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Jan Homann, Michael Freed; A Non-Conventional Circuit Mechanism for the Center-Surround Receptive Field of a Retinal Ganglion Cell. Invest. Ophthalmol. Vis. Sci. 2013;54(15):3392.
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© ARVO (1962-2015); The Authors (2016-present)
A conventional explanation for the receptive structure of a ganglion cell is that the center and antagonistic surround are provided by a narrow excitatory input and a broader inhibitory input, respectively. Yet the OFF-alpha ganglion cell receives excitatory and inhibitory inputs of about the same spatial extent. Thus the purpose of our study was to map the spatial structure of inhibitory and excitatory inputs to this ganglion cell type to understand how these inputs generate a center/surround receptive field.
We constructed a sequence of randomly flickering rings covering the whole receptive field (suggested by Dr. B. Borghuis) (Fig. 1). We recorded excitatory and inhibitory currents by voltage clamping in the whole-cell mode. We generated a spatio-temporal filter and a static nonlinearity for both currents. The amplitude of the filter was plotted against ring radius.
Spatial plots of both excitatory and inhibitory currents showed center-surround structure (Fig. 2). Excitatory and inhibitory plots were concentric, such that an increase in excitatory conductance was spatially and temporally aligned with a decrease in inhibitory conductance and vice versa. The excitatory current’s center outweighed its surround (c/s = 4.5) whereas the inhibitory current was spatially balanced (c/s = 1.1). Compared to the excitatory current, the inhibitory current was less rectified. At the resting potential, both inhibitory and excitatory conductances contributed equally to currents in the ganglion cell, and thus these currents showed a typical center-surround structure.
The receptive field of the OFF-alpha cell does not result from a conventional antagonism between inhibition and excitation. Instead inhibitory and excitatory conductances synergize with each other. Presumably then, the center-surround antagonism is pre-formed in the presynaptic bipolar and amacrine cells. The amacrine cells provide the inhibitory input and have a stronger receptive field surround than the bipolar cells. Changing the relative driving forces for excitatory and inhibition conductances may allow a dynamic adjustment of center/surround balance that would serve adaptation to strong contrasts or intensities as has been observed for the cortex.
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