Inhibitory Stabilization of the Cortical Network Underlies Visual Surround Suppression

By H. Ozeki, Ian M. Finn, Evan S. Schaffer, Kenneth D. Miller, D. Ferster. 2009

482 citations recorded by the source corpus.

SUMMARY In what regime does the cortical circuit operate? Our intracellular studies of surround suppression in cat primary visual cortex (V1) provide strong evidence on this question. Although suppression has been thought to arise from an increase in lateral inhibition, we find that the inhibition that cells receive is reduced, not increased, by a surround stimulus. Instead, suppression is mediated by a withdrawal of excitation. Thalamic recordings and previous work show that these effects cannot be explained by a withdrawal of thalamic input. We find in theoretical work that this behavior can only arise if V1 operates as an inhibition-stabilized network (ISN), in which excitatory recurrence alone is strong enough to destabilize visual responses but feedback inhibition maintains stability. We confirm two strong tests of this scenario experimentally, and show through simulation that observed cell-to-cell variability in surround effects, from facilitation to suppression, can arise naturally from variability in the ISN.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

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Citations in the corpus

Gamma-Aminobutyric Acid Concentration is Reduced in Visual Cortex in Schizophrenia and Correlates with Orientation-Specific Surround Suppression (2010, unknown): “…support from intracellular recordings of V1 neurons, in which presentation of a surround stimulus elicited a transient increase in inhibitory conductance, followed by a sustained reduction in both excitatory and inhibitory conductance, all of which were orientation selective (Ozeki et al., 2009).”
A Feedback Model of Attention Explains the Diverse Effects of Attention on Neural Firing Rates and Receptive Field Structure (2016, background): “The mechanisms for within-RF and surround suppression are likely to differ [43], and the mechanism for surround suppression remains largely unclear (see the apparently conflicting results of [44] and [45]; also [46] and [47]).”
Computing with a Canonical Neural Circuits Model with Pool Normalization and Modulating Feedback (2014, background): “…Brosch and H. Neumann Figure 5: Strong self-excitation and sigmoidal excitatory transfer function form an inhibition-stabilized network (ISN) (see Ozeki et al., 2009, Figure 6); that is, when additional surround input is provided, the intersection of the E-and I-nullcline is shifted down and to…”
GABAA inhibition controls response gain in visual cortex (2011, unknown): “, 2003; Priebe and Ferster, 2005) or for stimulus size (Ozeki et al., 2009; Haider et al., 2010).”
Balanced amplification: a new mechanism of selective amplification of neural activity patterns (2009, unknown): “) In V1 and other regions of cerebral cortex, recurrent excitation appears to be strong but balanced by similarly strong feedback inhibition (Chagnac-Amitai and Connors, 1989; Haider et al., 2006; Shu et al., 2003; Higley and Contreras, 2006; Ozeki et al., 2009), an arrangement often considered by t”
Synaptic and network mechanisms of sparse and reliable visual cortical activity during nonclassical receptive field stimulation. (2010, background): “response regime that strongly engages inhibitory circuits (Ozeki et al., 2009).”