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Characterization of genetically targeted neuron types in the zebrafish optic tectum.

Robles E, Smith SJ, Baier H - Front Neural Circuits (2011)

Bottom Line: The second type, a GABAergic non-stratified periventricular interneuron, extends a bushy arbor containing both dendrites and axons into the SGC and the deepest sublayers of the SFGS.Interestingly, the same axons form en passant synapses within the deepest neuropil layer of the tectum, the stratum album centrale.These observations establish a framework for studying the morphological and functional differentiation of neural circuits in the zebrafish visual system.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, University of California San Francisco San Francisco, CA, USA.

ABSTRACT
The optically transparent larval zebrafish is ideally suited for in vivo analyses of neural circuitry controlling visually guided behaviors. However, there is a lack of information regarding specific cell types in the major retinorecipient brain region of the fish, the optic tectum. Here we report the characterization of three previously unidentified tectal cell types that are specifically labeled by dlx5/6 enhancer elements. In vivo laser-scanning microscopy in conjunction with ex vivo array tomography revealed that these neurons differ in their morphologies, synaptic connectivity, and neurotransmitter phenotypes. The first type is an excitatory bistratified periventricular interneuron that forms a dendritic arbor in the retinorecipient stratum fibrosum et griseum superficiale (SFGS) and an axonal arbor in the stratum griseum centrale (SGC). The second type, a GABAergic non-stratified periventricular interneuron, extends a bushy arbor containing both dendrites and axons into the SGC and the deepest sublayers of the SFGS. The third type is a GABAergic periventricular projection neuron that extends a dendritic arbor into the SGC and a long axon to the torus semicircularis, medulla oblongata, and anterior hindbrain. Interestingly, the same axons form en passant synapses within the deepest neuropil layer of the tectum, the stratum album centrale. This approach revealed several novel aspects of tectal circuitry, including: (1) a glutamatergic mode of transmission from the superficial, retinorecipient neuropil layers to the deeper, output layers, (2) the presence of interneurons with mixed dendrite/axon arbors likely involved in local processing, and (3) a heretofore unknown GABAergic tectofugal projection to midbrain and hindbrain. These observations establish a framework for studying the morphological and functional differentiation of neural circuits in the zebrafish visual system.

No MeSH data available.


Related in: MedlinePlus

Summary of cell types labeled by the dg4ii plasmid. (A) Schematic of tectal anatomy and the relative sizes of the neuropil and primary retinorecipient laminae in the 5-dpf larvae. Measurements: (1) the maximum length of the tectal neuropil in the plane of the synaptic layers. (2) The maximum thickness of the neuropil in the axis perpendicular to the synaptic layers. (3) The maximum thickness of the primary retinorecipient layers (SO + SFGS). Note that these are maximum measurements at the center of the neuropil and the neuropil thickness is reduced at the edges. (B) Schematic traces of the cell types labeled by the dg4ii expression system and relative position of tectal neurite arbors. Note that nsPVINs an PVPNs primarily arborize in laminae that are primarily non-retinorecipient, whereas bsPVIN dendrites specifically target the SFGS layer. Dendrites are color coded in blue, glutamatergic axons in green (including retinal afferents indicated by green shading), and GABAergic axons in red. (C) Summary of morphological features that distinguish the three cell types identified. Arbor depth indicates the most superficial extent of the arbor as measured from the dorsal surface of the SO. Arbor width is the maximum measured distance in the plane of the synaptic layers. Thickness is the maximum length measured in the axis perpendicular to the synaptic layers. Data expressed as mean ± SD.
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Figure 10: Summary of cell types labeled by the dg4ii plasmid. (A) Schematic of tectal anatomy and the relative sizes of the neuropil and primary retinorecipient laminae in the 5-dpf larvae. Measurements: (1) the maximum length of the tectal neuropil in the plane of the synaptic layers. (2) The maximum thickness of the neuropil in the axis perpendicular to the synaptic layers. (3) The maximum thickness of the primary retinorecipient layers (SO + SFGS). Note that these are maximum measurements at the center of the neuropil and the neuropil thickness is reduced at the edges. (B) Schematic traces of the cell types labeled by the dg4ii expression system and relative position of tectal neurite arbors. Note that nsPVINs an PVPNs primarily arborize in laminae that are primarily non-retinorecipient, whereas bsPVIN dendrites specifically target the SFGS layer. Dendrites are color coded in blue, glutamatergic axons in green (including retinal afferents indicated by green shading), and GABAergic axons in red. (C) Summary of morphological features that distinguish the three cell types identified. Arbor depth indicates the most superficial extent of the arbor as measured from the dorsal surface of the SO. Arbor width is the maximum measured distance in the plane of the synaptic layers. Thickness is the maximum length measured in the axis perpendicular to the synaptic layers. Data expressed as mean ± SD.

Mentions: In contrast to the bsPVIN cell type, the inhibitory nsPVIN neuron type we identified has a compact arbor that spans the deeper layers of the SFGS and the SGC, suggesting that this neuron could potentially be a synaptic target of bsPVIN neurons. It is possible that these local interneurons mediate intratectal processing that functions to filter the visual information transmitted onto projection neurons. Recent experiments have provided evidence for a similar feed-forward inhibition circuit operating at the superficial layers of the larval tectum (Del Bene et al., 2010). This study characterized superficial interneurons (SINs), a class of inhibitory interneurons located near the neuropil surface that extend a broad, stratified arbor that is restricted to the SFGS. These neurons are selectively responsive to large visual stimuli and function to restrict the vertical flow of activity to the deep neuropil layers, thereby functioning as a size selectivity filter that makes the tectal circuit selective for small visual stimuli. Due to the laminar position of bsPVIN dendrites it is possible that these neurons receive excitatory inputs from retinal axons and inhibitory synapses from SINs and function to transmit visually evoked activity to the deeper neuropil layers containing the majority of projection neuron dendrites (see Figure 10C; Scott and Baier, 2009). The inhibitory nsPVIN population identified in this study could function as a feed-forward inhibitory circuit at the deeper layers of the tectum. nsPVINs contain dendritic arbors that span the SGC and only the deepest SFGS sublayer. In the mouse visual system RGC subpopulations with specific response properties have been shown to target specific laminae of the superior colliculus (Kim et al., 2008; Huberman et al., 2009). Therefore it is likely that there are functional differences between the synaptic inputs that target superficial and deep sublayers of the SFGS. Unlike the SFGS, which primarily receives retinal inputs, the SGC layer is known to receive non-visual afferents from telencephalon and thalamus (Meek, 1983), raising the possibility that nsPVINs integrate inputs from non-visual areas and retinal inputs with specific response properties. The role of inhibitory networks in the deeper layers of the tectal neuropil could be to restrict the number of projection neurons activated by a visual stimulus, possibly through modulation by afferent input from brain regions that process non-visual sensory information.


Characterization of genetically targeted neuron types in the zebrafish optic tectum.

Robles E, Smith SJ, Baier H - Front Neural Circuits (2011)

Summary of cell types labeled by the dg4ii plasmid. (A) Schematic of tectal anatomy and the relative sizes of the neuropil and primary retinorecipient laminae in the 5-dpf larvae. Measurements: (1) the maximum length of the tectal neuropil in the plane of the synaptic layers. (2) The maximum thickness of the neuropil in the axis perpendicular to the synaptic layers. (3) The maximum thickness of the primary retinorecipient layers (SO + SFGS). Note that these are maximum measurements at the center of the neuropil and the neuropil thickness is reduced at the edges. (B) Schematic traces of the cell types labeled by the dg4ii expression system and relative position of tectal neurite arbors. Note that nsPVINs an PVPNs primarily arborize in laminae that are primarily non-retinorecipient, whereas bsPVIN dendrites specifically target the SFGS layer. Dendrites are color coded in blue, glutamatergic axons in green (including retinal afferents indicated by green shading), and GABAergic axons in red. (C) Summary of morphological features that distinguish the three cell types identified. Arbor depth indicates the most superficial extent of the arbor as measured from the dorsal surface of the SO. Arbor width is the maximum measured distance in the plane of the synaptic layers. Thickness is the maximum length measured in the axis perpendicular to the synaptic layers. Data expressed as mean ± SD.
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Related In: Results  -  Collection

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Figure 10: Summary of cell types labeled by the dg4ii plasmid. (A) Schematic of tectal anatomy and the relative sizes of the neuropil and primary retinorecipient laminae in the 5-dpf larvae. Measurements: (1) the maximum length of the tectal neuropil in the plane of the synaptic layers. (2) The maximum thickness of the neuropil in the axis perpendicular to the synaptic layers. (3) The maximum thickness of the primary retinorecipient layers (SO + SFGS). Note that these are maximum measurements at the center of the neuropil and the neuropil thickness is reduced at the edges. (B) Schematic traces of the cell types labeled by the dg4ii expression system and relative position of tectal neurite arbors. Note that nsPVINs an PVPNs primarily arborize in laminae that are primarily non-retinorecipient, whereas bsPVIN dendrites specifically target the SFGS layer. Dendrites are color coded in blue, glutamatergic axons in green (including retinal afferents indicated by green shading), and GABAergic axons in red. (C) Summary of morphological features that distinguish the three cell types identified. Arbor depth indicates the most superficial extent of the arbor as measured from the dorsal surface of the SO. Arbor width is the maximum measured distance in the plane of the synaptic layers. Thickness is the maximum length measured in the axis perpendicular to the synaptic layers. Data expressed as mean ± SD.
Mentions: In contrast to the bsPVIN cell type, the inhibitory nsPVIN neuron type we identified has a compact arbor that spans the deeper layers of the SFGS and the SGC, suggesting that this neuron could potentially be a synaptic target of bsPVIN neurons. It is possible that these local interneurons mediate intratectal processing that functions to filter the visual information transmitted onto projection neurons. Recent experiments have provided evidence for a similar feed-forward inhibition circuit operating at the superficial layers of the larval tectum (Del Bene et al., 2010). This study characterized superficial interneurons (SINs), a class of inhibitory interneurons located near the neuropil surface that extend a broad, stratified arbor that is restricted to the SFGS. These neurons are selectively responsive to large visual stimuli and function to restrict the vertical flow of activity to the deep neuropil layers, thereby functioning as a size selectivity filter that makes the tectal circuit selective for small visual stimuli. Due to the laminar position of bsPVIN dendrites it is possible that these neurons receive excitatory inputs from retinal axons and inhibitory synapses from SINs and function to transmit visually evoked activity to the deeper neuropil layers containing the majority of projection neuron dendrites (see Figure 10C; Scott and Baier, 2009). The inhibitory nsPVIN population identified in this study could function as a feed-forward inhibitory circuit at the deeper layers of the tectum. nsPVINs contain dendritic arbors that span the SGC and only the deepest SFGS sublayer. In the mouse visual system RGC subpopulations with specific response properties have been shown to target specific laminae of the superior colliculus (Kim et al., 2008; Huberman et al., 2009). Therefore it is likely that there are functional differences between the synaptic inputs that target superficial and deep sublayers of the SFGS. Unlike the SFGS, which primarily receives retinal inputs, the SGC layer is known to receive non-visual afferents from telencephalon and thalamus (Meek, 1983), raising the possibility that nsPVINs integrate inputs from non-visual areas and retinal inputs with specific response properties. The role of inhibitory networks in the deeper layers of the tectal neuropil could be to restrict the number of projection neurons activated by a visual stimulus, possibly through modulation by afferent input from brain regions that process non-visual sensory information.

Bottom Line: The second type, a GABAergic non-stratified periventricular interneuron, extends a bushy arbor containing both dendrites and axons into the SGC and the deepest sublayers of the SFGS.Interestingly, the same axons form en passant synapses within the deepest neuropil layer of the tectum, the stratum album centrale.These observations establish a framework for studying the morphological and functional differentiation of neural circuits in the zebrafish visual system.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, University of California San Francisco San Francisco, CA, USA.

ABSTRACT
The optically transparent larval zebrafish is ideally suited for in vivo analyses of neural circuitry controlling visually guided behaviors. However, there is a lack of information regarding specific cell types in the major retinorecipient brain region of the fish, the optic tectum. Here we report the characterization of three previously unidentified tectal cell types that are specifically labeled by dlx5/6 enhancer elements. In vivo laser-scanning microscopy in conjunction with ex vivo array tomography revealed that these neurons differ in their morphologies, synaptic connectivity, and neurotransmitter phenotypes. The first type is an excitatory bistratified periventricular interneuron that forms a dendritic arbor in the retinorecipient stratum fibrosum et griseum superficiale (SFGS) and an axonal arbor in the stratum griseum centrale (SGC). The second type, a GABAergic non-stratified periventricular interneuron, extends a bushy arbor containing both dendrites and axons into the SGC and the deepest sublayers of the SFGS. The third type is a GABAergic periventricular projection neuron that extends a dendritic arbor into the SGC and a long axon to the torus semicircularis, medulla oblongata, and anterior hindbrain. Interestingly, the same axons form en passant synapses within the deepest neuropil layer of the tectum, the stratum album centrale. This approach revealed several novel aspects of tectal circuitry, including: (1) a glutamatergic mode of transmission from the superficial, retinorecipient neuropil layers to the deeper, output layers, (2) the presence of interneurons with mixed dendrite/axon arbors likely involved in local processing, and (3) a heretofore unknown GABAergic tectofugal projection to midbrain and hindbrain. These observations establish a framework for studying the morphological and functional differentiation of neural circuits in the zebrafish visual system.

No MeSH data available.


Related in: MedlinePlus