Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2010 Oct 29;330(6004):669-73.
doi: 10.1126/science.1192949.

Filtering of visual information in the tectum by an identified neural circuit

Filippo Del Bene  1 , Claire Wyart, Estuardo Robles, Amanda Tran, Loren Looger, Ethan K Scott, Ehud Y Isacoff, Herwig Baier
Affiliations

Filtering of visual information in the tectum by an identified neural circuit

Filippo Del Bene et al. Science. .

Abstract

The optic tectum of zebrafish is involved in behavioral responses that require the detection of small objects. The superficial layers of the tectal neuropil receive input from retinal axons, while its deeper layers convey the processed information to premotor areas. Imaging with a genetically encoded calcium indicator revealed that the deep layers, as well as the dendrites of single tectal neurons, are preferentially activated by small visual stimuli. This spatial filtering relies on GABAergic interneurons (using the neurotransmitter γ-aminobutyric acid) that are located in the superficial input layer and respond only to large visual stimuli. Photo-ablation of these cells with KillerRed, or silencing of their synaptic transmission, eliminates the size tuning of deeper layers and impairs the capture of prey.

PubMed Disclaimer

Figures

Fig. 1
Fig. 1
Ca2+ responses in the tectal neuropil reveal size selectivity of deep layers. (A) Fluorescent signal from retinal axon terminals in the tectum of an Atoh7:Gal4, UAS:GCaMP1.6 larva. Region of interest (ROI) is demarcated by the orange dashed line. Neuropil boundaries are indicated by white dashed lines. (B) Tectal responses in an Atoh7:Gal4, UAS:GCaMP1.6 larva to a full-screen flash (50° visual angle) or to black bars (2° wide, moving A→P or P→A with a speed of 0.25°/ms). (C) Average maximum responses in the Atoh7:Gal4, UAS:GCaMP1.6 larvae (n = 5). (D) Tuning of retinal axons in the Atoh7:Gal4, UAS:GCaMP1.6 larvae to bars of increasing width (n = 5). (E) Fluorescent signal from posterior PVPNs in Gal4s1038t, UAS:GCaMP1.6 larva. ROIs for superficial (orange) and deep (green) neuropil layers are indicated by dashed lines. Neuropil boundary is white dashed line. (F to H) Responses to three visual stimuli in a Gal4s1038t, UAS:GCaMP1.6 larva. (I) Ratios of maximum responses in deep and superficial neuropil layers to bars of increasing width in Gal4s1038t, UAS:GCaMP1.6 larvae (n = 7 for 2° and 50°; n = 3 for other stimuli). (J to L) Average maximum responses in Gal4s1038t, UAS:GCaMP1.6 larvae (n = 7). *P < 0.05, **P < 0.01 (t test). (M) Reconstruction of a single PVN expressing UAS:GCaMP3, Dlx5/6:Gal4. (N) Ca2+ response of the PVN shown in (M). (O) Average maximum ΔF/F response in this cell. (P) Average response of bar-selective PVNs (n = 7). Error bars indicate SEM. Gray bars in (B), (F), (G), (H), and (N) indicate time of visual stimulation.
Fig. 2
Fig. 2
The neuropil Ca2+ response to a large visual stimulus is shaped by tectum-intrinsic GABAergic inhibition. (A and B) Effect of bicuculline administration to the tectum in Atoh7:Gal4, UAS:GCaMP1.6 transgenics. Response to a full-screen flash in a single larva (A) and average (n = 3) maximal response (B) before (CTRL, blue) and after bicuculline treatment (magenta). (C and D) Effect of intraocular injection of bicuculline in Atoh7:Gal4, UAS:GCaMP1.6. Response to a full-screen flash in a single larva (C) and average (n = 4) maximal response (D) before (CTRL, blue) and after bicuculline treatment (magenta). (E and F) Representative responses in superficial (orange) and deep (green) neuropil layers in Gal4s1038t, UAS:GCaMP1.6 larva before (E) and after bicuculline administration to tectum (F). (G and H) Average maximal response to a full-screen flash (G) and ratios (H) of Gal4s1038t, UAS:GCaMP1.6 larvae (n = 4) in superficial (orange) and deep (green) tectal neuropil layers before (CTRL) and after bicuculline administration. ***P < 0.001 (t test). Error bars indicate SEM. Gray bars in (A), (C), (E), and (F) indicate time of visual stimulation.
Fig. 3
Fig. 3
GABAergic identity and size tuning of superficial interneurons. (A) Gad67 in situ hybridization in the tectum at 5 days post-fertilization (dpf). Black arrows indicate expression in SINs. (B) GABA (red) and GCAMP1.6 (green) immunoreactivity in the tectum of a 7 dpf Gal4s1156t, UAS:GCaMP1.6 larva. White arrows indicate colocalization (yellow) of GABA and GCaMP1.6. Nuclei counterstained in blue with DAPI. (C) Fluorescent signal in Gal4s1156t, UAS:GCaMP1.6 larva. ROI is demarcated by a green dashed line. The neuropil boundary is a white dashed line. (D and E) In vivo confocal image of single SIN expressing cytoplasmic DsRed (red) and synaptophysin-GFP (Syp-GFP, green). Top view (maximum projection of image stack) is in (D); side view (50° rotation of image stack) in (E). Dashed line indicates location of skin above the surface of the tectum. (F) Responses to visual stimuli in a Gal4s1156t, UAS:GCaMP1.6 larva. (G) Maximum average responses (n = 4). Scale bars, 50 μm in (A) and (C), 30 μm in (D) and (E). Error bars indicate SEM.
Fig. 4
Fig. 4
Prey capture and PVN Ca2+ responses after silencing or removal of SINs. (A) Prey capture is reduced in Gal4s1156t, UAS:TeTxLC-CFP larvae, but not in Gal4s1038t, UAS:TeTxLC-CFP, relative to control (n = 10 for each genotype). (B and C) TUNEL staining detects KillerRed-induced, localized apoptosis in 7-dpf Gal4s1013t, UAS:KillerRed, UAS:GCaMP1.6 larva after targeted illumination of the SO (B). Contralateral tectum served as control (C). Dotted rectangle indicates targeted area in (B) and control area in (C), where apoptosis was scored. Dashed outlines indicate neuropil boundary. (D) Illuminated region (left) shows elevated staining with annexin V relative to control (right). Dotted rectangles indicate regions where apoptosis was assessed. (E) Ratios of maximum responses to full-screen flash in Gal4s1013t, UAS:KillerRed, UAS:GCaMP1.6 larvae before and after photo-ablation of SINs. Ratio is about 1 in the illuminated tectum and half in control (CTRL). Scale bars, 50 μm. ***P < 0.001 (t test). Error bars indicate SEM.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Isa T. Curr Opin Neurobiol. 2002;12:668. - PubMed
    1. Scott EK, Baier H. Front Neural Circuits. 2009;3:13. - PMC - PubMed
    1. Vanegas H, Laufer M, Amat J. J Comp Neurol. 1974;154:43. - PubMed
    1. Meek J, Schellart NA. J Comp Neurol. 1978;182:89. - PubMed
    1. Nevin LM, Robles E, Baier H, Scott EK. BMC Biol. 2010;8:126. - PMC - PubMed

Publication types

MeSH terms

LinkOut - more resources