Resonance properties of different neuronal populations in the immature mouse neocortex

Abstract

In vivo recordings in the immature neocortex revealed spontaneous and sensory‐driven oscillatory activity from delta (0.5–4 Hz) to gamma (30–100 Hz) frequencies. In order to investigate whether the resonance properties of distinct neuronal populations in the immature neocortex contribute to these network oscillations, we performed whole‐cell patch‐clamp recordings from visually identified neurons in tangential and coronal neocortical slices from postnatal day (P)0–P7 C57Bl/6 mice. Subthreshold resonance was analysed by sinusoidal current injection of varying frequency. All Cajal–Retzius cells showed subthreshold resonance, with an average frequency of 2.6 ± 0.1 Hz (n = 60), which was massively reduced by ZD7288, a blocker of hyperpolarization‐activated cation currents. Approximately 65.6% (n = 61) of the supragranular pyramidal neurons showed subthreshold resonance, with an average frequency of 1.4 ± 0.1 Hz (n = 40). Application of Ni2+ suppressed subthreshold resonance, suggesting that low‐threshold calcium currents contribute to resonance in these neurons. Approximately 63.6% (n = 77) of the layer V pyramidal neurons showed subthreshold resonance, with an average frequency of 1.4 ± 0.2 Hz (n = 49), which was abolished by ZD7288. Only 44.1% (n = 59) of the subplate neurons showed subthreshold resonance, with an average frequency of 1.3 ± 0.2 Hz (n = 26) and a small resonance strength. In summary, these results demonstrate that neurons in all investigated layers show resonance behavior, with either hyperpolarization‐activated cation or low‐threshold calcium currents contributing to the subthreshold resonance. The observed resonance frequencies are in the range of slow activity patterns observed in the immature neocortex, suggesting that subthreshold resonance may support the generation of this activity.

Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration

“…This could be due to resonance phenomena in cortical principal neurons, which have been shown to possess a preferred subthreshold frequency close to 1.6 Hz (ref. 21). …”

HCN1 subunits contribute to the kinetics of Ih in neonatal cortical plate neurons

“…Small changes in current properties of HCN channels in neuronal networks, including current kinetics, have macroscopic consequences due to interactions with other currents in complex systems (Tsay et al, ; George et al, ). This might be developmentally relevant, for example, for intrinsic resonance properties—to which I h considerably contributes (at P0‐2 in layer I cortical neurons (Sun et al, ))—or for the coupling between excitatory postsynaptic potentials and action potentials in young neurons (Chen et al, ; Ouardouz et al, ). In summary, a functional role for HCN1 subunits at P0 seems more likely than their presence as a mere concomitant effect.…”

Ionic Basis for Membrane Potential Resonance in Neurons of the Inferior Olive

“…Therefore, we pharmacologically examined other possible candidates. We focused on HCN channels, because they play a crucial role in resonance in some neurons (Hu et al, 2002;Sun et al, 2012;Ulrich, 2014;Zemankovics et al, 2010). In the presence of 20 mM ZD7288, a blocker of HCN channels, impedance declined with the frequency of input currents in Cav3.1 KO mice at all tested membrane potentials ( Figures 3A, 3C, and 3G).…”