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Functionally distinct inhibitory neurons at the first stage of visual cortical processing

Abstract

Here we explore inhibitory circuits at the thalamocortical stage of processing in layer 4 of the cat's visual cortex, focusing on the anatomy and physiology of the interneurons themselves. Our immediate aim was to explore the inhibitory mechanisms that contribute to orientation selectivity, perhaps the most dramatic response property to emerge across the thalamocortical synapse. The broader goal was to understand how inhibitory circuits operate. Using whole-cell recording in cats in vivo, we found that layer 4 contains two populations of inhibitory cells defined by receptive field class—simple and complex. The simple cells were selective for stimulus orientation, whereas the complex cells were not. Our observations help to explain how neurons become sensitive to stimulus orientation and maintain that selectivity as stimulus contrast changes. Overall, the work suggests that different sources of inhibition, either selective for specific features or broadly tuned, interact to provide appropriate representations of elements within the environment.

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Figure 8: Summary of results.
Figure 1: Morphology of smooth cells with simple receptive fields.
Figure 2: The receptive fields of smooth and spiny simple cells look alike.
Figure 3: Push-pull structure of the smooth simple cell receptive field.
Figure 4: Smooth simple cells are orientation-selective.
Figure 5: Morphology of smooth cells with complex receptive fields.
Figure 6: Push-push structure of the complex smooth cell receptive field.
Figure 7: Smooth complex cells are not orientation-selective.

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Acknowledgements

We thank T.N. Wiesel for discussions, K.D. Miller for improving the manuscript, R.C. Reid for contributing software and C.G. Marshall, K.D. Naik and J.M. Provost for assistance with the reconstructions. Supported by National Institutes of Health EY09593 to J.A.H.

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Correspondence to Judith A Hirsch.

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Supplementary information

Supplementary Fig. 1.

Responses to oriented bars for three additional simple and three additional complex cells. Each panel in a-f shows results from a single interneuron; simple cells (a-c), complex cells (d-f). For every cell, a contour plot of the receptive field is shown above averaged responses to variously oriented moving bars. In each column of records, the top trace depicts the response evoked by an optimally oriented bar; subsequent records show responses to bars tilted 22, 45, and 90° away from the preferred orientation. For the simple cell of panel a, an optimally oriented dark bar evoked a pattern of depolarization, hyperpolarization and depolarization as it crossed the Off, On and Off subregions. The response was similar at the near preferred angle and then diminished as the stimulus tilted towards the orthogonal orientation; similar patterns were seen in c for a cell whose receptive field also had three subregions. The records shown in b are from a cell whose receptive field has just two subregions. As a bright bar coursed over the On and Off subregions it first elicited a depolarization, then a hyperpolarization and finally a second depolarization on exit from the receptive field. For complex cells, (d-f), responses to the moving bars were similar at all orientations. Scale bars are 5 mV and 200 msec; all conventions as for figures in the text. A plot of the tuning curves for depolarization for all cells is shown in g; gray lines indicate curves for complex cells and black lines curves for simple cells. (JPG 43 kb)

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Hirsch, J., Martinez, L., Pillai, C. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci 6, 1300–1308 (2003). https://doi.org/10.1038/nn1152

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