Selective Functional Interactions between Excitatory and Inhibitory Cortical Neurons and Differential Contribution to Persistent Activity of the Slow Oscillation

Abstract

The neocortex depends upon a relative balance of recurrent excitation and inhibition for its operation. During spontaneous Up states, cortical pyramidal cells receive proportional barrages of excitatory and inhibitory synaptic potentials. Many of these synaptic potentials arise from the activity of nearby neurons, although the identity of these cells is relatively unknown, especially for those underlying the generation of inhibitory synaptic events. To address these fundamental questions, we developed an in vitro submerged slice preparation of the mouse entorhinal cortex that generates robust and regular spontaneous recurrent network activity in the form of the slow oscillation. By performing whole cell recordings from multiple cell types identified with green fluorescent protein expression and electrophysiological and/or morphological properties, we show that distinct functional subpopulations of neurons exist in the entorhinal cortex, with large variations in contribution to the generation of balanced excitation and inhibition during the slow oscillation. The most active neurons during the slow oscillation are excitatory pyramidal and inhibitory fast spiking interneurons, receiving robust barrages of both excitatory and inhibitory synaptic potentials. Weak action potential activity was observed in stellate excitatory neurons and somatostatin containing interneurons. In contrast, interneurons containing neuropeptide Y, vasoactive intestinal peptide, or the 5-hydroxytryptamine (serotonin) 3a receptor, were silent. Our data demonstrate remarkable functional specificity in the interactions between different excitatory and inhibitory cortical neuronal subtypes, and suggest that it is the large recurrent interaction between pyramidal neurons and fast spiking interneurons that is responsible for the generation of persistent activity that characterizes the depolarized states of the cortex.

Fast Gamma Oscillations Are Generated Intrinsically in CA1 without the Involvement of Fast-Spiking Basket Cells

“…Disconnecting CA3 from CA1 did not affect the frequency of gamma oscillations in our experiments, consistent with focal KA application only activating local circuits and not all of the hippocampus. Interestingly, also disconnecting the subiculum moderately increased the gamma frequency in CA1, perhaps due to removal of an inhibitory feedback mechanism from the subiculum to CA1 (Sun et al, 2014).…”

“…experimentally because both axo-axonic and fast-spiking basket cells express parvalbumin, and optogenetically driving parvalbumin-positive interneurons is sufficient to generate gamma rhythms (Cardin et al, 2009;Sohal et al, 2009). …”

Imaging extracellular potassium dynamics in brain tissue using a potassium-sensitive nanosensor

“…17 Slices were imaged in an open chamber superfused with ACSF, bubbled with 95% O 2 5% CO 2 . ACSF solution contains (mM): NaCl 125, KCl 3, NaHCO 3 25, CaCl 2 1.2, MgSO 4 1, NaH 2 PO 4 1.25, glucose 10.…”

Neural networks with excitatory and inhibitory components: Direct and inverse problems by a mean-field approach

“…Many brain activities emerge as the combined effect of excitatory and inhibitory components associated with synaptic plasticity [1][2][3][4][5][6]. In mammalians, the fraction of inhibitory neurons is close to 20%-30% [7], and it seems plausible that this value was determined by evolutionary constraints, aiming at the effectiveness of brain functions.…”