The Development of Phasic and Tonic Inhibition in the Rat Visual Cortex

Hyun-Jong Jang; Kwang-Hyun Cho; Sung-Won Park; Myung-Jun Kim; Shin Hee Yoon; Duck-Joo Rhie

doi:10.4196/kjpp.2010.14.6.399

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Jang, Cho, Park, Kim, Yoon, and Rhie: The Development of Phasic and Tonic Inhibition in the Rat Visual Cortex

Original Article

Korean J Physiol Pharmacol 2010;14(6):399-405.

Published online: 18 February 2010

DOI: https://doi.org/10.4196/kjpp.2010.14.6.399

The Development of Phasic and Tonic Inhibition in the Rat Visual Cortex

Hyun-Jong Jang¹, Kwang-Hyun Cho^1,², Sung-Won Park¹, Myung-Jun Kim¹, Shin Hee Yoon¹, Duck-Joo Rhie^1,^2,

¹Department of Physiology, College of Medicine, The Catholic University of Korea, Seoul 137-701, Korea

²Catholic Neuroscience Center, The Catholic University of Korea, Seoul 137-701, Korea

Corresponding to: Duck-Joo Rhie, Department of Physiology, College of Medicine, The Catholic University of Korea, 505, Banpo-dong, Seocho-gu, Seoul 137-701, Korea. (Tel) 82-2-2258-7277, (Fax) 82-2-532-9575, (E-mail) djrhie@catholic.ac.kr

Received 1 November 2010 Revised 8 November 2010 Accepted 9 November 2010

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Gamma-aminobutyric acid (GABA)-ergic inhibition is important in the function of the visual cortex. In a previous study, we reported a developmental increase in GABA_A receptor-mediated inhibition in the rat visual cortex from 3 to 5 weeks of age. Because this developmental increase is crucial to the regulation of the induction of long-term synaptic plasticity, in the present study we investigated in detail the postnatal development of phasic and tonic inhibition. The amplitude of phasic inhibition evoked by electrical stimulation increased during development from 3 to 8 weeks of age, and the peak time and decay kinetics of inhibitory postsynaptic potential (IPSP) and current (IPSC) slowed progressively. Since the membrane time constant decreased during this period, passive membrane properties might not be involved in the kinetic changes of IPSP and IPSC. Tonic inhibition, another mode of GABA_A receptor-mediated inhibition, also increased developmentally and reached a plateau at 5 weeks of age. These results indicate that the time course of the postnatal development of GABAergic inhibition matched well that of the functional maturation of the visual cortex. Thus, the present study provides significant insight into the roles of inhibitory development in the functional maturation of the visual cortical circuits.

Keywords: Development, GABA, Inhibition, Tonic inhibition, Visual cortex

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Fig. 1.

Developmental changes in the passive membrane properties. Passive membrane properties were measured by injection of a small negative current (–80 pA). (A) Developmental changes in input resistance. Left panel: upper trace shows the command current and lower traces show the averaged responses of membrane potential in layer 2/3 pyramidal cells at 3- (‘3 weeks,’ dashed line), 5- (‘5 weeks,’ thin solid line), and 8-week-old rats (‘8 weeks,’ thick solid line). The right panel plots individual data (symbols) and averages (thick solid lines). IR: input resistance. (B) Developmental changes in membrane time constant. Left panel: upper trace shows the command current and lower traces show normalized responses of membrane potential in layer 2/3 pyramidal cells. The right panel plots individual data (symbols) and averages (thick solid lines). τ_memb: membrane time constant. ^∗p<0.05, and ^∗∗∗p<0.001 between groups linked by lines.

Fig. 2.

Development of phasic inhibition. Inhibitory postsynaptic potential (IPSP) and inhibitory postsynaptic current (IPSC) were recorded at 0 mV of membrane potential in the presence of DNQX (20 μM) and D-AP5 (50 μM) at stimulation intensities that evoked 20 mV depolarization at –75 mV membrane potential. (A) Averaged IPSPs (left traces) and IPSCs (right traces) showing differences between groups. IPSPs and IPSCs were recorded from slices of 3-(‘3 weeks,’ thin dashed lines), 5- (‘5 weeks,’ thin solid lines), 8- (‘8 weeks,’ thick solid lines), and 12-week-old rats (‘12 weeks,’ thick dashed lines). (B) Individual data (symbols) and averages (thick lines) for excitatory postsynaptic potential (EPSP), excitatory post-synaptic current (EPSC), IPSP, and IPSC for each of the groups indicated in the lower panels. ^∗p<0.05 between groups linked by lines.

Fig. 3.

Developmental changes in the kinetics of phasic inhibition. (A) Peak time of IPSP (left panel) and IPSC (right panel). Upper traces show normalized IPSPs and IPSCs of 3- (‘3 weeks,’ dashed line), 5- (‘5 weeks,’ thin solid line), and 8-week-old rats (‘8 weeks,’ thick solid line) with an extended time scale. Lower panels plot individual data (symbols) and averages (thick lines) for the peak time of IPSPs and IPSCs. (B) Decay time constant of IPSP (left panel) and IPSC (right panel). Upper traces show normalized IPSPs and IPSCs of 3- (dashed line), 5- (thin solid line), and 8-week-old rats (thick solid line). Lower panels plot individual data (symbols) and averages (thick lines) for the decay time constant of IPSPs and IPSCs. τ_decay: decay time constant. ^∗p<0.05, ^∗∗p<0.01, and ^∗∗∗p<0.001 between groups linked by lines.

Fig. 4.

Developmental changes in the kinetics of excitation. (A) Peak time of EPSP (left panel) and EPSC (right panel). Upper traces show normalized EPSPs and EPSCs of 3- (‘3 weeks,’ dashed line), 5- (‘5 weeks,’ thin solid line), and 8-week-old rats (‘8 weeks,’ thick solid line) with extended time scale. Lower panels plot individual data (symbols) and averages (thick lines) for the peak time of EPSPs and EPSCs. (B) Decay time constant of EPSP (left panel) and EPSC (right panel). Upper traces show normalized EPSPs and EPSCs of 3- (dashed line), 5- (thin solid line), and 8-week-old rats (thick solid line). Lower panels plot individual data (symbols) and averages (thick lines) for the decay time constant of EPSPs and EPSCs. τ_decay: decay time constant. ^∗∗p<0.01, and ^∗∗∗p<0.001 between groups linked by lines.

Fig. 5.

Developmental changes in tonic inhibition. Tonic inhibition was measured as the difference between the holding current before and after the application of the GABA_A receptor antagonist bicuculline (10 μM) while membrane potential was clamped at –75 mV. (A) Current traces at the holding potential of –75 mV before and after the application of bicuculline for 3- (top trace), 5- (middle trace), and 8-week-old rats (bottom trace). White solid lines indicate periods at which holding currents were measured. Grey dashed lines indicate holding currents measured before the application of bicuculline. (B) Individual data (symbols) and averages (thick lines) of the changes in holding currents for 3- (‘3 weeks’), 5- (‘5 weeks’), and 8-week-old rats (‘8 weeks’). ^∗∗∗p<0.001 vs. ‘3 weeks’.

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