Neural activity responsiveness by maturation of inhibition underlying critical period plasticity
IntroductionNeural circuits develop during critical periods (CPs) and exhibit heightened plasticity to adapt to the surrounding environment. Accumulating evidence indicates that the maturation of inhibitory circuits, such as gamma-aminobutyric acid and parvalbumin-positive interneurons, plays a cruc...
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Frontiers Media S.A.
2025-01-01
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| Series: | Frontiers in Neural Circuits |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncir.2024.1519704/full |
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| author | Ibuki Matsumoto Sou Nobukawa Sou Nobukawa Sou Nobukawa Sou Nobukawa Takashi Kanamaru Takashi Kanamaru Yusuke Sakemi Yusuke Sakemi Nina Sviridova Nina Sviridova Tomoki Kurikawa Nobuhiko Wagatsuma Kazuyuki Aihara Kazuyuki Aihara |
| author_facet | Ibuki Matsumoto Sou Nobukawa Sou Nobukawa Sou Nobukawa Sou Nobukawa Takashi Kanamaru Takashi Kanamaru Yusuke Sakemi Yusuke Sakemi Nina Sviridova Nina Sviridova Tomoki Kurikawa Nobuhiko Wagatsuma Kazuyuki Aihara Kazuyuki Aihara |
| author_sort | Ibuki Matsumoto |
| collection | DOAJ |
| description | IntroductionNeural circuits develop during critical periods (CPs) and exhibit heightened plasticity to adapt to the surrounding environment. Accumulating evidence indicates that the maturation of inhibitory circuits, such as gamma-aminobutyric acid and parvalbumin-positive interneurons, plays a crucial role in CPs and contributes to generating gamma oscillations. A previous theory of the CP mechanism suggested that the maturation of inhibition suppresses internally driven spontaneous activity and enables synaptic plasticity to respond to external stimuli. However, the neural response to external stimuli and neuronal oscillations at the neural population level during CPs has not yet been fully clarified. In the present study, we aimed to investigate neuronal activity responsiveness with respect to the maturation of inhibition at gamma-band frequencies.MethodWe calculated inter-trial phase coherence (ITPC), which quantifies event-related phase modulations across trials, using a biologically plausible spiking neural network that generates gamma oscillations through interactions between excitatory and inhibitory neurons.ResultsOur results demonstrated that the neuronal response coherence to external periodic inputs exhibits an inverted U-shape with respect to the maturation of inhibition. Additionally, the peak of this profile was consistent with the moderate suppression of the gamma-band spontaneous activity.DiscussionThis finding suggests that the neuronal population's highly reproducible response to increased inhibition may lead to heightened synaptic plasticity. Our computational model can help elucidate the underlying mechanisms that maximize synaptic plasticity at the neuronal population level during CPs. |
| format | Article |
| id | doaj-art-938ff55573d34f1ead628f0b3bf1a464 |
| institution | Kabale University |
| issn | 1662-5110 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neural Circuits |
| spelling | doaj-art-938ff55573d34f1ead628f0b3bf1a4642025-01-22T07:15:14ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102025-01-011810.3389/fncir.2024.15197041519704Neural activity responsiveness by maturation of inhibition underlying critical period plasticityIbuki Matsumoto0Sou Nobukawa1Sou Nobukawa2Sou Nobukawa3Sou Nobukawa4Takashi Kanamaru5Takashi Kanamaru6Yusuke Sakemi7Yusuke Sakemi8Nina Sviridova9Nina Sviridova10Tomoki Kurikawa11Nobuhiko Wagatsuma12Kazuyuki Aihara13Kazuyuki Aihara14Graduate School of Information and Computer Science, Chiba Institute of Technology, Chiba, JapanGraduate School of Information and Computer Science, Chiba Institute of Technology, Chiba, JapanDepartment of Computer Science, Chiba Institute of Technology, Chiba, JapanDepartment of Preventive Intervention for Psychiatric Disorders, National Center of Neurology and Psychiatry, Tokyo, JapanResearch Center for Mathematical Engineering, Chiba Institute of Technology, Chiba, JapanDepartment of Mechanical Science and Engineering, Kogakuin University, Tokyo, JapanInternational Research Center for Neurointelligence, The University of Tokyo, Tokyo, JapanResearch Center for Mathematical Engineering, Chiba Institute of Technology, Chiba, JapanInternational Research Center for Neurointelligence, The University of Tokyo, Tokyo, JapanInternational Research Center for Neurointelligence, The University of Tokyo, Tokyo, JapanDepartment of Intelligent Systems, Tokyo City University, Tokyo, JapanDepartment of Complex and Intelligent Systems, Future University, Hakodate, Hokkaido, JapanDepartment of Information Science, Toho University, Chiba, JapanResearch Center for Mathematical Engineering, Chiba Institute of Technology, Chiba, JapanInternational Research Center for Neurointelligence, The University of Tokyo, Tokyo, JapanIntroductionNeural circuits develop during critical periods (CPs) and exhibit heightened plasticity to adapt to the surrounding environment. Accumulating evidence indicates that the maturation of inhibitory circuits, such as gamma-aminobutyric acid and parvalbumin-positive interneurons, plays a crucial role in CPs and contributes to generating gamma oscillations. A previous theory of the CP mechanism suggested that the maturation of inhibition suppresses internally driven spontaneous activity and enables synaptic plasticity to respond to external stimuli. However, the neural response to external stimuli and neuronal oscillations at the neural population level during CPs has not yet been fully clarified. In the present study, we aimed to investigate neuronal activity responsiveness with respect to the maturation of inhibition at gamma-band frequencies.MethodWe calculated inter-trial phase coherence (ITPC), which quantifies event-related phase modulations across trials, using a biologically plausible spiking neural network that generates gamma oscillations through interactions between excitatory and inhibitory neurons.ResultsOur results demonstrated that the neuronal response coherence to external periodic inputs exhibits an inverted U-shape with respect to the maturation of inhibition. Additionally, the peak of this profile was consistent with the moderate suppression of the gamma-band spontaneous activity.DiscussionThis finding suggests that the neuronal population's highly reproducible response to increased inhibition may lead to heightened synaptic plasticity. Our computational model can help elucidate the underlying mechanisms that maximize synaptic plasticity at the neuronal population level during CPs.https://www.frontiersin.org/articles/10.3389/fncir.2024.1519704/fullcritical periodgamma-aminobutyric acidspontaneous activityinter-trial phase coherencespiking neural networksynaptic plasticity |
| spellingShingle | Ibuki Matsumoto Sou Nobukawa Sou Nobukawa Sou Nobukawa Sou Nobukawa Takashi Kanamaru Takashi Kanamaru Yusuke Sakemi Yusuke Sakemi Nina Sviridova Nina Sviridova Tomoki Kurikawa Nobuhiko Wagatsuma Kazuyuki Aihara Kazuyuki Aihara Neural activity responsiveness by maturation of inhibition underlying critical period plasticity Frontiers in Neural Circuits critical period gamma-aminobutyric acid spontaneous activity inter-trial phase coherence spiking neural network synaptic plasticity |
| title | Neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| title_full | Neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| title_fullStr | Neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| title_full_unstemmed | Neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| title_short | Neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| title_sort | neural activity responsiveness by maturation of inhibition underlying critical period plasticity |
| topic | critical period gamma-aminobutyric acid spontaneous activity inter-trial phase coherence spiking neural network synaptic plasticity |
| url | https://www.frontiersin.org/articles/10.3389/fncir.2024.1519704/full |
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