Synaptic and Network Mechanisms of Sparse and Reliable Visual Cortical Activity during Nonclassical Receptive Field Stimulation

Abstract

SUMMARY During natural vision, the entire visual field is stimulated by images rich in spatiotemporal structure. Although many visual system studies restrict stimuli to the classical receptive field (CRF), it is known that costimulation of the CRF and the surrounding nonclassical receptive field (nCRF) increases neuronal response sparseness. The cellular and network mechanisms underlying increased response sparseness remain largely unexplored. Here we show that combined CRF + nCRF stimulation increases the sparseness, reliability, and precision of spiking and membrane potential responses in classical regular spiking (RSC) pyramidal neurons of cat primary visual cortex. Conversely, fast-spiking interneurons exhibit increased activity and decreased selectivity during CRF + nCRF stimulation. The increased sparseness and reliability of RSC neuron spiking is associated with increased inhibitory barrages and narrower visually evoked synaptic potentials. Our experimental observations were replicated with a simple computational model, suggesting that network interactions among neuronal subtypes ultimately sharpen recurrent excitation, producing specific and reliable visual responses.

Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex

“…This result is consistent with our present study, as the movies we used spanned a large portion of the visual field. Thus, we believe that the fact that we found lower temporal variability in the movie responses compared with the grating responses can at least in part be explained by the same network effects observed by Haider et al (2010); rich, full-field stimuli engage the cortical network, whereas these effects are much less pronounced when simplistic stimuli are presented. Indeed, previous studies have found that combinations of simple stimuli, such as bars of different orientations, engage the visual cortex differently than if those features were presented in isolation.…”

“…High reliability in neural responses to natural movie stimuli was recently reported by Haider et al (2010). Interestingly, reliability, as well as sparseness, increased when the nonclassical receptive field was stimulated, compared with when only the classical receptive field received stimulation.…”

Intersubject variability and induced gamma in the visual cortex: DCM with empirical Bayes and neural fields

“…In this context, the activity of inhibitory cells within the visual network depends on stimulus condition and different sizes lead to changes in the excitation to inhibition balance—and weak suppression of interneurons [Haider et al, 2010]. Changes in the amplitude of gamma oscillations may be due to interactions between principal cells and interneurons as the grating patch expands beyond the classical receptive field.…”

Cortical states control visual spatial perception

“…Reduction of correlated activity (decorrelation) best accounts for perceptual improvements in these tasks (Cohen and Maunsell, 2009), but the neuronal subtypes involved remain unclear. Identifying cortical neuron subtypes in higher mammals presents challenges, since action potentials of many excitatory neurons are indistinguishable from those of inhibitory neurons (Constantinople et al, 2009;Haider et al, 2010;Soares et al, 2017;Vigneswaran et al, 2011). This may hinder full understanding of excitatory and inhibitory contributions to decorrelation and sensory perception.…”