Effect of cortical spreading depression on basal forebrain neurons

Abstract

During natural sleep and anesthesia, rhythmic hypo- and hyperpolarizations alternate in cortical pyramidal cells and are reflected as slow (<1 Hz) cortical rhythm at the level of the electroencephalogram (EEG). Membrane potential changes in pyramidal neurons were initially attributed to the rhythmic fluctuation of the cholinergic input as the basal forebrain (BF) neurons fire in synchrony with cortical waves, but a more recent proposal suggested that the slow rhythm was of cortical origin. In the present experiments, interaction between the cortex and the BF was examined in urethane-anesthetized rats. BF neuronal activity was inhibited by local infusion of lidocaine into the substantia innominata in one group of rats, while in another group, the slow cortical rhythm was blocked by inducing spreading depression (SD) in the cortex. Slow cortical rhythm persisted after unilateral lidocaine injection, but rhythmic firing in BF neurons disappeared following SD induction. These findings support the view that slow cortical rhythm is generated in the cortex and transmitted to the BF through descending fibers. According to anatomical data, these fibers can excite cholinergic cells only indirectly as they terminate on non-cholinergic neurons. Thus, timing of activity changes in BF neurons during the slow cortical rhythm might give some clue regarding their transmitter specificity.

Unilateral Cortical Spreading Depression Affects Sleep Need and Induces Molecular and Electrophysiological Signs of Synaptic Potentiation In Vivo

“…Another possibility is that slow waves were caused by a local disruption of cholinergic transmission in the cerebral cortex. Cholinergic antagonists such as atropine induce cortical slow waves in all behavioral states (Bradley et al 1968), and CSD virtually silences neuronal activity within the basal forebrain, where many cholinergic neurons are located (Szentgyorgyi et al 2006). Moreover, slow waves induced by cholinergic antagonists subside during active waking (Buzsaki et al 1988) similar to the disappearance of slow waves with active exploration in our rats.…”

Effect of sleep deprivation on multi-unit discharge activity of basal forebrain

“…In addition, BF neuronal responses can be evoked from cortex (Gyengési et al. , 2008) and cortical slow rhythms can be generated and transmitted to the BF (Szentgyörgyi et al. , 2006), suggesting that the changes in the cortical activity may result in changes in the BF discharge rate.…”

“…Studies on both anaesthetized and freely moving rats have demonstrated a relationship between EEG waves and BF discharge rates (Detari et al, 1997a,b;Kostin et al, 2008;Lee et al, 2004Lee et al, , 2005. In addition, BF neuronal responses can be evoked from cortex (Gyenge´si et al, 2008) and cortical slow rhythms can be generated and transmitted to the BF (Szentgyo¨rgyi et al, 2006), suggesting that the changes in the cortical activity may result in changes in the BF discharge rate. Recent studies have demonstrated electrophysiological and molecular changes in the cortex associated with SD (Cirelli, 2006;Huber et al, 2007;Vyazovskiy et al, 2008).…”

Interaction of slow cortical rhythm with somatosensory information processing in urethane-anesthetized rats

“…SCR was declared to be of cortical origin as thalamic ablations did not abolish cortical active and silent states (Steriade et al, 1993b) and cortical ablations prevented active states from occurring in the striatum and thalamus (Nita et al, 2003;Steriade et al, 1993b). The SCR is synchronized over the cortical mantle (Volgushev et al, 2006), and also reaches subcortical targets, including the striatum (Wilson & Kawaguchi, 1996), basal forebrain (Szentgyorgyi et al, 2006), subthalamic nucleus-globus pallidus (Magill et al, 2000), hippocampus (Wolansky et al, 2006), thalamus (Steriade et al, 1994), and pedunculopontine tegmental nucleus (PPT) (Balatoni & Detari, 2003).…”