Slow oscillation of membrane currents mediated by glutamatergic inputs of rat somatosensory cortical neurons: in vivo patch‐clamp analysis

Abstract

Using in vivo patch-clamp technique, the slow oscillation of membrane currents was characterized by its synaptic nature, correlation with electroencephalogram (EEG) and responses to different anesthetic agents, in primary somatosensory cortex (SI) neurons in urethane-anesthetized rats. In more than 90% of the SI neurons, the slow oscillation of the inward currents (0.1-2.5 Hz) with the duration of several hundreds of a millisecond was observed at the holding membrane potential of -70 mV. The reversal potential of the inward currents was approximately 0 mV and was suppressed by application of an alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA) receptor antagonist. In most cases (> 90%) the inward current was synchronized with positive wave of the surface EEG recorded from ipsilateral and even contralateral cortical regions. The frequency as well as duration of the slow oscillation decreased by a volatile anesthetic agent, isoflurane (1.5-5.0%), and excitatory postsynaptic currents (EPSCs) were almost abolished at the highest concentration. Intraperitoneal injection of pentobarbital (25 mg/kg) also decreased the frequency of the slow oscillation without affecting short EPSCs. When gamma-aminobutyric acid A (GABA(A)) receptors were activated by local microinjection of muscimol (3 x 10(-3) m, 1-10 microL) into the thalamus, the frequency of the slow oscillation markedly decreased, but was not abolished completely. These findings suggest that the slow oscillation of the inward currents is generated by the summation of glutamatergic EPSCs, and affected by isoflurane and pentobarbital differently. In addition, GABAergic system in the thalamus can affect the frequency, but is not essentially implicated in the genesis of the slow oscillation.

Large Scale Cortical Functional Networks Associated with Slow-Wave and Spindle-Burst-Related Spontaneous Activity

“…Soon after its description in anesthetized cats, it was shown during natural sleep in cats (Steriade et al, 1996; Amzica and Steriade, 1998) and in humans (Achermann and Borbély, 1997; Simon et al, 2000) and it has since been demonstrated in rodents (Cowan and Wilson, 1994; Petersen et al, 2003; Doi et al, 2007; Ruiz-Mejias et al, 2011). Subsequent investigations have shown it exists in nearly all sensory, motor and association areas of the cortex (Steriade et al, 1993c; Ferezou et al, 2006; Mohajerani et al, 2013) and synchronizes the membrane potential of cells in different functional regions far removed from each other (Destexhe et al, 1999; Volgushev et al, 2006; Dickson, 2010).…”

Thermal Hyperalgesia via Supraspinal Mechanisms in Mice Lacking Glutamate Decarboxylase 65

“…Recently, the in vivo whole-cell patch-clamp recording technique has been applied to rat somatosensory cortical neurons (Doi et al, 2007). Recording neurons, which respond to brush or pinch stimulation of contralateral hind limb, were located between 0.5 and 1.0 mm in the depth from the brain surface (Doi et al, 2007), suggesting that these neurons are largely layer V pyramidal neurons. Taking these findings into consideration, we then looked at the influence of deleting GAD65 gene on spontaneous GABAergic synaptic currents in sensory cortical neurons (layer V).…”

“…Layer V pyramidal neurons receive thalamic input from the main specific sensory relay the ventral posteromedial nucleus and as such are considered to function within the sensory pathway (Deschênes et al, 1994). Recently, the in vivo whole-cell patch-clamp recording technique has been applied to rat somatosensory cortical neurons (Doi et al, 2007). Recording neurons, which respond to brush or pinch stimulation of contralateral hind limb, were located between 0.5 and 1.0 mm in the depth from the brain surface (Doi et al, 2007), suggesting that these neurons are largely layer V pyramidal neurons.…”

Whisker row deprivation affects the flow of sensory information through rat barrel cortex

“…Urethane anesthesia creates a state of delta-wave activity where the EEG fluctuates at 0.5–4 Hz due to the burst-pause activity of L5 neurons, similar to the condition present in natural slow-wave sleep (Armstrong-James et al 1985; Armstrong-James and Fox 1988). The burst activity is generated partly by intracortical circuits, particularly via horizontal connections in L5 (Beltramo et al 2013; Chauvette et al 2010; Le Bon-Jego and Yuste 2007), and partly by thalamic input originating in principal and intralaminar thalamic nuclei (David et al 2013; Doi et al 2007; Fox and Armstrong-James 1986). The decrease in spontaneous activity in the L5RS cells was accompanied by a hyperpolarization in membrane potential, suggesting a decrease in excitatory drive.…”