A Critical Role of Inhibition in Temporal Processing Maturation in the Primary Auditory Cortex.
Faithful representation of sound envelopes in primary auditory cortex (A1) is vital for temporal processing and perception of natural sounds. However, the emergence of cortical temporal processing mechanisms during development remains poorly understood. Although cortical inhibition has been proposed to play an important role in this process, direct in-vivo evidence has been lacking. Using loose-patch recordings in rat A1 immediately after hearing onset, we found that stimulus-following ability in fast-spiking neurons was significantly better than in regular-spiking (RS) neurons. In-vivo whole-cell recordings of RS neurons revealed that inhibition in the developing A1 demonstrated much weaker adaptation to repetitive stimuli than in adult A1. Furthermore, inhibitory synaptic inputs were of longer duration than observed in vitro and in adults. Early in development, overlap of the prolonged inhibition evoked by 2 closely following stimuli disrupted the classical temporal sequence between excitation and inhibition, resulting in slower following capacity. During maturation, inhibitory duration gradually shortened accompanied by an improving temporal following ability of RS neurons. Both inhibitory duration and stimulus-following ability demonstrated exposure-based plasticity. These results demonstrate the role of inhibition in setting the pace for experience-dependent maturation of temporal processing in the auditory cortex.
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Dongqin
D
Cai
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.|Department of Otolaryngology, Weifang People's Hospital, Weifang, Shandong 261000, China.
Rongrong
R
Han
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Miaomiao
M
Liu
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Fenghua
F
Xie
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Ling
L
You
State Key Laboratory of Biomembrane and Membrane Biotechnology, Tsinghua-Peking Joint Center for Life Sciences, School of Life Sciences, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Yi
Y
Zheng
Department of Otolaryngology, Affiliated Hospital of Weifang Medical University, Weifang, Shandong 261031, China.
Limin
L
Zhao
State Key Laboratory of Biomembrane and Membrane Biotechnology, Tsinghua-Peking Joint Center for Life Sciences, School of Life Sciences, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Jun
J
Yao
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Yiwei
Y
Wang
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Tsinghua University, Beijing 100084, China.
Yin
Y
Yue
Department of Otolaryngology, Kavli Center for Fundamental Neuroscience, University of California at San Francisco, California, MA 94158, USA.
Christoph E
CE
Schreiner
Department of Biomedical Engineering, School of Medicine, IDG/McGovern Institute for Brain Research, Center for Brain-Inspired Computing Research, Tsinghua University, Beijing 100084, China.
Kexin
K
Yuan
D000161:Acoustic Stimulation; D000200:Action Potentials / Q000502:physiology*; D000367:Age Factors; D000818:Animals; D000831:Animals, Newborn; D001303:Auditory Cortex / Q000166:cytology* / Q000254:growth & development*; D017097:Electric Impedance; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000145:classification / Q000502:physiology*; D018408:Patch-Clamp Techniques; D051381:Rats; D017207:Rats, Sprague-Dawley; D013997:Time Factors