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The contribution of spike threshold to the dichotomy of cortical simple and complex cells

Abstract

The existence of two classes of cells, simple and complex, discovered by Hubel and Wiesel in 1962, is one of the fundamental features of cat primary visual cortex. A quantitative measure used to distinguish simple and complex cells is the ratio between modulated and unmodulated components of spike responses to drifting gratings, an index that forms a bimodal distribution. We have found that the modulation ratio, when derived from the subthreshold membrane potential instead of from spike rate, is unimodally distributed, but highly skewed. The distribution of the modulation ratio as derived from spike rate can, in turn, be predicted quantitatively by the nonlinear properties of spike threshold applied to the skewed distribution of the subthreshold modulation ratio. Threshold also increases the spatial segregation of ON and OFF regions of the receptive field, a defining attribute of simple cells. The distinction between simple and complex cells is therefore enhanced by threshold, much like the selectivity for stimulus features such as orientation and direction. In this case, however, a continuous distribution in the spatial organization of synaptic inputs is transformed into two distinct classes of cells.

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Figure 1: The nonlinear transformation from the voltage modulation ratio to the firing rate modulation ratio.
Figure 2: Intracellular responses to drifting gratings in four example neurons.
Figure 3: The distribution of responses to drifting gratings across our sample population.
Figure 4: The nonlinear transformation from the voltage modulation ratio to the firing rate modulation ratio in primary visual cortex.
Figure 5: The transformation between voltage modulation ratio and the firing rate modulation ratio in single cells.
Figure 6: ON and OFF spatial maps for both membrane potential and spikes.
Figure 7: A comparison of the various measures of grating modulation and spatial segregation of ON and OFF responses.

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Acknowledgements

We thank D.L. Ringach, J.D. Victor and K.D. Miller for comments on the manuscript. I. Lampl, D.C. Gillespie and J.S. Anderson participated in data collection. This work was supported by grants from the National Institutes of Health, the National Science Foundation and the Human Frontier Science Program.

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Correspondence to David Ferster.

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Priebe, N., Mechler, F., Carandini, M. et al. The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nat Neurosci 7, 1113–1122 (2004). https://doi.org/10.1038/nn1310

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