Abstract
In vivo, theta (4–7 Hz) and gamma (30–80 Hz) neuronal network oscillations are known to coexist and display phase-amplitude coupling (PAC). However, in vitro, these oscillations have for many years been studied in isolation. Using an improved brain slice preparation technique we have, using co-application of carbachol (10 μM) and kainic acid (150 nM), elicited simultaneous theta (6.6 ± 0.1 Hz) and gamma (36.6 ± 0.4 Hz) oscillations in rodent primary motor cortex (M1). Each oscillation showed greatest power in layer V. Using a variety of time series analyses we detected significant cross-frequency coupling in 74% of slice preparations.Differences were observed in the pharmacological profile of each oscillation. Thus, gamma oscillations were reduced by the GABAA receptor antagonists, gabazine (250 nM and 2 μM), and picrotoxin (50 μM) and augmented by AMPA receptor antagonism with SYM2206 (20 μM). In contrast, theta oscillatory power was increased by gabazine, picrotoxin and SYM2206. GABAB receptor blockade with CGP55845 (5 μM) increased both theta and gamma power, and similar effects were seen with diazepam, zolpidem, MK801 and a series of metabotropic glutamate receptor antagonists. Oscillatory activity at both frequencies was reduced by the gap junction blocker carbenoxolone (200 μM) and by atropine (5 μM).These data show theta and gamma oscillations in layer V of rat M1 in vitro are cross-frequency coupled, and are mechanistically distinct. The development of an in vitro model of phase-amplitude coupled oscillations will facilitate further mechanistic investigation of the generation and modulation of coupled activity in mammalian cortex.
Highlights
Previous work in our laboratory (Yamawaki et al, 2008) showed that the amplitude of beta oscillatory activity was greatest in deep layers of primary motor cortex (M1) and we investigated the power of theta and gamma activity across cortical layers
We have previously shown that beta frequency oscillatory activity in M1 is sensitive to ligands which bind at the benzodiazepine site of the GABAA receptor, and we explored the actions of benzodiazepine site ligands on theta and gamma activity
It is well established that activation of metabotropic glutamate receptor (mGluR) may induce oscillatory activity in vitro (Whittington et al, 1995), and we investigated the effect of antagonists for each of the group I mGluR subtypes to assess their involvement in theta and gamma oscillations in M1
Summary
Gamma oscillations (30e80 Hz) play a role in attentive states such as sensory perception (Engel and Singer, 2001; Gray et al, 1989; Gray, 1994; Singer and Gray, 1995), memory processing (Chrobak and Buzsaki, 1998; Lisman and Idiart, 1995) and movement execution (Brown et al, 1998; Cheyne et al, 2008; Abbreviations: aCSF, artificial cerebrospinal fluid; CCh, carbachol; EPSC, excitatory postsynaptic current; EPSP, excitatory postsynaptic potential; IPSP, inhibitory postsynaptic potential; KA, kainic acid; LFP, local field potential; M1, primary motor cortex; mGluR, metabotropic glutamate receptor; PAC, Phase-amplitude coupling.Muthukumaraswamy, 2010; Pfurtscheller et al, 2003). The amplitude of the gamma frequency oscillation is enhanced in phase with the theta cycle due to neuron recruitment This phenomenon, known as cross-frequency coupling (CFC; Canolty et al, 2006), aids interneuronal network communication and processing such that communications arriving out of phase may be ignored while information in phase may be treated preferentially. In this way, theta may serve to act as a global temporal coordinator of local network activity (Sirota et al, 2008), and theta-gamma coupling has been shown to be essential for structuring of motor-related activity in rodent M1 (Igarashi et al, 2013)
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