Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro

Abstract

Concomitant application of the cholinergic agonist carbachol and nanomolar doses of kainate can elicit persistent gamma frequency oscillations in all layers of the mouse somatosensory cortex in vitro. Receptor pharmacology with bath‐applied antagonists indicated that oscillatory network activity depended crucially on the participation of cholinergic muscarinic, (S)‐α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazolepropionic acid (AMPA)/kainate and GABAA receptors. The timing of action potentials and the occurrence of excitatory as well as inhibitory postsynaptic events was highly correlated with the phasic change of extracellularly recorded population activity. Firing probability was lowest during the peak negativity of IPSPs and gradually increased during their ensuing decay. In conjunction with the effect of a barbiturate to decrease the frequency of gamma oscillations, this suggests a crucial role of IPSPs in phasing the suprathreshold activity of principal neurons. At nearby (< 1 mm) sites contained within any given cortical layer, oscillatory extra‐ and intracellular activity was highly synchronous with no apparent phase lag. However, interlaminar mapping experiments demonstrated a phase reversal of both extra‐ and intracellularly recorded activity near the lower border of thalamo‐recipient layer 4, thus corroborating findings that have been obtained in vivo. In conclusion, a modest increase of tonic excitatory drive in conjunction with the activation of cholinergic muscarinic receptors can elicit persistent gamma frequency network oscillations in the rodent somatosensory cortex. These findings (re)emphasize the role of the cholinergic ascending system in the cortical processing of sensory information.

Interaction between neocortical and hippocampal networks via slow oscillations

“…Gamma oscillations have also been observed in vivo in the hippocampus and the entorhinal cortex of rats (Stumpf, 1965;Buzsáki et al, 1983;Chrobak and Buzsáki, 1998a;Bragin et al, 1995a), the amygdala, the entorhinal and perirhinal cortices and the neocortex of cats (Boeijinga and Lopes da Silva, 1988;Gray et al, 1989;Engel et al, 1991;Collins et al, 2001), the neocortex of the monkeys (Kreiter and Singer, 1996) and in the human neocortex (Llinás and Ribary, 1993;Uchida et al, 2001). Gamma oscillations are also induced by various pharmacological manipulations in vitro Buhl et al, 1998;Fisahn et al, 1998). In the hippocampus, at least two distinct gamma generators have been identified: one depends on the perforant path input from the entorhinal cortex, whereas the other emerges in the CA3 region Csicsvari et al, 2003).…”

Origin of intrinsic irregular firing in cortical interneurons

“…Cortical GABAergic interneurons have a range of functions including the gating (13) and entrainment (14) of neuronal firing, dendritic integration (15), synaptic plasticity (16), and the generation of network oscillations (10,11). There are several morphologically and physiologically distinct classes of interneurons (17).…”

“…The irregularity of pyramidal neuron firing in vivo arises from the intense, ongoing, temporally correlated synaptic activity that bombards cortical neurons (1, 2, 5-7). The lower in vitro irregularity can be raised to in vivo levels by using fluctuating current injection (8), hyperosmolar solution (9), and a neuromodulatory mixture (10,11).…”

Adolescent Cannabinoid Exposure Permanently Suppresses Cortical Oscillations in Adult Mice

“…The method we used-KA (400 nM) and CCh (20 mM)-reliably produces b and g oscillations in cortical slices (Buhl et al, 1998;Oke et al, 2010) that strongly resemble network synchrony in the intact neocortex (Steriade et al, 1996). KA and CCh promote robust LFP oscillations in vitro by enhancing excitatory drive (Buhl et al, 1998;Cunningham et al, 2003) and activating cholinergic receptors on GABAergic interneurons Gulyás et al, 2010). Coronal brain slices containing medial prefrontal cortex (mPFC) or primary somatosensory cortex (SCx) were prepared from adult mice administered WIN or vehicle during adolescence (Figure 1a).…”

“…Discrete fast Fourier transforms (FFTs) were performed on 10 s of LFP data and oscillation power (area under the curve) was integrated at different frequencies (y ¼ 4-7 Hz; a ¼ 8-12 Hz; b ¼ 13-29 Hz; g ¼ 30-80 Hz). Frequency bandwidth boundaries were based on Buhl et al, 1998 and. Statistical analyses were performed with STATA (Version 12, StataCorp, College Station, TX).…”