Adaptation modulates correlated subthreshold response variability in visual cortex

Abstract

Cortical sensory responses are highly variable across stimulus presentations. This variability can be correlated across neurons (due to some combination of dense intracortical connectivity, cortical activity level, and cortical state), with fundamental implications for population coding. Yet the interpretation of correlated response variability (or "noise correlation") has remained fraught with difficulty, in part because of the restriction to extracellular neuronal spike recordings. Here, we measured response variability and its correlation at the most microscopic level of electrical neural activity, the membrane potential, by obtaining dual whole cell recordings from pairs of cortical pyramidal neurons during visual processing in the turtle whole brain ex vivo preparation. We found that during visual stimulation, correlated variability adapts toward an intermediate level and that this correlation dynamic is likely mediated by intracortical mechanisms. A model network with external inputs, synaptic depression, and structure reproduced the observed dynamics of correlated variability. These results suggest that intracortical adaptation self-organizes cortical circuits toward a balanced regime at which correlated variability is maintained at an intermediate level. Correlated response variability has profound implications for stimulus encoding, yet our understanding of this phenomenon is based largely on spike data. Here, we investigate the dynamics and mechanisms of membrane potential-correlated variability (CC) in visual cortex with a combined experimental and computational approach. We observe a visually evoked increase in CC, followed by a fast return to baseline. Our results further suggest a link between this observation and the adaptation-mediated dynamics of emergent network phenomena.

Induced cortical oscillations in turtle cortex are coherent at the mesoscale of population activity, but not at the microscale of the membrane potential of neurons

“…Furthermore, the intracellular and extracellular activity we observed was qualitatively similar to that reported in previous studies in which cryoanesthesia (rather than propofol) was administered to the turtle (Kriegstein 1987;Prechtl et al 1997Prechtl et al , 2000. Finally, using the approach describe in this article, we have recorded extracellular visual responses (Clawson et al 2017;Shew et al 2015;Wright et al 2017) that were qualitatively similar to those in the awake animal (Rutishauser et al 2013).…”

Single-Cell Membrane Potential Fluctuations Evince Network Scale-Freeness and Quasicriticality

“…Turtles were anesthetized with propofol (2 mg of propofol/kg) then decapitated. Dissection proceeded as described previously (Saha et al, 2011;Crockett et al, 2015;Wright et al, 2017a).…”

Single-cell membrane potential fluctuations evince network scale-freeness and quasicriticality

“…Turtles were anesthetized with Propofol (2 mg Propofol/kg), then decapitated. Dissection proceeded as described previously (Saha et al, 2011;Crockett et al, 2015;Wright et al, 2017a).…”

“…Recorded Vm fluctuations taken in the dark (no visual stimulation) were interpreted as ongoing activity. Such ongoing cortical activity was interrupted by visual stimulation of the retina with whole-field flashes and naturalistic movies as described previously (Wright et al, 2017a;Wright et al, 2017b;Wright and Wessel, 2017). An uninterrupted recording of ongoing activity lasted for 2 to 5 minutes.…”