A spontaneous state of weakly correlated synaptic excitation and inhibition in visual cortex

Abstract

Cortical spontaneous activity reflects an animal’s behavioral state and affects neural responses to sensory stimuli. The correlation between excitatory and inhibitory synaptic input to single neurons is a key parameter in models of cortical circuitry. Recent measurements demonstrated highly correlated synaptic excitation and inhibition during spontaneous “up-and-down” states, during which excitation accounted for approximately 80% of inhibitory variance (Shu et al., 2003; Haider et al., 2006). Here we report in vivo whole-cell estimates of the correlation between excitation and inhibition in the rat visual cortex under pentobarbital anesthesia, during which up-and-down states are absent. Excitation and inhibition are weakly correlated, relative to the up-and-down state: excitation accounts for less than 40% of inhibitory variance. Although these correlations are lower than when the circuit cycles between up-and-down states, both behaviors may arise from the same circuitry. Our observations provide evidence that different correlational patterns of excitation and inhibition underlie different cortical states.

Network and cellular mechanisms underlying heterogeneous excitatory/inhibitory balanced states

“…Since it was first proposed that excitatory/inhibitory ( E / I ) balance emerges within brain networks (van Vreeswijk & Sompolinsky, ), a large body of theoretical and experimental work has focused on clarifying its regulation and possible role in maintaining desired spatiotemporal activity states (Deneve & Machens, ). Co‐occurring E / I responses have been observed for many modalities, for example, in auditory cortex (D'Amour & Froemke, ; Wehr & Zador, ), visual cortex (Liu et al, ; Tan, Andoni, & Priebe, ) and olfactory cortex (Poo & Isaacson, ; Stettler & Axel, ). Besides activity evoked by stimuli, balanced excitation and inhibition also appear to be present during spontaneous brain activity (Graupner & Reyes, ; Murphy & Miller, ) and may play a critical role in generating certain brain rhythms (Atallah & Scanziani, ).…”

“…The interaction of recurrent inhibitory and excitatory circuits also regulates the occurrence of cortical up and down states (Haider, Duque, Hasenstaub, & McCormick, ; Shu, Hasenstaub, & McCormick, ), and it was shown that different levels of correlation between excitation and inhibition can emerge from the same neuronal circuitry, depending on the specific cortical state—with correlations observed to be lower during anesthesia than during states exhibiting up and downstate activity (Tan et al, ).…”

“…It is impossible to simultaneously measure the excitatory and inhibitory post‐synaptic currents (EPSCs and IPSCs) at every neuron across a network. Several indirect experimental quantifications (e.g., cell‐wise measurement of excitatory and inhibitory conductance obtained from whole‐cell recording) have also been used (Landau, Egger, Dercksen, Oberlaender, & Sompolinsky, ; Monier, Fournier, & Fregnac, ; Tan et al, ; Wehr & Zador, ; Xue, Atallah, & Scanziani, ). Although each of these captures characteristics of E / I balance in some way, none of them quantifies all of the features that simultaneously contribute to E / I balance.…”

Simultaneous Bayesian Estimation of Excitatory and Inhibitory Synaptic Conductances by Exploiting Multiple Recorded Trials

“…For example, Tan et al (2013) proposed a methodology to calculate the Pearson correlation of excitatory and inhibitory SCs from stationary data based on the dependency of the variance of membrane current on holding potential. This approach is distinct from MtKF because MtKF infers the full time course of conductances as opposed to only certain statistics.…”

Bringing the Dynamics of Movement under Control

“…Testing this model prediction directly might be difficult, as it is hard to isolate excitatory and inhibitory inputs onto a single neuron simultaneously. However, the observed arrangement makes the prediction that the magnitude of temporal fluctuations in membrane potential measured at the reversal of either excitation or inhibition should be much larger than those measured at normal operating potentials, which can be tested (Tan et al, 2013).…”