Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque

Center for Neural Science, New York University, New York, New York 10003, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 09/2006; 26(34):8715-26. DOI: 10.1523/JNEUROSCI.0821-06.2006
Source: PubMed


The modulation sensitivity of visual neurons can be influenced by remote stimuli which, when presented alone, cause no change in the ongoing discharge rate of the neuron. We show here that the extraclassical surrounds that underlie these effects are present in magnocellular-pathway (MC) but not in parvocellular-pathway (PC) retinal ganglion cells of the macaque. The response of MC cells to drifting gratings and flashing spots was halved by drifting or contrast-reversing gratings surrounding their receptive fields, but PC cell responses were unaffected. The suppression cannot have arisen from the classical receptive field, or been caused by scattered light, because it could be evoked by annuli that themselves caused little or no response from the cell, and is consistent with the action of a divisive suppressive mechanism. Suppression in MC cells was broadly tuned for spatial and temporal frequency and greater at high contrast. If perceptual phenomena with similar stimulus contexts, such as the "shift effect" and saccadic suppression, have a retinal component, then they reflect the activity of the MC pathway.

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    • "However, little is known about the development of surround modulation and its dependence on early sensory experience , and how this impacts the ability to encode complex natural scenes. Surround modulation is mediated by excitatory and inhibitory interactions at different stages of the mature visual pathway, including the retina (Olveczky et al., 2003; Solomon et al., 2006) and visual cortex (Stettler et al., 2002; Angelucci and Bressloff, 2006; Girardin and Martin, 2009; Ozeki et al., 2009; Haider et al., 2010; Adesnik et al., 2012; Nienborg et al., 2013; Vaiceliunaite et al., 2013). Since both excitatory and inhibitory circuits refine after eye opening (Fré gnac and Imbert, 1984; Katagiri et al., 2007; Kuhlman et al., 2011; Ko et al., 2013) and are susceptible to changes in visual experience (Ruthazer and Stryker, 1996; Zufferey et al., 1999; White et al., 2001; Chattopadhyaya et al., 2004; Maffei et al., 2004), the effectiveness of surround modulation may be expected to change during postnatal development. "
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    • "Finally, our stimulus drove responses across much of the visual field exciting essentially all neurons in the visual system to some degree. It is possible that masking in Drosophila depends on the spatial configuration and extent of stimuli as it does in the human visual system (50,51) and that altering the relative sizes of the excitatory and inhibitory stimulus components can lead to a range of contrast response functions that encompass both response- and contrast-gain effects (42). "
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    • "– Divisive normalization is a mechanism that normalizes the response of a neuron by the summed activity of a pool of neurons. Such a computation is used in the retina to obtain light adaptation (Solomon et al. 2006), in area V1 (Heeger 1992), and in area MT (Simoncelli and Heeger 1998), where it explains the non-linear properties of neurons. Normalization is also used to remove noise from the responses of the units of a population code, thus improving the quality of the encoded information (Deneve et al. 1999). "
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