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Articles, Systems/Circuits

A Convolutional Subunit Model for Neuronal Responses in Macaque V1

Brett Vintch, J. Anthony Movshon and Eero P. Simoncelli
Journal of Neuroscience 4 November 2015, 35 (44) 14829-14841; DOI: https://doi.org/10.1523/JNEUROSCI.2815-13.2015
Brett Vintch
1Center for Neural Science,
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J. Anthony Movshon
1Center for Neural Science,
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Eero P. Simoncelli
1Center for Neural Science,
2Courant Institute of Mathematical Sciences, and
3Howard Hughes Medical Institute, New York University, New York, New York 10003
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  • Figure 1.
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    Figure 1.

    Subunit model for a single channel. a, A signal flow diagram describes how stimulus information is converted to a firing rate. The stimulus is passed through a bank of spatially shifted, but otherwise identical, linear-nonlinear subunits. The activity of these subunits is combined with a weighted sum over space (and optionally time; not shown), and passed through an output nonlinearity to generate a firing rate. b, Responses of intermediate model stages are depicted for an example input (for simplicity, a single frame is shown, rather than a temporal sequence). Each stage, except for the last, maps a spatially distributed array of inputs to a spatially distributed array of responses, depicted as pixel intensities in an image. The pooling stage sums over these responses and applies the final output nonlinearity.

  • Figure 2.
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    Figure 2.

    The LN and energy models fit to space-time (XT) data for an example simple cell and an example complex cell. a, c, LN model. XT filter is depicted as a grayscale image, with intensity indicating filter weight. Oblique filter orientation indicates a preference for moving stimuli (Adelson and Bergen 1985). In this figure and others, the input is in unspecified units, adjusted to span the range of linear responses that arise, given the combination of the experimental stimuli and fitted model parameters. The noisy appearance of the complex cell linear filter is indicative of a poor fit. b, d, Energy model, with two quadrature pairs of filters (one excitatory and one inhibitory). Display contrast for filters is normalized within each model (e.g., the suppressive filters are slightly weaker than the excitatory filters, and thus are plotted with proportionately less contrast). The energy model is invariant to phase, allowing it to capture this property of complex cells, but preventing it from describing simple cells (rsimple = 0.08, rcomplex = 0.41).

  • Figure 3.
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    Figure 3.

    The Rust-STC and subunit models fit to XT data for the example simple and complex cells of Figure 2. a, c, Rust-STC model. Contrast of individual filters indicates their weighted contribution to the full model. The output nonlinearity is a joint function of the excitatory and suppressive drive (see Materials and Methods) and is depicted as a 2D image in which intensity is proportional to firing rate. Cross-validated model performance: rsimple = 0.56, rcomplex = 0.47. b, d, Subunit model with two channels (excitatory and suppressive). The subunit filters are constrained to have unit norm, but the intensities in the image depicting the linear pooling weights indicate their relative contribution to the response. Cross-validated model performance: rsimple = 0.55, rcomplex = 0.42.

  • Figure 4.
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    Figure 4.

    Comparison of models across all cells fit to space-time (XT) data. Model performance is measured as the correlation between the measured spike count and the model-predicted firing rate. Each point corresponds to a cell, with hollow symbols indicating performance on training data and solid symbols indicating performance on held out testing data (i.e., cross-validated). a, b, The subunit model outperforms both the LN and energy models. c, The subunit model outperforms the Rust-STC model on cross-validated data (solid points), but not on training data (hollow points), a clear indication that the Rust-STC model is overfitting. d, Relative performance of Rust-STC, energy, and LN models, plotted by projecting the 3D vector of r values for each cell onto the surface of the unit sphere. The relative performance of energy versus LN models gives an intrinsic indication of cell complexity. The Rust-STC model outperforms the energy model for most complex cells and has performance approximately comparable with the LN model for simple cells (the LN model is a special case of the Rust-STC model). e, Relative performance of subunit, energy, and LN models. The subunit model consistently outperforms the other models, independent of cell type.

  • Figure 5.
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    Figure 5.

    Dependence of model-estimated pooling extent and strength on cell complexity. The abscissa of each graph represents a complexity index (derived from the LN and energy models as (Eenergy − ELN)/(Eenergy + ELN); see Materials and Methods). A value of −1 indicates a purely simple cell; and a value of 1 indicates a purely complex cell. a, Relative spatial pooling size in the fitted subunit model increases with cell complexity. For each cell, we computed the ratio of SDs of 2D Gaussian envelopes fitted to the pooling weights and the subunit filter. As expected, complex cells pool over a larger relative region than simple cells. This same effect is seen for the suppressive channel (gray x's). b, Relative temporal pooling size is not correlated with cell complexity, but pooling duration of the inhibitory channel is generally larger than that of the excitatory channel. c, Relative strength of excitatory to inhibitory channels increases with cell complexity. Relative strength is computed as the ratio of SDs of the two channel responses (i.e., generator signals) over all stimuli.

  • Figure 6.
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    Figure 6.

    The LN and energy models fitted to space-space-time (XYT) data from an example complex cell. a, The LN model shows selectivity for spatial patterns over time. The 3D filter kernel is depicted on the right as a stack of spatial filters, each associated with one (25 ms) temporal frame. Three relevant time slices (50, 75, and 100 ms) are replotted on the left for clarity. b, The energy model, with two quadrature pairs of filters (one excitatory, one inhibitory).

  • Figure 7.
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    Figure 7.

    The Rust-STC and subunit models fitted to XYT data from the example complex cell of Figure 6. Conventions follow Figure 6. a, Rust-STC model. The high dimensionality of the XYT filters means that the parameters of this model are difficult to estimate and the resulting filters are very noisy. b, Subunit model. The convolutional nature of the subunit model allows it to cleanly capture the structure of the complex cell receptive field. There is a clear selectivity for upward motion over time and suppression by opposite-direction motion at a lower spatial frequency.

  • Figure 8.
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    Figure 8.

    Comparison of model performances across a subset of XYT cells (n = 21), for which we obtained responses to a 1000-frame stimulus repeated 20 times. a, Model performance is computed as the average correlation (r) between the observed spike count for each of the 20 trials and the model-predicted firing rate. We also computed performance for an “oracle,” which predicts responses on a given trial using a rate estimated by averaging the other 19 trials. This provides an approximate upper-bound on performance of any stimulus-driven model. b–d, The subunit model outperforms all other models on cross-validated testing data (solid), but not on training data (hollow). This indicates significant overfitting for the other models, especially the Rust-STC model. e, Comparison of subunit and Rust-STC models to the oracle. On average, the subunit model (orange points) captures 76% of the variance explained by the oracle, and the Rust-STC model (purple points) captures 49%.

  • Figure 9.
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    Figure 9.

    Predicting responses to drifting gratings. a, Black dots indicate the measured tuning curve for drifting gratings over 16 directions. Colored lines indicate the model-predicted tuning curves for all four model types (model predictions are rescaled for illustration purposes; see Materials and Methods). b, For all cells, we quantify model tuning curve accuracy as the correlation between the actual tuning curve and the model-predicted tuning curve. Here, a histogram is plotted over all cells (n = 38). Triangles represent population means. Error bars (horizontal lines) indicate SD. c, Error in direction preference is smallest for the subunit model, but all models are unbiased in their error. d, Error in circular variance measures the width of the tuning curves (flat curves have a CV of 1). All models tend to predict flatter tuning curves than those measured from drifting gratings, but the subunit model is better than the other models on average. Black and blue curves at the bottom illustrate actual and model predicted tuning curves, respectively.

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The Journal of Neuroscience: 35 (44)
Journal of Neuroscience
Vol. 35, Issue 44
4 Nov 2015
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A Convolutional Subunit Model for Neuronal Responses in Macaque V1
Brett Vintch, J. Anthony Movshon, Eero P. Simoncelli
Journal of Neuroscience 4 November 2015, 35 (44) 14829-14841; DOI: 10.1523/JNEUROSCI.2815-13.2015

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A Convolutional Subunit Model for Neuronal Responses in Macaque V1
Brett Vintch, J. Anthony Movshon, Eero P. Simoncelli
Journal of Neuroscience 4 November 2015, 35 (44) 14829-14841; DOI: 10.1523/JNEUROSCI.2815-13.2015
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