Clin Exp Otorhinolaryngol.  2019 Aug;12(3):279-286. 10.21053/ceo.2018.01431.

Abrupt Change in Electrophysiological Properties Begins From Postnatal Day 7 Before Hearing Onset in the Developing Mice Auditory Cortical Layer II/III Neurons

Affiliations
  • 1Department of Physiology, Dankook University College of Medicine, Cheonan, Korea. ansil67@hanmail.net

Abstract


OBJECTIVES
In the developing auditory cortex, maturation of electrophysiological properties and cell types before and after hearing onset has been reported previously. However, the exact timing of firing pattern change has not been reported. In this study, firing pattern change was investigated from postnatal day 3 (P3) to P12 in auditory cortical layer II/III neurons to investigate whether firing pattern changes dramatically after a specific point during development.
METHODS
ICR mice pups aged from P3 to P12 were sacrificed to obtain 300-mm-thick brain slices containing the primary auditory cortex. From cortical layer II/III neurons, the patterns of action potential firing generated by current injection were examined using whole cell current clamp technique and the characteristics of Na⁺ currents involved in action potential firing were investigated using whole cell voltage clamp technique.
RESULTS
From P3 to P6, most cells did not show action potential firing (29 of 46 cells), and some cells responding to current injection showed a single action potential at the initial depolarizing current step (17 of 46 cells). This firing pattern changes from P7. From P7 to P9, cells begin to show regular spiking to current injection. The spiking frequency increased after P10. In studying Na⁺ current with whole cell voltage clamp, Na⁺ current densities increased gradually (32.0±2.0 pA/pF [P3-P6, n=7], 51.2±2.0 pA/pF [P7-P9, n=13], and 69.5±3.7 pA/pF [P10-P12, n=13]) in low external [Na⁺] condition. Na⁺ current recovery was accelerated and inactivation curves shifted to hyperpolarization with age.
CONCLUSION
As regular spiking cells were observed from P7 but never from P3 to P6, P7 might be regarded as an important milestone in the development of auditory cortical layer II/III neurons. This change might mainly result from the increase in Na⁺ current density.

Keyword

ICR Mice; Auditory Cortex; Action Potential

MeSH Terms

Action Potentials
Animals
Auditory Cortex
Brain
Fires
Hearing*
Mice*
Mice, Inbred ICR
Neurons*

Figure

  • Fig. 1. Intrinsic neuronal properties from P4 (A), P8 (B), and P11 (C) mice. The current protocol is shown above figures. Filled squares below figures (A-C) indicate voltage measuring points for the current-voltage relationship in (D-F). Current-voltage relations in neurons of different ages are shown in (D-F: P3–P6 [D], P7–P9 [E], P10–P12 [F]). Fitting lines obtained from linear regression are drawn over the mean values. A graph of input resistances against age is shown in (G). Asterisks over columns indicate the statistical significance. (H) The relation between the number of spikes and injected currents is shown. (I) A graph of resting membrane potential against age is shown. P, postnatal day.

  • Fig. 2. Na+ currents recorded from neurons of different ages. The current protocol is shown above figures. In (A-C), the external [Na+] was reduced from 150 mM to 88 mM. Na+ currents recorded when [Na+] was 150 mM are shown in (D). Asterisks shown in figures indicate delayed response due to space clamp error. Current-voltage relations recorded in the low [Na+] condition are shown in (E). The peak current densities obtained from (E) are shown in (F). P, postnatal day; aCSF, artificial cerebrospinal fluid.

  • Fig. 3. Inactivation of Na+ currents from neurons of different ages. Inset: Na+ currents in a P5 neuron. The voltage protocol is shown above the inset. (A) The fraction of peak currents (I/Imax) is plotted against the inactivation voltage. The smooth curve is the best fit to a modified first order Boltzmann equation. Half inactivation voltages obtained from (A) are shown in (B). Asterisks over columns indicate the statistical significance. P, postnatal day.

  • Fig. 4. Na+ current recovery from inactivation. The first Na+ current was elicited by step depolarization from –71.2 to –31.2 mV. After a 10-millisecond initial interval, 1 millisecond was added to each interval. A total of 25 sweeps were performed (A–C). The relative current (I/Imax) plotted as a function of interpulse interval was shown in (D), where a single exponential function was fitted to the data. (E) The time constants were 4.7±0.5 (P3–P6, n=13), 2.8±0.2 (P7–P9, n=3), and 2.3±0.1 (P10–P12, n=21). Asterisks over columns indicate the statistical significance. P, postnatal day.


Reference

1. Ehret G. Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc. 1976; Mar-Apr. 1(5):179–84.
2. Chang EF, Merzenich MM. Environmental noise retards auditory cortical development. Science. 2003; Apr. 300(5618):498–502.
Article
3. de Villers-Sidani E, Chang EF, Bao S, Merzenich MM. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J Neurosci. 2007; Jan. 27(1):180–9.
Article
4. Iwasa H, Potsic WP. Maturational change of early, middle, and late components of the auditory evoked responses in rats. Otolaryngol Head Neck Surg. 1982; Jan-Feb. 90(1):95–102.
Article
5. Mourek J, Himwich WA, Myslivecek J, Callison DA. The role of nutrition in the development of evoked cortical responses in rat. Brain Res. 1967; Oct. 6(2):241–51.
Article
6. Wise SP, Jones EG. Developmental studies of thalamocortical and commissural connections in the rat somatic sensory cortex. J Comp Neurol. 1978; Mar. 178(2):187–208.
Article
7. Gillespie DC, Kim G, Kandler K. Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci. 2005; Mar. 8(3):332–8.
Article
8. Kim G, Kandler K. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci. 2003; Mar. 6(3):282–90.
Article
9. Kungel M, Friauf E. Physiology and pharmacology of native glycine receptors in developing rat auditory brainstem neurons. Brain Res Dev Brain Res. 1997; Sep. 102(2):157–65.
Article
10. Lohrke S, Srinivasan G, Oberhofer M, Doncheva E, Friauf E. Shift from depolarizing to hyperpolarizing glycine action occurs at different perinatal ages in superior olivary complex nuclei. Eur J Neurosci. 2005; Dec. 22(11):2708–22.
11. Friauf E, Kandler K. Auditory projections to the inferior colliculus of the rat are present by birth. Neurosci Lett. 1990; Nov. 120(1):58–61.
Article
12. Phillips DP, Orman SS, Musicant AD, Wilson GF. Neurons in the cat’s primary auditory cortex distinguished by their responses to tones and wide-spectrum noise. Hear Res. 1985; Apr. 18(1):73–86.
Article
13. Pfeiffer RR. Classification of response patterns of spike discharges for units in the cochlear nucleus: tone-burst stimulation. Exp Brain Res. 1966; 1(3):220–35.
Article
14. Creutzfeldt O, Hellweg FC, Schreiner C. Thalamocortical transformation of responses to complex auditory stimuli. Exp Brain Res. 1980; 39(1):87–104.
Article
15. Metherate R, Aramakis VB. Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res Dev Brain Res. 1999; Jun. 115(2):131–44.
Article
16. Oswald AM, Reyes AD. Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J Neurophysiol. 2008; Jun. 99(6):2998–3008.
Article
17. Ryugo DK, Killackey HP. Differential telencephalic projections of the medial and ventral divisions of the medial geniculate body of the rat. Brain Res. 1974; Dec. 82(1):173–7.
Article
18. Cruikshank SJ, Rose HJ, Metherate R. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol. 2002; Jan. 87(1):361–84.
Article
19. Burgard EC, Hablitz JJ. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J Neurophysiol. 1993; Jan. 69(1):230–40.
Article
20. Ramoa AS, McCormick DA. Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections. J Neurosci. 1994; Apr. 14(4):2089–97.
Article
21. Zhou FM, Hablitz JJ. Postnatal development of membrane properties of layer I neurons in rat neocortex. J Neurosci. 1996; Feb. 16(3):1131–9.
Article
22. Huguenard JR, Hamill OP, Prince DA. Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol. 1988; Mar. 59(3):778–95.
Article
23. McCormick DA, Prince DA. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol. 1987; Dec. 393:743–62.
Article
24. Cummins TR, Xia Y, Haddad GG. Functional properties of rat and human neocortical voltage-sensitive sodium currents. J Neurophysiol. 1994; Mar. 71(3):1052–64.
Article
25. Carrascal L, Nieto-Gonzalez JL, Cameron WE, Torres B, Nunez-Abades PA. Changes during the postnatal development in physiological and anatomical characteristics of rat motoneurons studied in vitro. Brain Res Brain Res Rev. 2005; Sep. 49(2):377–87.
Article
26. Matzner O, Devor M. Na+ conductance and the threshold for repetitive neuronal firing. Brain Res. 1992; Nov. 597(1):92–8.
Article
27. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE. The origin of spontaneous activity in the developing auditory system. Nature. 2007; Nov. 450(7166):50–5.
Article
28. Clause A, Kim G, Sonntag M, Weisz CJ, Vetter DE, Rubsamen R, et al. The precise temporal pattern of prehearing spontaneous activity is necessary for tonotopic map refinement. Neuron. 2014; May. 82(4):822–35.
Article
Full Text Links
  • CEO
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr