Pharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro

doi:10.1016/j.neuroscience.2007.10.021

Neuroscience

Volume 151, Issue 2, 24 January 2008, Pages 386-395

https://doi.org/10.1016/j.neuroscience.2007.10.021 Get rights and content

Abstract

Parkinson’s disease (PD) is associated with enhanced synchronization of neuronal network activity in the beta (15–30 Hz) frequency band across several nuclei of the basal ganglia (BG). Deep brain stimulation of the subthalamic nucleus (STN) appears to reduce this pathological oscillation, thereby alleviating PD symptoms. However, direct stimulation of primary motor cortex (M1) has recently been shown to be effective in reducing symptoms in PD, suggesting a role for cortex in patterning pathological rhythms. Here, we examine the properties of M1 network oscillations in coronal slices taken from rat brain. Oscillations in the high beta frequency range (layer 5, 27.8±1.1 Hz, n=6) were elicited by co-application of the glutamate receptor agonist kainic acid (400 nM) and muscarinic receptor agonist carbachol (50 μM). Dual extracellular recordings, local application of tetrodotoxin and recordings in M1 micro-sections indicate that the activity originates within deep layers V/VI. Beta oscillations were unaffected by specific AMPA receptor blockade, abolished by the GABA type A receptor (GABA_AR) antagonist picrotoxin and the gap-junction blocker carbenoxolone, and modulated by pentobarbital and zolpidem indicating dependence on networks of GABAergic interneurons and electrical coupling. High frequency stimulation (HFS) at 125 Hz in superficial layers, designed to mimic transdural/transcranial stimulation, generated gamma oscillations in layers II and V (incidence 95%, 69.2±7.3 Hz, n=17) with very fast oscillatory components (VFO; 100–250 Hz). Stimulation at 4 Hz, however, preferentially promoted theta activity (incidence 62.5%, 5.1±0.6 Hz, n=15) that effected strong amplitude modulation of ongoing beta activity. Stimulation at 20 Hz evoked mixed theta and gamma responses. These data suggest that within M1, evoked theta, gamma and fast oscillations may coexist with and in some cases modulate pharmacologically induced beta oscillations.

Section snippets

Experimental procedures

Recordings were made in coronal slices (400 μm) containing M1, obtained from 40 to 60 g male Wistar rats. All experiments were performed in accordance with the Animals (Scientific Procedures) Act 1986, European Communities Directive 1986 (86/609/EEC) and the Aston University ethical review documents. Every effort was made to minimize the number of animals used and their suffering. Animals were first anesthetized with isoflurane and decapitated. The brain was quickly removed and placed in

Results

Under control conditions, in all layers of M1, network oscillations were not observed in the absence of pharmacological manipulations. Bath application of either the glutamate receptor agonist KA (400 nM) or muscarinic receptor agonist CCh (50 μM) alone increased neuronal activity, but no synchronous oscillatory activity was observed. However, co-application of KA and CCh reliably generated oscillatory activity in the high beta frequency range (25–30 Hz), which could be recorded in all cortical

Layer V drives oscillatory activity at beta frequencies

We have shown that co-application of KA and CCh produced robust beta oscillations in coronal slices of rat M1, and that other oscillatory frequencies can be elicited through stimulation paradigms. Previous reports in which KA and CCh have been applied alone or in combination have described oscillatory network activity in somatosensory cortex (Boddeke et al 1997, Buhl et al 1998, Roopun et al 2006), hippocampus (Fisahn et al 1998, Shimono et al 2000), and entorhinal cortex, (Cunningham et al.,

Acknowledgments

Research supported by Aston University overseas student bursary (N.Y.) and RCUK research fellowship (S.D.H.). We would like to thank Miles Whittington, Roger Traub, Mark Cunningham and Peter Magill for discussions and comments on the manuscript.

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Cellular neurosciencePharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro

Abstract

Section snippets

Experimental procedures

Results

Layer V drives oscillatory activity at beta frequencies

Acknowledgments

Clin Neurophysiol

Neuroscience

Exp Neurol

Lancet

Biochem Biophys Res Commun

Neuron

Neurosci Lett

Neurosci Lett

Clin Neurophysiol

Neuroscience

Neurosci Res

Neuropharmacology

Clin Neurophysiol

Neurosci Lett

Neuroscience

The primate subthalamic nucleusII. Neuronal activity in the MPTP model of Parkinsonism

J Neurophysiol

Synchronous 20 Hz rhythmic activity in hippocampal networks induced by activation of metabotropic glutamate receptors in vitro

Neuroscience

Cortical correlate of the Piper rhythm in humans

J Neurophysiol

Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease

J Neurosci

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

J Physiol

Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man

J Physiol

Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys

J Neurosci

Mechanism of action of the hypnotic zolpidem in vivo

Br J Pharmacol

Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro

J Neurosci

Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements

J Neurophysiol

Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism

Brain Res

Cellular neuroscience
Pharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro