Control of Phasic Firing by a Background Leak Current in Avian Forebrain Auditory Neurons.

André A Dagostin,Claudio V Mello,Peter V Lovell,Ricardo M Leão,Markus M Hilscher

doi:10.3389/fncel.2015.00471

Abstract

Central neurons express a variety of neuronal types and ion channels that promote firing heterogeneity among their distinct neuronal populations. Action potential (AP) phasic firing, produced by low-threshold voltage-activated potassium currents (VAKCs), is commonly observed in mammalian brainstem neurons involved in the processing of temporal properties of the acoustic information. The avian caudomedial nidopallium (NCM) is an auditory area analogous to portions of the mammalian auditory cortex that is involved in the perceptual discrimination and memorization of birdsong and shows complex responses to auditory stimuli We performed in vitro whole-cell patch-clamp recordings in brain slices from adult zebra finches (Taeniopygia guttata) and observed that half of NCM neurons fire APs phasically in response to membrane depolarizations, while the rest fire transiently or tonically. Phasic neurons fired APs faster and with more temporal precision than tonic and transient neurons. These neurons had similar membrane resting potentials, but phasic neurons had lower membrane input resistance and time constant. Surprisingly phasic neurons did not express low-threshold VAKCs, which curtailed firing in phasic mammalian brainstem neurons, having similar VAKCs to other NCM neurons. The phasic firing was determined not by VAKCs, but by the potassium background leak conductances, which was more prominently expressed in phasic neurons, a result corroborated by pharmacological, dynamic-clamp, and modeling experiments. These results reveal a new role for leak currents in generating firing diversity in central neurons.

Highlights

The brain possesses an astonishing diversity of neuronal cells with firing properties that are adapted for the roles they play in different aspects of computational processing
Phasic firing is controlled by the expression of Kv1 low-voltage-activated potassium currents (VAKCs; Manis and Marx, 1991; Brew and Forsythe, 1995; Dodson et al, 2002; Svirskis et al, 2002; Fukui and Ohmori, 2003), while Kv3 high-threshold activated potassium currents are important for shortening the Action potential (AP) and high-frequency firing (Fukui and Ohmori, 2003; Macica et al, 2003)
Electrophysiological recordings in current clamp mode, from randomly selected NCM neurons (162 neurons from 87 birds), revealed three distinct classes of neurons that could be classified based on their patterns of AP firing elicited by square pulses of depolarizing current (Figure 1)

Summary

Introduction

The brain possesses an astonishing diversity of neuronal cells with firing properties that are adapted for the roles they play in different aspects of computational processing. The mammalian cerebral cortex contains distinct classes of GABAergic interneurons that exhibit firing patterns ranging from fast spiking to slow adapting, to intrinsic burst firing. Such characteristic electrophysiological features are thought to be adaptations for the computational. Heterogeneity in firing properties can be correlated with specific combinations of ion channels whose regulated expression varies considerably across neuronal populations (Llinas, 1998). Voltage-activated potassium channels, including both inactivating and delayed rectifier types, have received considerable attention for the roles they play in determining the neuronal excitability and firing patterns (Llinas, 1998; Dodson and Forsythe, 2004). Subthreshold conductances, like potassium inwardly rectifiers (IKir) and hyperpolarization activated cation channels (Ih), and background (“leak”) conductances are generally thought to be mainly associated with the regulation of passive membrane properties and resting membrane potential (RMP; Day et al, 2005; Biel et al, 2009; Enyedi and Czirják, 2010; Hibino et al, 2010; Leao et al, 2012), and have received less attention with respect to cellular firing properties

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