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Research ArticleResearch Article: Confirmation, Sensory and Motor Systems

Rapid Analysis of Visual Receptive Fields by Iterative Tomography

Calvin D. Eiber, Jin Y. Huang, Spencer C. Chen, Natalie Zeater, Alexander N. J. Pietersen, Dario A. Protti and Paul R. Martin
eNeuro 19 November 2021, 8 (6) ENEURO.0046-21.2021; https://doi.org/10.1523/ENEURO.0046-21.2021
Calvin D. Eiber
1Save Sight Institute, The University of Sydney, Sydney, New South Wales 2000, Australia
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
3Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2000, Australia
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Jin Y. Huang
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
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Spencer C. Chen
3Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2000, Australia
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Natalie Zeater
1Save Sight Institute, The University of Sydney, Sydney, New South Wales 2000, Australia
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
3Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2000, Australia
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Alexander N. J. Pietersen
1Save Sight Institute, The University of Sydney, Sydney, New South Wales 2000, Australia
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
3Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2000, Australia
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Dario A. Protti
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
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Paul R. Martin
1Save Sight Institute, The University of Sydney, Sydney, New South Wales 2000, Australia
2School of Medical Sciences, The University of Sydney, Sydney, New South Wales 2006 Australia
3Australian Research Council Centre of Excellence for Integrative Brain Function, The University of Sydney, Sydney, New South Wales 2000, Australia
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    Figure 1.

    Schematic example of tomographic analysis. A, Example stimulus locations (achromatic flashing bar, 5 Hz) presented to a M-on cell (10.3° eccentricity) in marmoset LGN. B, Peristimulus histograms (PSTHs) to 2 s of stimulation at 5 Hz. Horizontal bar shows stimulus onset and duration. C, Computed NNMF weights for each bar position, normalized to 100% per-weight maximum, corresponding to the PSTHs shown in B. D, Response component profiles from NNMF analysis, corresponding to center and surround mechanisms. In order to emphasize the non-negativity of the NNMF output, prestimulus baselines were not subtracted from the components displayed. E, Receptive field maps of the component weights shown in C. Negative values indicate inhibitory contributions to the spatial summation for that component.

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    Figure 2.

    Geniculate array recording. A, Reconstructed LGN and electrode track, showing the location of 16 channels relative to the layers of the LGN. Two K blue-on cells, two K-on/off cells, and one P-on cell were recorded from this site. B, Contour plot of simultaneously recorded RFs for these cells to cone-isolating stimuli, showing outlines at 90% and 50% of the peak response amplitude (filled/shaded areas). C, NNMF component profiles for three example cells; prestimulus baselines were not subtracted. Horizontal bar: stimulus onset and duration. D, Receptive field maps corresponding to the components shown in C. For the K-on/off cell a displaced hot-spot (attributable to weak excitatory input from the nondominant eye) is indicated with an open arrowhead. For the K blue-on cell, spatially coextensive inputs are evident for S-cone-isolating and ML-cone-isolating stimuli.

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    Figure 3.

    Analysis of geniculate receptive field structure. A, NNMF component profiles for three example cells recorded in marmoset LGN in response to achromatic flashed bars. Upper–lower, P-on cell, M-on cell, K-on/off cell (respective eccentricity 1.6°, 14.6°, and 29.2°). Each row shows one example cell. Sine waves show the response at the stimulus frequency (5 Hz for the P and M cell; 10 Hz for the K-on/off cell). For the P and M cell, the two components capture the responses of the center and the surround; for the K-on/off cell, the two components capture a rapidly-adapting and a nonadapting components of the response. B, Response spectra for the computed NNMF components (red and blue). Asterisk shows stimulation frequency. C, Scatterplot of (normalized) component weights versus distance from the receptive field center. Gaussian fits are shown as thick lines. Each point represents one stimulus (bar) presentation. D, Receptive field maps for the two components. A surround component can be localized for the M cell but not the P cell, and the spatial map for the K-on/off cell demonstrates spatially co-extensive on+off input.

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    Figure 4.

    Summary statistics for visual cells in the LGN. A, Observed receptive field center and surround strength. B, Ratio of surround gain to center gain versus eccentricity, measured with bars (large markers) and drifting grating stimuli (small markers). Box charts (right) show the range, median, and intraquartile range of gain ratio for the flashing-bar and drifting-grating stimuli, **p < 0.001. C, Correlation between receptive field center radii (Eq. 3) measured with drifting grating stimuli or flashing bars. D, Receptive field center and surround radius versus eccentricity, as measured using flashing bars and drifting gratings.

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    Figure 5.

    Example mouse RGC responses. A, Representative traces for stimuli intersecting the receptive field center. From top to bottom, an A2 ON cell, an A2 OFF cell, and a C6 cell. Horizontal bar shows stimulus onset and duration. Time courses of the first three NNMF components (i, ii, iii) are shown separately for the C6 cell. B, Dendritic morphology of these cells. Bottom panel shows spatial profiles for components (i, ii, iii) of the C6 cell. C, Receptive field maps for these cells. Receptive field strength is given in imp/s per 100 × 100 μm2; 1 pixel = 12 μm2. Lower two panels show maps for components i, iii of the C6 cell. D, Relationship between dendritic field diameter and measured receptive field diameter for our sample of mouse RGCs. Morphology of traced RGCs shown at 1:10 scale.

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    Figure 6.

    Example and summary statistics for correlation between physiology and anatomy. A, Receptive field map for an A-on RGC, in imp/s per 100 × 100 μm. B, Contour plot of receptive field showing outlines of 90% (red outline) and 50% (orange outline) of the peak response relative to the cell dendritic morphology. C, Correlation between receptive field strength and dendrite density, at 1 point per 12 μm2, showing fitted relationship between physiological and anatomic data. D, Summary r2 (coefficient of determination) values across the population of RGCs. Arrowhead indicates cell shown in A–C. Error bar shows standard deviation.

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Rapid Analysis of Visual Receptive Fields by Iterative Tomography
Calvin D. Eiber, Jin Y. Huang, Spencer C. Chen, Natalie Zeater, Alexander N. J. Pietersen, Dario A. Protti, Paul R. Martin
eNeuro 19 November 2021, 8 (6) ENEURO.0046-21.2021; DOI: 10.1523/ENEURO.0046-21.2021

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Rapid Analysis of Visual Receptive Fields by Iterative Tomography
Calvin D. Eiber, Jin Y. Huang, Spencer C. Chen, Natalie Zeater, Alexander N. J. Pietersen, Dario A. Protti, Paul R. Martin
eNeuro 19 November 2021, 8 (6) ENEURO.0046-21.2021; DOI: 10.1523/ENEURO.0046-21.2021
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Keywords

  • lateral geniculate nucleus
  • marmoset
  • receptive field
  • retina
  • sensory coding
  • vision

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