Gamma Band Unit Activity and Population Responses in the Pedunculopontine Nucleus

Abstract

The pedunculopontine nucleus (PPN) is involved in the activated states of waking and paradoxical sleep, forming part of the reticular activating system (RAS). The studies described tested the hypothesis that single unit and/or population responses of PPN neurons are capable of generating gamma band frequency activity. Whole cell patch clamp recordings (immersion chamber) and population responses (interface chamber) were conducted on 9- to 20-day-old rat brain stem slices. Regardless of cell type (I, II, or III) or type of response to the nonselective cholinergic receptor agonist carbachol (excitation, inhibition, biphasic), almost all PPN neurons fired at gamma band frequency, but no higher, when subjected to depolarizing steps (50 +/- 2 Hz, mean +/- SE). Nonaccommodating neurons fired at 18-100 Hz throughout depolarizing steps, while most accommodating neurons exhibited gamma band frequency of action potentials followed by gamma band membrane oscillations. These oscillations were blocked by the sodium channel blocker tetrodotoxin (TTX), suggesting that at least some are mediated by sodium currents. Population responses in the PPN showed that carbachol induced peaks of activation in the theta and gamma range, while glutamatergic receptor agonists induced overall increases in activity at theta and gamma frequencies, although in differing patterns. Gamma band activity appears to be a part of the intrinsic membrane properties of PPN neurons, and the population as a whole generates different patterns of gamma band activity under the influence of specific transmitters. Given sufficient excitation, the PPN may impart gamma band activation on its targets.

Cholinergic and glutamatergic agonists induce gamma frequency activity in dorsal subcoeruleus nucleus neurons

“…On the other hand, pyramidal cells in mouse neocortex plateaued below gamma frequency (45). In the PPN, all neurons plateaued at gamma frequency and had gamma frequency membrane oscillations (34) due to the presence of P/Q-type calcium channels (22).…”

“…Further analysis was conducted using MatLab software (The MathWorks, Natick, MA). Plots of the eventrelated spectral perturbation (ERSP) for each population response were generated with the EEGLAB MatLab Toolbox (14), as has been described previously (34).…”

Modulation of gamma oscillations in the pedunculopontine nucleus by neuronal calcium sensor protein-1: relevance to schizophrenia and bipolar disorder

“…The neurons were localized in the pars compacta in the posterior PPN, which is easily identified in sagittal sections of the brainstem (Kezunovic et al 2011;Simon et al 2010). The recording region was located mainly in the pars compacta in the posterior PPN, immediately dorsal to the superior cerebellar peduncle.…”

“…Within a short time after rupturing the membrane, the intracellular solution reached equilibrium with the pipette solution without significant changes in either series resistance (ranging 5-12 M⍀) or membrane capacitance values. We first identified PPN neurons by cell type as previously described (Garcia-Rill et al 2007Simon et al 2010). PPN cell type I PPN neurons (LTS current), type II PPN cells (Ia current), and type III PPN neurons (LTS ϩ Ia currents) were identified as previously described (Kezunovic et al 2011.…”

“…Gamma activity in the motor cortex lags behind coherent activity in subcortical structures (Lalo et al 2008;Litvak et al 2012), suggesting that gamma synchronization reflects an arousal-related event for enabling initiation of movement (Brucke et al 2012;Cheyne and Ferrari 2013;Jenkinson et al 2013). In addition, we showed that every cell in the reticular activating system (RAS), especially the pedunculopontine nucleus (PPN), plateaus at gamma frequencies (Kezunovic et al 2011;Simon et al 2010;Urbano et al 2012). We made similar observations in the intralaminar thalamus (ILT), specifically the parafascicular nucleus (Pf), which relays PPN activity to the cortex .…”