Elsevier

Brain Research

Volume 1752, 1 February 2021, 147258
Brain Research

Intrinsic properties of avian interaural level difference sound localizing neurons

https://doi.org/10.1016/j.brainres.2020.147258Get rights and content

Highlights

  • LLDp neurons are heterogeneous in their intrinsic firing patterns.

  • Tonic regular firing neurons dominate.

  • Neurons with different firing patterns are about evenly distributed in LLDp.

  • Action potentials differ in their parameters among different firing patterns.

  • Phasic and tonic firing neurons may assume different functions in LLDp.

Abstract

Intrinsic properties of neurons are one major determinant for how neurons respond to their synaptic inputs and shape their outputs in neural circuits. Here, we studied the intrinsic properties of neurons in the chicken posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp), the first interaural level difference (ILD) encoder of the avian auditory pathway. Using whole-cell recordings in brain slices, we revealed that the LLDp is composed of a heterogeneous neuron population based on their firing patterns. LLDp neurons were broadly classified as either phasic or tonic firing neurons, with further classification applied to tonic firing neurons, such as regular (most dominant, n = 82 out of 125 cells, 65.6%), pauser, or adaptive firing. Neurons with different firing patterns were distributed about evenly across the dorsoventral as well as mediolateral axis of LLDp. Phasic firing neurons were of faster membrane time constant, and lower excitability than tonic firing neurons. The action potentials (APs) elicited at the current thresholds displayed significant differences in first spike latency, AP peak amplitude, half-width, and maximal rising and falling rates. Interestingly, for APs elicited at suprathreshold currents (400 pA above thresholds), some of the differences diminished while a few others emerged. Remarkably, most parameters of the APs at thresholds were significantly different from those of APs at suprathresholds. Combined with our previous study (Curry and Lu, 2016), the results lend support to the two-cell type model for ILD coding in the avian system.

Introduction

Computation of sound localization information using interaural level difference (ILD) as a cue in mammals takes place first in the lateral superior olive (LSO). In birds, the first nucleus that encodes ILD is the posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp, formerly known as VLVp, the nucleus ventralis lemnisci lateralis pars posterior) (Mogdans and Knudsen, 1994). LLDp neurons receive excitatory input from the contralateral cochlear nucleus angularis (NA) (Conlee and Parks, 1986, Takahashi and Konishi, 1988), and receive inhibitory input primarily from the other LLDp, which is driven by excitatory input originating from the ipsilateral NA (Manley et al., 1988, Takahashi and Keller, 1992). A number of in vivo studies have demonstrated the roles of LLDp neurons in ILD processing (Adolphs, 1993, Sato et al., 2010, Takahashi and Keller, 1992). Our previous study has reported the mechanisms of synaptic inhibition underlying ILD coding in the LLDp, and proposed a two-cell type model (Curry and Lu, 2016). However, the report on the intrinsic properties of LLDp neurons is lacking, impeding our understanding of how these ILD coding neurons may respond to their synaptic inputs in ILD processing.

Knowledge of the mammalian system provides insight to potential strategies in the construction of intrinsic properties that may be favorable for ILD processing. For example, the principal ILD encoding LSO neurons exhibit a highly regular firing pattern in vivo (Tsuchitani, 1982; but also see Franken et al., 2018) and a tonic firing pattern in response to prolonged depolarizing current injections in vitro (Adam et al., 1999, Wu and Kelly, 1995), allowing for modulation of spike firing rate to represent the interaction of synaptic excitation and inhibition. This differs from the intrinsic properties of the neurons in the medial nucleus of trapezoid body (MNTB), which exhibit a characteristic single action potential (AP) in response to sustained depolarization, and maintain high temporal fidelity (Banks and Smith, 1992, Dodson et al., 2002, Klug and Trussell, 2006). Consequently, the MNTB provides fast and temporally precise and reliable inhibition to various binaural neurons including those in the LSO (reviewed by Grothe, 2003, Grothe et al., 2010). Based on the known circuitry, neurons in the LLDp on one side need to perform the tasks that are performed by both LSO in order to encode ILDs (Mogdans and Knudsen, 1994) and MNTB in order to provide direct inhibitory input to the LLDp on the other side of the brain (Curry and Lu, 2016, Takahashi and Keller, 1992). These two tasks are unlikely to be performed by the same population of cells displaying similar neuronal properties. Therefore, we hypothesized that LLDp neurons are heterogeneous in intrinsic properties, such that one population would exhibit a highly regular firing pattern, like principle LSO neurons, which could encode increases in sound levels by an increase in firing frequency, and another population would exhibit a precise phasic firing pattern, like MNTB neurons, which could provide temporally modulated inhibition to the opposite LLDp. To test this hypothesis, we investigated the intrinsic properties of LLDp neurons using whole-cell patch clamp to compare the passive properties (e.g. input resistance and membrane time constant) and active properties (e.g. AP parameters) to determine if LLDp neurons could be categorized into distinct cell-types that may relate to specific circuit function.

Section snippets

Results

In acutely obtained coronal brainstem slices, the LLD was recognized as a heavily myelinated ovoid region medial and ventral to the semilunar nucleus, a landmark structure with distinct shape and contrast (Fig. 1A). After biocytin staining processing, both the LLD and the semilunar nucleus showed distinct borders (Fig. 1B), clearly separated from surrounding tissue. The border of the LLDp was distinguished by a medial lamina, such that cells were sampled from the lateral portion of the LLD,

Heterogeneous LLDp neurons based on spike firing patterns

The results of this study reveal that the LLDp is composed of a heterogeneous neuronal population, which may allow for a segregation of ILD processing functions among distinct cell types. The majority of LLDp neurons display a tonic regular firing pattern (T1), however, there is evidence for different firing patterns, including phasic and tonic irregular firing types. Based on the sampled neurons, there does not appear to be a distinct spatial segregation of firing types in the LLDp, such that

Animals

All animal procedures were approved by the Institutional Animal Care and Use Committee at the Northeast Ohio Medical University (NEOMED) and were performed in accordance with the National Institutes of Health policies on animal use. Fertilized white leghorn chicken eggs were purchased from Charles River and incubated in our laboratory at NEOMED.

Slice preparation and in vitro whole-cell recordings

Brainstem slices (300 μm in thickness) were prepared from white leghorn chick embryos (E17–E19), as described previously (Curry and Lu, 2016). While the

Author Contributions

Y.L. conceived the study; R.C. and Y.L. designed research; R.C. and Y.L. performed experiments and analyzed data; R.C. and Y.L. wrote the paper.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank Dr. Yuan Wang for advice in identifying the LLDp, and Lin Cai for data analysis and editorial assistance. This work was supported by National Institute on Deafness and other Communication Disorders Grants F31DC015707 (R.C.) and R01DC016054 (Y.L.).

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    Current address: Charles River, Ashland, OH 44805, USA.

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