Abstract
Neurons in the primary visual cortex are known for responding vigorously but with high variability to classical stimuli such as drifting bars or gratings. By contrast, natural scenes are encoded more efficiently by sparse and temporal precise spiking responses. We used a conductance-based model of the visual system in higher mammals to investigate how two specific features of the thalamo-cortical pathway, namely push-pull receptive field organization and fast synaptic depression, can contribute to this contextual reshaping of V1 responses. By comparing cortical dynamics evoked respectively by natural vs. artificial stimuli in a comprehensive parametric space analysis, we demonstrate that the reliability and sparseness of the spiking responses during natural vision is not a mere consequence of the increased bandwidth in the sensory input spectrum. Rather, it results from the combined impacts of fast synaptic depression and push-pull inhibition, the later acting for natural scenes as a form of “effective” feed-forward inhibition as demonstrated in other sensory systems. Thus, the combination of feedforward-like inhibition with fast thalamo-cortical synaptic depression by simple cells receiving a direct structured input from thalamus composes a generic computational mechanism for generating a sparse and reliable encoding of natural sensory events.
Highlights
Simple cells, in the thalamic recipient layers of area V1, exhibit spatial segregation and contrast opponency between their spiking ON- and OFF-subfields (Hirsch et al, 1998; Martinez et al, 2005)
Our objective was to systematically investigate how push-pull receptive field organization of V1 simple cells and feedforward synaptic depression at the thalamocortical synapse could contribute to this contextual reshaping of V1 responses
Other artificial and natural images/movies stimuli have been extensively used to characterize Lateral Geniculate Nucleus (LGN) response properties (Ferster et al, 1996; Cai et al, 1997; Kara et al, 2000; Mante et al, 2005, 2008; Allen and Freeman, 2006; Butts et al, 2007, 2010, 2011; Sadagopan and Ferster, 2012). These studies show that LGN cells follow the driving frequency of a drifting grating (Carandini et al, 2005; Mante et al, 2005) and that natural visual stimuli are encoded in an episodic manner, i.e., epochs increased evoked activity are interleaved with quiet epochs (Butts et al, 2010)
Summary
In the thalamic recipient layers of area V1, exhibit spatial segregation and contrast opponency between their spiking ON- and OFF-subfields (Hirsch et al, 1998; Martinez et al, 2005). As a consequence, their spiking follows the driving temporal frequency of drifting gratings of optimal orientation and spatial frequency (Figures 1A,B). V1 Model for Natural Images becomes shorter than the time constant of the autocorrelation function of the natural stimulus contrast dynamics (Figure 1D). It is still not completely understood what mechanisms underlie these differences between artificial and naturalistic conditions
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