Hyperpolarization-activated cyclic nucleotide-gated cation channels regulate auditory coincidence detection in nucleus laminaris of the chick - PubMed (original) (raw)

Hyperpolarization-activated cyclic nucleotide-gated cation channels regulate auditory coincidence detection in nucleus laminaris of the chick

Rei Yamada et al. J Neurosci. 2005.

Abstract

Coincidence detection of bilateral acoustic signals in nucleus laminaris (NL) is the first step in azimuthal sound source localization in birds. Here, we demonstrate graded expression of hyperpolarization-activated cyclic nucleotide-gated (HCN) cation channels along the tonotopic axis of NL and its role in the regulation of coincidence detection. Expression of HCN1 and HCN2, but not HCN3 or HCN4, was detected in NL. Based on measurement of both subtype mRNA and protein, HCN1 varied along the tonotopic axis and was minimal in high-characteristic frequency (CF) neurons. In contrast, HCN2 was evenly distributed. The resting conductance was larger and the steady-state activation curve of Ih was more positive in neurons of middle to low CF than those of high CF, consistent with the predominance of HCN1 channels in these neurons. Application of 8-Br-cAMP or noradrenaline generated a depolarizing shift of the Ih voltage activation curve. This shift was larger in neurons of high CF than in those of middle CF. The shift in the activation voltage of Ih depolarized the resting membrane, accelerated the EPSP time course, and significantly improved the coincidence detection in neurons of high CF, suggesting that Ih may improve the localization of sound sources.

PubMed Disclaimer

Figures

Figure 1.

Reduced expression of HCN1 mRNA in the high CF region. A, B, Expression patterns of HCN1 mRNA (A) and HCN2 mRNA (B), detected by in situ hybridization. Orientation of these subcoronal slices is indicated in E by thick dotted lines. Numbers on each slice (Aa, Ab) correspond to sectors indicated in E. M, Medial; D, dorsal. C, D, High magnification of boxes in Ab and Bb, HCN1 mRNA (C) and HCN2 mRNA (D). E, Two-dimensional projection of NL (Rubel and Parks, 1975; Kuba et al., 2005). Eleven sectors were defined depending on their rostromedial and caudolateral position within NL and were classified into three CF regions: high (black sectors, 2.5–3.3 kHz), middle (white sectors, 1–2.5 kHz), and low (gray sectors, 0.4–1 kHz).

Figure 2.

Graded expression of HCN1 channels along tonotopic axis. A, B, Subcoronal slices stained with HCN1 (A) and HCN2 (B) antibodies. Orientation of these subcoronal slices is indicated in F by dotted lines. The traces beside each panel are the relative intensity profiles of immunoreactivity in each slice (see Materials and Methods). Numbers on the abscissa indicate the sectors. M, Medial; D, dorsal. C, D, The high magnification of boxes in Ab and Bb. E, The relative immunoreactivity was measured in the neuropil and averaged for three CF regions (6 chicks). Statistical significance is indicated by **p < 0.01 in this and the following figures. F, The relationship of slices to the tonotopic region of the nucleus (see Fig. 1 E).

Figure 3.

Membrane properties in three CF neurons. A, B, Voltage responses to depolarizing and hyperpolarizing currents of 70–80 ms duration in the control (A) and after bath application of ZD7288 (0.1 m

)(B). For A–C, a, High CF neurons; b, middle CF neurons; c, low CF neurons. The injected currents are indicated in each trace. Holding potential is indicated to the left in this and the following figures. C, Voltage and current relationship measured at the end of current injection of –1.2 to 2 nA in the control (filled circles) and after application of ZD7288 (open squares) was plotted against the injected current (mean ± SE; SE was small and was masked by symbols in the control). D, E, Input resistance (D) and membrane time constant (E). Filled bars, Control; open bars, in the presence of ZD7288. Numbers in parentheses are the numbers of cells in this and subsequent figures. After application of ZD7288, input resistance and membrane time constant increased significantly in the middle CF and the low CF neurons but not in the high CF neurons. Statistical significance is indicated by *p < 0.05 in this and the following figures.

Figure 4.

EPSP time course. A, EPSPs recorded before (thinner traces) and after (thicker traces) application of ZD7288 (0.1 m

). a, High CF neuron; b, middle CF neuron; c, low CF neuron. EPSPs were recorded at –63 mV. EPSPs in the control and in ZD7288 were amplitude normalized and superimposed to facilitate comparison of the time course. EPSP amplitude was 6.3 ± 0.8 mV (control) versus 5.8 ± 0.8 mV (ZD7288, n = 9; p = 0.66) for high CF neurons, 7.8 ± 1.0 versus 6.7 ± 0.7 mV (n = 10; p = 0.38) for middle CF neurons, and 4.9 ± 0.5 versus 4.4 ± 0.4 mV (n = 15; p = 0.38) for low CF neurons. B, C, Half-amplitude width (B) and 10–90% rise time (C) of EPSP in the control (filled bars) and in ZD7288 (open bars).

Figure 5.

Comparison of _I_h among three CF neurons. A, Represent ative current traces. For A, B, and D, a, High CF neurons; b, middle CF neurons; c, low CF neurons. The pulse protocol is indicated at the bottom of Aa. The same pulse protocol was used in subsequent voltage-clamp experiments (Figs. 6, 7). The initial current and the steady-state current were measured at the times indicated by diamonds (see also D) and triangles. B, Difference between the data and the curve fits for the single (top) and double (bottom) exponential functions (see Results). The double-exponential fit gave much better results than the single-exponential fit. C, Fast (a) and slow (b) time constants of current activation and the fraction of fast component (c) were plotted against step 1 potential. For C, E, and F, Black symbols, High CF neurons; white symbols, middle CF neurons; gray symbols, low CF neurons. D, The expanded traces after step1 (a1, b1, c1) and step2 (a2, b2, c2). Amplitude of initial current was measured at the peak, indicated by dashed lines (a1, b1, c1), and averaged value was plotted in E (diamonds). Tail current amplitude (_I_tail–_I_min) was scaled between 0 and 1 and was plotted against the step 1 potential in F. Step 1 potentials are indicated at corresponding tail currents. E, I–V relationships of both in itial (diamonds) and steady-state (inverted triangles) current measured at the times indicated in A and D. SEs were small and were masked by the symbols in the high CF and the middle CF neurons. F, Voltage dependence of activation measured from the tail current. Solid lines are the Boltzmann fits to the average data. _V_h and S (see Results) were measured in each experiment and averaged (Table 1). Note that the voltage dependence was 10mV more positive in the middle CF and low CF neurons than that in the high CF neurons (p < 0.01).

Figure 6.

Modulation of _I_h by 8-Br-cAMP. A, B, Representative current traces recorded before (a) and after (b) bath application of 8-Br-cAMP (0.6 m

). Recordings were made in the same cells. A, High CF neurons; B, middle CF neurons. C, D, Fast (a) and slow (b) time constants and the fraction of the fast component (c) were plotted. For C–F, Filled symbols, Control; open symbols, 8-Br-cAMP. C, High CF neurons; D, middle CF neurons. In the middle CF neurons, the fast time constant was slightly shortened, but the slow time constant was not affected (p > 0.07). E, F, Voltage-dependent activation curves. In high CF neurons (E), _V_h = –95.5 and S = 9.8 mV for control; _V_h = –85.4 and S = 10.6 mV in 8-Br-cAMP (p < 0.01). In middle CF neurons (F), _V_h = –85.8 and S = 10.1 mV for control; _V_h = –82.6 and S = 10.0 mV in 8-Br-cAMP (p < 0.05).

Figure 7.

Modulation of _I_h by NA. A, B, Representative current traces recorded before (a) and after (b) bath application of NA (50 μ

). Recordings were made in the same cells. A, High CF neurons; B, middle CF neurons. C, D, Fast (a) and slow (b) time constants and the fraction of the fast component (c) were plotted. For C–F, Filled symbols, Control; open symbols, NA. C, High CF neurons; D, middle CF neurons. E, F, Voltage dependence of activation curves. In high CF neurons (E), _V_h =–95.7 and S = 9.8 mV for control; _V_h = –86.4 and S = 11.7 mV in NA (p < 0.01). In middle CF neurons (F), _V_h = –86.7 and S = 9.9 mV for control; _V_h = –82.3 and S = 10.4 mV in NA (p < 0.05). Note that NA mimicked the effects of 8-Br-cAMP.

Figure 8.

NA accelerates EPSP and improves the coincidence detection in high CF neurons. A, B, EPSPs were recorded before and after bath application of NA (50 μ

) in the same cells. A, High CF neurons; B, middle CF neurons. The membrane potential is indicated near the trace, and the dashed line indicates the level of resting membrane potential. C, Four superimposed voltage traces in response to bilateral stimuli at different stimulus time intervals (Δ_t_ in milliseconds, indicated in the figure). a, Before bath application of NA; b, after bath application of NA. D, Probability of spike generation as a function of Δ_t_ was calculated from six neurons. Note that the time window (arrows) was reduced after application of NA (p < 0.05).

Cited by

Cellular Strategies for Frequency-Dependent Computation of Interaural Time Difference.
Yamada R, Kuba H. Yamada R, et al. Front Synaptic Neurosci. 2022 May 6;14:891740. doi: 10.3389/fnsyn.2022.891740. eCollection 2022. Front Synaptic Neurosci. 2022. PMID: 35602551 Free PMC article. Review.
Dendritic synapse geometry optimizes binaural computation in a sound localization circuit.
Yamada R, Kuba H. Yamada R, et al. Sci Adv. 2021 Nov 26;7(48):eabh0024. doi: 10.1126/sciadv.abh0024. Epub 2021 Nov 24. Sci Adv. 2021. PMID: 34818046 Free PMC article.
High-Frequency Neuronal Bursting is Essential for Circadian and Sleep Behaviors in Drosophila.
Fernandez-Chiappe F, Frenkel L, Colque CC, Ricciuti A, Hahm B, Cerredo K, Muraro NI, Ceriani MF. Fernandez-Chiappe F, et al. J Neurosci. 2021 Jan 27;41(4):689-710. doi: 10.1523/JNEUROSCI.2322-20.2020. Epub 2020 Dec 1. J Neurosci. 2021. PMID: 33262246 Free PMC article.
Olfactory marker protein directly buffers cAMP to avoid depolarization-induced silencing of olfactory receptor neurons.
Nakashima N, Nakashima K, Taura A, Takaku-Nakashima A, Ohmori H, Takano M. Nakashima N, et al. Nat Commun. 2020 May 4;11(1):2188. doi: 10.1038/s41467-020-15917-2. Nat Commun. 2020. PMID: 32366818 Free PMC article.
Genetic coupling of signal and preference facilitates sexual isolation during rapid speciation.
Xu M, Shaw KL. Xu M, et al. Proc Biol Sci. 2019 Oct 23;286(1913):20191607. doi: 10.1098/rspb.2019.1607. Epub 2019 Oct 23. Proc Biol Sci. 2019. PMID: 31640515 Free PMC article.

References

1. Aston-Jones G, Bloom FE (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1: 876–886. - PMC - PubMed
1. Banks MI, Pearce RA, Smith PH (1993) Hyperpolarization-activated cation current (Ih) in neurons of the medial nucleus of the trapezoid body: voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. J Neuro-physiol 70: 1420–1432. - PubMed
1. Bobker DH, Williams JT (1989) Serotonin augments the cationic current Ih in central neurons. Neuron 2: 1535–1540. - PubMed
1. Chen C (2004) ZD7288 inhibits postsynaptic glutamate receptor-mediated responses at hippocampal perforant path-granule cell synapses. Eur J Neurosci 19: 643–649. - PubMed
1. Chevaleyre V, Castillo PE (2002) Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc Natl Acad Sci USA 99: 9538–9543. - PMC - PubMed

Hyperpolarization-activated cyclic nucleotide-gated cation channels regulate auditory coincidence detection in nucleus laminaris of the chick - PubMed (original) (raw)