynaptic inhibitor of Rap, and α-actinin, a family of actin-cross-linking proteins. SPAR and α-actinin engage in bidirectional structural plasticity of dendritic spines: SPAR promotes spine head enlargement, whereas increased α-actinin2 expression favors dendritic spine elongation and thinning. Surprisingly, SPAR and α-actinin2 can function in an additive rather than antagonistic fashion at the same dendritic spine, generating combination spine/filopodia hybrids. These data identify a molecular pathway bridging the actin cytoskeleton and Rap at synapses, and suggest that formation of spines and filopodia are not necessarily opposing forms of structural plasticity.

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Trends in Neurosciences

PerspectivesSpinules: a case for retinal synaptic plasticity

Abstract

J. Comp. Neurol.

Tissue and Cell

J. Neurocytol.

Science

J. Neurocytol.

J. Comp. Neurol.

The Retina

Brain Res.

Vis. Neurosci.

Curr. Opin. Neurobiol.

J. Comp. Neurol.

Brain Res.

Mikroskopie

Eur. J. Cell. Biol.

Neurosci. Lett.

Am. J. Ophthalmol.

Science

Perspectives
Spinules: a case for retinal synaptic plasticity