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Clonal relationships impact neuronal tuning within a phylogenetically ancient vertebrate brain structure.

Muldal AM, Lillicrap TP, Richards BA, Akerman CJ - Curr. Biol. (2014)

Bottom Line: To address this question, we examined the influence of lineage on the response properties of neurons within the optic tectum, a visual brain area found in all vertebrates.If lineage relationships do not influence the functional properties of tectal neurons, one prediction is that the RF positions of sister neurons should be no more (or less) similar to one another than those of neighboring control neurons.Our data reveal that the RF centers of sister neurons are significantly more similar than would be expected by chance.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.

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Two-Photon Calcium Imaging of Sister Neurons and Nearby Nonsister Neurons in the Optic Tectum(A) Experimental setup for in vivo calcium imaging and visual stimulation.(B) Two-photon stack through a region of tectum containing a single clone (red) and loaded with OGB1-AM (cyan). The z axis represents depth relative to the pial surface.(C) Single plane containing two dextran-labeled sister neurons. The scale bar represents 50 μm.(D) Example traces showing visually evoked calcium responses recorded from the neurons labeled in (C). Thin lines denote single trials; thick lines denote the mean response across trials. The corresponding visual stimuli are shown above. Raw spatial RFs and Gaussian fits corresponding to these neurons are also shown (right).(E) Fitted spatial RF maps obtained simultaneously from the two labeled sister neurons (red) and 83 nearby nonsister tectal neurons (cyan) shown in (C), superimposed onto their respective soma positions. The scale bar represents 50 μm.(F) Population data showing that clonally labeled tectal neurons do not differ from nonlabeled neurons in terms of their response magnitude (mean ΔF/F, p = 0.35; maximum ΔF/F, p = 0.31; n = 11 labeled neurons and n = 531 nonlabeled neurons; Mann-Whitney U test), their spatial selectivity (R2 values for Gaussian RF fits, p = 0.34), or the eccentricities of their RFs, as measured by either the euclidean (p = 0.16) or Chebyshev (p = 0.24) distance from the center of the stimulus area to the center of the fitted RF. Plots indicate mean ± SD.
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fig3: Two-Photon Calcium Imaging of Sister Neurons and Nearby Nonsister Neurons in the Optic Tectum(A) Experimental setup for in vivo calcium imaging and visual stimulation.(B) Two-photon stack through a region of tectum containing a single clone (red) and loaded with OGB1-AM (cyan). The z axis represents depth relative to the pial surface.(C) Single plane containing two dextran-labeled sister neurons. The scale bar represents 50 μm.(D) Example traces showing visually evoked calcium responses recorded from the neurons labeled in (C). Thin lines denote single trials; thick lines denote the mean response across trials. The corresponding visual stimuli are shown above. Raw spatial RFs and Gaussian fits corresponding to these neurons are also shown (right).(E) Fitted spatial RF maps obtained simultaneously from the two labeled sister neurons (red) and 83 nearby nonsister tectal neurons (cyan) shown in (C), superimposed onto their respective soma positions. The scale bar represents 50 μm.(F) Population data showing that clonally labeled tectal neurons do not differ from nonlabeled neurons in terms of their response magnitude (mean ΔF/F, p = 0.35; maximum ΔF/F, p = 0.31; n = 11 labeled neurons and n = 531 nonlabeled neurons; Mann-Whitney U test), their spatial selectivity (R2 values for Gaussian RF fits, p = 0.34), or the eccentricities of their RFs, as measured by either the euclidean (p = 0.16) or Chebyshev (p = 0.24) distance from the center of the stimulus area to the center of the fitted RF. Plots indicate mean ± SD.

Mentions: We then used two-photon calcium imaging to assess the response properties of clonally related neurons. We mapped spatial receptive fields (RFs) by simultaneously recording visually evoked calcium responses in both dextran-labeled and nonlabeled tectal neurons in the same animals (Figures 3A–3C; Supplemental Experimental Procedures) [14–16]. For clones to be included in the analysis, labeled neurons were required to exhibit robust spatially localized RFs, as determined statistically by fitting each RF with a 2D Gaussian function (Figures 3D and 3E; Supplemental Experimental Procedures). Clones in which only one neuron satisfied these criteria had to be excluded because sister comparisons were not possible. Under these criteria, we obtained a subset of animals with significant spatially selective responses in multiple dextran-labeled sister neurons and in a large fraction of nonlabeled neighboring neurons (11 labeled neurons, 531 nonlabeled neurons, four animals). Importantly, there was no significant difference between labeled and nonlabeled neurons in terms of their response amplitudes, the quality (R2) of the RF fits, or the eccentricity of their RF centers (Figure 3F).


Clonal relationships impact neuronal tuning within a phylogenetically ancient vertebrate brain structure.

Muldal AM, Lillicrap TP, Richards BA, Akerman CJ - Curr. Biol. (2014)

Two-Photon Calcium Imaging of Sister Neurons and Nearby Nonsister Neurons in the Optic Tectum(A) Experimental setup for in vivo calcium imaging and visual stimulation.(B) Two-photon stack through a region of tectum containing a single clone (red) and loaded with OGB1-AM (cyan). The z axis represents depth relative to the pial surface.(C) Single plane containing two dextran-labeled sister neurons. The scale bar represents 50 μm.(D) Example traces showing visually evoked calcium responses recorded from the neurons labeled in (C). Thin lines denote single trials; thick lines denote the mean response across trials. The corresponding visual stimuli are shown above. Raw spatial RFs and Gaussian fits corresponding to these neurons are also shown (right).(E) Fitted spatial RF maps obtained simultaneously from the two labeled sister neurons (red) and 83 nearby nonsister tectal neurons (cyan) shown in (C), superimposed onto their respective soma positions. The scale bar represents 50 μm.(F) Population data showing that clonally labeled tectal neurons do not differ from nonlabeled neurons in terms of their response magnitude (mean ΔF/F, p = 0.35; maximum ΔF/F, p = 0.31; n = 11 labeled neurons and n = 531 nonlabeled neurons; Mann-Whitney U test), their spatial selectivity (R2 values for Gaussian RF fits, p = 0.34), or the eccentricities of their RFs, as measured by either the euclidean (p = 0.16) or Chebyshev (p = 0.24) distance from the center of the stimulus area to the center of the fitted RF. Plots indicate mean ± SD.
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fig3: Two-Photon Calcium Imaging of Sister Neurons and Nearby Nonsister Neurons in the Optic Tectum(A) Experimental setup for in vivo calcium imaging and visual stimulation.(B) Two-photon stack through a region of tectum containing a single clone (red) and loaded with OGB1-AM (cyan). The z axis represents depth relative to the pial surface.(C) Single plane containing two dextran-labeled sister neurons. The scale bar represents 50 μm.(D) Example traces showing visually evoked calcium responses recorded from the neurons labeled in (C). Thin lines denote single trials; thick lines denote the mean response across trials. The corresponding visual stimuli are shown above. Raw spatial RFs and Gaussian fits corresponding to these neurons are also shown (right).(E) Fitted spatial RF maps obtained simultaneously from the two labeled sister neurons (red) and 83 nearby nonsister tectal neurons (cyan) shown in (C), superimposed onto their respective soma positions. The scale bar represents 50 μm.(F) Population data showing that clonally labeled tectal neurons do not differ from nonlabeled neurons in terms of their response magnitude (mean ΔF/F, p = 0.35; maximum ΔF/F, p = 0.31; n = 11 labeled neurons and n = 531 nonlabeled neurons; Mann-Whitney U test), their spatial selectivity (R2 values for Gaussian RF fits, p = 0.34), or the eccentricities of their RFs, as measured by either the euclidean (p = 0.16) or Chebyshev (p = 0.24) distance from the center of the stimulus area to the center of the fitted RF. Plots indicate mean ± SD.
Mentions: We then used two-photon calcium imaging to assess the response properties of clonally related neurons. We mapped spatial receptive fields (RFs) by simultaneously recording visually evoked calcium responses in both dextran-labeled and nonlabeled tectal neurons in the same animals (Figures 3A–3C; Supplemental Experimental Procedures) [14–16]. For clones to be included in the analysis, labeled neurons were required to exhibit robust spatially localized RFs, as determined statistically by fitting each RF with a 2D Gaussian function (Figures 3D and 3E; Supplemental Experimental Procedures). Clones in which only one neuron satisfied these criteria had to be excluded because sister comparisons were not possible. Under these criteria, we obtained a subset of animals with significant spatially selective responses in multiple dextran-labeled sister neurons and in a large fraction of nonlabeled neighboring neurons (11 labeled neurons, 531 nonlabeled neurons, four animals). Importantly, there was no significant difference between labeled and nonlabeled neurons in terms of their response amplitudes, the quality (R2) of the RF fits, or the eccentricity of their RF centers (Figure 3F).

Bottom Line: To address this question, we examined the influence of lineage on the response properties of neurons within the optic tectum, a visual brain area found in all vertebrates.If lineage relationships do not influence the functional properties of tectal neurons, one prediction is that the RF positions of sister neurons should be no more (or less) similar to one another than those of neighboring control neurons.Our data reveal that the RF centers of sister neurons are significantly more similar than would be expected by chance.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.

Show MeSH
Related in: MedlinePlus