Contralateral 80–280 Hz EEG ripples and hippocampal single unit discharge inhibition in response to acute tetanization of rat right caudate putamen in vivo

Abstract

Clinically, 4–8 Hz (or 30–80 Hz) stimulation of the caudate nucleus ceases (or enhances) the neocortical and hippocampal epileptiform activities of the epilepsy patients. Possibly, electric stimulation of the caudate nucleus could produce epilepsy. In order to prove this point we delivered the acute tetanization (60 Hz, 2 s, 0.4–0.6 mA) into the rat right caudate putamen nucleus (ATRC) and examined bilateral neocortical EEG and hippocampal unit discharges in vivo. The results demonstrated that: (1) 80–280 Hz EEG ripples could be evoked bilaterally, and more stronger on the contralateral side. And the maximum amplitudes of the power spectra (μV²/Hz) have higher shifting variability among multiple contralateral EEG ripples. (2) The EEG ripples were coupled contralaterally with the hippocampal neuronal firing inhibition. (3) An episode of 10–15 Hz EEG oscillations was ipsilaterally coupled with rhythmic hippocampal neuronal bursts. It suggested that the hemispheric reactions of neocortical EEG and hippocampal neuronal discharges are lateralized in response to the stimulation. It implies that the epileptic network activities were reorganized by the ATRC. Neocortical EEG ripples, called as seizure-like fast oscillations, were repetitively evoked by the ATRC.

Introduction

Fast oscillations (>80 Hz), termed ripples, were observed either in the cortex (Jones and Barth, 1999, Jones et al., 2000, Cunningham et al., 2004a, Traub et al., 2005) or in the hippocampus (HPC) (Ylinen et al., 1995, Traub et al., 1999, Bragin et al., 1999, Bragin et al., 2002a). Not only hippocampal but also neocortical gamma oscillations have distinctive electrophysiological changes of the neurons, which act as network members (Maier et al., 2003, Cunningham et al., 2004b). These ripples are attributed to a short-term synchronization of the coordinated activity of neuronal ensembles within a local network (Plenz and Kitai, 1996, Grenier et al., 2001, Grenier et al., 2003, Bragin et al., 2002a, Bragin et al., 2003). In humans occipital gamma oscillations (30–80 Hz) and sensorimotor cortical beta oscillations were modulated during the establishment of neural network before the forthcoming predictable visual stimulus (Kilner et al., 2005). It indicated that the hippocampal or neocortical ripples carry the important information of the neural network and may imply the reorganization of new functional neural network.

Generally, the HPC and the neocortex are related to epileptogenesis in humans and animals. The ripples within them are regarded as seizure-like oscillations or epileptic network seizures. They are commonly detected during animal epilepsy (Bragin et al., 2002b, Bragin et al., 2004, Grenier et al., 2001, Grenier et al., 2003, Staba et al., 2004). 80–160 Hz entorhinal cortical and hippocampal ripples were simultaneously observed also in epileptic patients (Bragin et al., 1999). A lot of elegant research works have proved the local network or cellular mechanisms of the ripples, but not the distant. For example, the hippocampal ripple genesis needs synchronously local neuronal bursting (Maier et al., 2003, Dzhala and Staley, 2004). And the neocortical ripples could be suppressed by electric stimulation of local network in humans (Kinoshita et al., 2004). It implied a possible network or cellular modulation of the distant brain areas on the ripples also.

The basal ganglia play an effective role in controlling seizures in animal epilepsy (Magill et al., 2005) and human epilepsy (da Silva et al., 1999). The cat hippocampal epilepsy was inhibited by the caudate nucleus stimulation (La Grutta and Sabatino, 1988, Vella et al., 1991). Clinically, 4–8 Hz caudate nucleus stimulation decreased the neocortical epileptic activity. But not all the seizures could be eliminated. 30–100 Hz caudate nucleus stimulation could enhance the epileptiform activities of the neocortex and the HPC in the epilepsy patients (Chkhenkeli et al., 2004). We have to understand the effect of caudate nucleus stimulation on fundamental neocortical or hippocampal EEG activities without epilepsy. It may be used to interpret why no satisfy therapy effects were observed when the caudate nucleus stimulation is delivered to control patients’ epilepsy. To prove the point view the parameter of 60 Hz, 2 s is chosen to stimulate the rat caudate putamen in the present work, which was used for the establishment of an effective model of status epilepticus in the HPC before (Rafiq et al., 1995). The bilateral neocortical or hippocampal EEG and hippocampal unit discharges are empathetically detected after electric tetanization of the rat caudate putamen (CPu). The work aims at the effect of the unilaterally electric activated-CPu on bilateral neocortical EEG activities and its hippocampal cellular electrophysiological changes.