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Modulation of neuronal activity in cortical organoids with bioelectronic delivery of ions and neurotransmitters.

ABSTRACT: Precise modulation of brain activity is fundamental for the proper establishment and maturation of the cerebral cortex. To this end, cortical organoids are promising tools to study circuit formation and the underpinnings of neurodevelopmental disease. However, the ability to manipulate neuronal activity with high temporal resolution in brain organoids remains limited. To overcome this challenge, we introduce a bioelectronic approach to control cortical organoid activity with the selective delivery of ions and neurotransmitters. Using this approach, we sequentially increased and decreased neuronal activity in brain organoids with the bioelectronic delivery of potassium ions (K⁺) and γ-aminobutyric acid (GABA), respectively, while simultaneously monitoring network activity. This works highlights bioelectronic ion pumps as tools for high-resolution temporal control of brain organoid activity toward precise pharmacological studies that can improve our understanding of neuronal function.

SUBMITTER: Park Y

PROVIDER: S-EPMC10831944 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Modulation of neuronal activity in cortical organoids with bioelectronic delivery of ions and neurotransmitters.

Park Yunjeong Y Hernandez Sebastian S Hernandez Cristian O CO Schweiger Hunter E HE Li Houpu H Voitiuk Kateryna K Dechiraju Harika H Hawthorne Nico N Muzzy Elana M EM Selberg John A JA Sullivan Frederika N FN Urcuyo Roberto R Salama Sofie R SR Aslankoohi Elham E Knight Heather J HJ Teodorescu Mircea M Mostajo-Radji Mohammed A MA Rolandi Marco M

Cell reports methods 20240112 1

Precise modulation of brain activity is fundamental for the proper establishment and maturation of the cerebral cortex. To this end, cortical organoids are promising tools to study circuit formation and the underpinnings of neurodevelopmental disease. However, the ability to manipulate neuronal activity with high temporal resolution in brain organoids remains limited. To overcome this challenge, we introduce a bioelectronic approach to control cortical organoid activity with the selective delive ...[more]

PMID: 38218190

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Project description:Cortical areas have the capacity of large-scale reorganization following sensory deafferentation. However, it remains unclear whether this phenomenon is a unique process that homogeneously affects the entire deprived cortical region or whether it is susceptible to changes depending on neuronal networks across distinct cortical layers. Here, we studied how the local circuitry within each layer of the deafferented cortex forms the basis for neuroplastic changes after immediate thoracic spinal cord injury (SCI) in anaesthetized rats. In vivo electrophysiological recordings from deafferented hindlimb somatosensory cortex showed that SCI induces layer-specific changes mediating evoked and spontaneous activity. In supragranular layer 2/3, SCI increased gamma oscillations and the ability of these neurons to initiate up-states during spontaneous activity, suggesting an altered corticocortical network and/or intrinsic properties that may serve to maintain the excitability of the cortical column after deafferentation. On the other hand, SCI enhanced the infragranular layers' ability to integrate evoked sensory inputs leading to increased and faster neuronal responses. Delayed evoked response onsets were also observed in layer 5/6, suggesting alterations in thalamocortical connectivity. Altogether, our data indicate that SCI immediately modifies the local circuitry within the deafferented cortex allowing supragranular layers to better integrate spontaneous corticocortical information, thus modifying column excitability, and infragranular layers to better integrate evoked sensory inputs to preserve subcortical outputs. These layer-specific neuronal changes may guide the long-term alterations in neuronal excitability and plasticity associated with the rearrangements of somatosensory networks and the appearance of central sensory pathologies usually associated with spinal cord injury. KEY POINTS: Sensory stimulation of forelimb produces cortical evoked responses in the somatosensory hindlimb cortex in a layer-dependent manner. Spinal cord injury favours the input statistics of corticocortical connections between intact and deafferented cortices. After spinal cord injury supragranular layers exhibit better integration of spontaneous corticocortical information while infragranular layers exhibit better integration of evoked sensory stimulation. Cortical reorganization is a layer-specific phenomenon.

Dataset Information

Modulation of neuronal activity in cortical organoids with bioelectronic delivery of ions and neurotransmitters.

Publications

Modulation of neuronal activity in cortical organoids with bioelectronic delivery of ions and neurotransmitters.

Similar Datasets

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