Corticocortical innervation subtypes of layer 5 intratelencephalic cells in the murine secondary motor cortex

Im, Sanghun; Ueta, Yoshifumi; Ôtsuka, Takeshi; Morishima, Mieko; Youssef, Mohamed Ben; Hirai, Yasuharu; Kobayashi, Kenta; Kaneko, Ryosuke; Morita, Kenji; Kawaguchi, Yasuo

doi:10.1093/cercor/bhac052

Cited by 4 publications

(5 citation statements)

References 66 publications

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“…Accordingly, we infer that PA-iTMS mainly causes LTP in the infragranular callosal-projecting neurons, most typically L5a ITs, which are reported to be directly engaged in lateral inhibition by Martinotti cells ( Jiang et al, 2015 ). Apart from modulating the activities of Martinotti cells, the L5a ITs also relay LTP to L5b PTNs directly via local IT-PTN connections ( Kim et al, 2015 ; Baker et al, 2018 ; Im et al, 2023 ), and to L2/3 ITs through translaminar projections ( Silberberg and Markram, 2007 ). While the LTP relayed through L5a IT-L2/3 IT connections follows the same pathway as AP-iTMS, the LTP relayed through the local connections between L5a IT and L5b PTN can bypass the L2/3 IT-mediated SICF circuitry, and results in direct potentiation of the L5b PTNs.…”

Section: Discussionmentioning

confidence: 99%

Different effects of I-wave periodicity repetitive TMS on motor cortex interhemispheric interaction

Tian

Izumi

2023

Front. Neurosci.

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BackgroundActivity of the neural circuits in the human motor cortex can be probed using transcranial magnetic stimulation (TMS). Changing TMS-induced current direction recruits different cortical neural circuits. I-wave periodicity repetitive TMS (iTMS) substantially modulates motor cortex excitability through neural plasticity, yet its effect on interhemispheric interaction remains unclear.ObjectiveTo explore the modulation of interhemispheric interaction by iTMS applied in different current directions.Materials and MethodsTwenty right-handed healthy young volunteers (aged 27.5 ± 5.0 years) participated in this study with three visits. On each visit, iTMS in posterior–anterior/anterior–posterior direction (PA-/AP-iTMS) or sham-iTMS was applied to the right hemisphere, with corticospinal excitability and intracortical facilitation of the non-stimulated left hemisphere evaluated at four timepoints. Ipsilateral silent period was also measured at each timepoint probing interhemispheric inhibition (IHI).ResultsPA- and AP-iTMS potentiated cortical excitability concurrently in the stimulated right hemisphere. Corticospinal excitability of the non-stimulated left hemisphere increased 10 min after both PA- and AP-iTMS intervention, with a decrease in short-interval intracortical facilitation (SICF) observed in AP-iTMS only. Immediately after the intervention, PA-iTMS tilted the IHI balance toward inhibiting the non-stimulated hemisphere, while AP-iTMS shifted the balance toward the opposite direction.ConclusionsOur findings provide systematic evidence on the plastic modulation of interhemispheric interaction by PA- and AP-iTMS. We show that iTMS induces an interhemispheric facilitatory effect, and that PA- and AP-iTMS differs in modulating interhemispheric inhibition.

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Section: Discussionmentioning

confidence: 99%

Different effects of I-wave periodicity repetitive TMS on motor cortex interhemispheric interaction

Tian

Izumi

2023

Front. Neurosci.

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“…Two mouse lines were used, wild-type (C57BL/6JJmsSlc, obtained from Japan SLC) and Tlx3-Cre [B6.FVB(Cg)-Tg(Tlx3-cre)PL56Gsat/Mmucd (RRID: MMRRC_041158-UCD )]. The Tlx3-Cre mouse line has Cre -expressing neurons in a subpopulation of IT neurons in L5a and superficial layer 5b ( Gerfen et al, 2013 ; Callaway et al, 2021 ; Muñoz-Castañeda et al, 2021 ; Im et al, 2022 ). Virtually all Tlx3-Cre -positive ( Tlx3 +) neurons have their axonal arborizations confined within the telencephalon and have few axons in the thalamus, brainstem, and spinal cord ( Gerfen et al, 2013 ; Callaway et al, 2021 ; Im et al, 2022 ).…”

Section: Methodsmentioning

confidence: 99%

“…The Tlx3-Cre mouse line has Cre -expressing neurons in a subpopulation of IT neurons in L5a and superficial layer 5b ( Gerfen et al, 2013 ; Callaway et al, 2021 ; Muñoz-Castañeda et al, 2021 ; Im et al, 2022 ). Virtually all Tlx3-Cre -positive ( Tlx3 +) neurons have their axonal arborizations confined within the telencephalon and have few axons in the thalamus, brainstem, and spinal cord ( Gerfen et al, 2013 ; Callaway et al, 2021 ; Im et al, 2022 ). In addition, the majority of L5a IT neurons in the secondary motor cortex innervate the striatum ( Im et al, 2022 ).…”

Section: Methodsmentioning

confidence: 99%

“…Virtually all Tlx3-Cre -positive ( Tlx3 +) neurons have their axonal arborizations confined within the telencephalon and have few axons in the thalamus, brainstem, and spinal cord ( Gerfen et al, 2013 ; Callaway et al, 2021 ; Im et al, 2022 ). In addition, the majority of L5a IT neurons in the secondary motor cortex innervate the striatum ( Im et al, 2022 ). We thus consider that Tlx3 + neurons well represent a subset of L5a IT neurons that project to the striatum.…”

Section: Methodsmentioning

confidence: 99%

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Layer 5 Intratelencephalic Neurons in the Motor Cortex Stably Encode Skilled Movement

Shinotsuka,

Tanaka,

Terada

et al. 2023

J. Neurosci.

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The primary motor cortex (M1) and the dorsal striatum play a critical role in motor learning and the retention of learned behaviors. Motor representations of corticostriatal ensembles emerge during motor learning. In the coordinated reorganization of M1 and the dorsal striatum for motor learning, layer 5a (L5a), which connects M1 to the ipsi- and contra-lateral dorsal striatum, should be a key layer. Although M1 L5a neurons represent movement-related activity in the late stage of learning, it is unclear whether the activity is retained as a memory engram. Here, usingTlx3-Cremale transgenic mice, we conducted two-photon calcium imaging of striatum-projecting L5a intratelencephalic (IT) neurons in forelimb M1 during late sessions of a self-initiated lever-pull task, and in sessions after 6 days of non-training following the late sessions. We found that trained male animals exhibited stable motor performance before and after the non-training days. At the same time, we found that M1 L5a IT neurons strongly represented the well-learned forelimb movement, but not uninstructed orofacial movements. A subset of M1 L5a IT neurons consistently coded the well-learned forelimb movement before and after the non-training days. Inactivation of M1 IT neurons after learning impaired task performance when the lever was made heavier or when the target range of the pull distance was narrowed. These results suggest that a subset of M1 L5a IT neurons continuously represent skilled movement after learning and serve to fine-tune the kinematics of well-learned movement.Significance StatementMotor memory persists even when it is not used for a while. Intratelencephalic neurons in layer 5a (L5a IT neurons) of the primary motor cortex (M1) gradually come to represent skilled forelimb movements during motor learning. However, it remains to be determined whether these changes persist over a long period and how these neurons contribute to skilled movements. Here, we show that a subset of M1 L5a IT neurons retain information for skilled forelimb movements even after non-training days. Furthermore, suppressing the activity of these neurons during skilled forelimb movements impaired behavioral stability and adaptability. Our results suggest the importance of M1 L5a IT neurons for tuning skilled forelimb movements over a long period.

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“…The laminar location roughly corresponds to their typical projection targets (Molyneaux et al 2007 ; Petreanu et al 2007 ; Mao et al 2011 ; Han et al 2018 ): for example, L2/3 pyramidal cell axons arborize within the telencephalic regions [intratelencephalic (IT) cells], while L5 of the frontal cortex consists of two major subtypes, contralaterally projecting IT cells and pontine nuclei-projecting pyramidal tract (PT) cells (Hallman et al 1988 ; Cowan and Wilson 1994 ; Reiner et al 2003 ; Arlotta et al 2005 ; Morishima and Kawaguchi 2006 ; Morishima et al 2011 ; Ueta et al 2014 ; Kawaguchi 2017 ). L5 IT cells in the secondary motor cortex (M2) broadly send feedback signals to multiple cortical areas, and contain diverse projection types with different L1-targeting preference (Im et al 2023 ). PT cells project to the ipsilateral pontine nuclei (Kita and Kita 2012 ), and they also innervate the other brain regions outside the telencephalon such as the thalamus, superior colliculus, zona incerta, the other brainstem areas and the spinal cord (Hirai et al 2012 ; Kita and Kita 2012 ).…”

Section: Cell Type Classification In the Neocortexmentioning

confidence: 99%

Synaptic configuration and reconfiguration in the neocortex are spatiotemporally selective

Sohn

2023

Anat Sci Int

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Brain computation relies on the neural networks. Neurons extend the neurites such as dendrites and axons, and the contacts of these neurites that form chemical synapses are the biological basis of signal transmissions in the central nervous system. Individual neuronal outputs can influence the other neurons within the range of the axonal spread, while the activities of single neurons can be affected by the afferents in their somatodendritic fields. The morphological profile, therefore, binds the functional role each neuron can play. In addition, synaptic connectivity among neurons displays preference based on the characteristics of presynaptic and postsynaptic neurons. Here, the author reviews the “spatial” and “temporal” connection selectivity in the neocortex. The histological description of the neocortical circuitry depends primarily on the classification of cell types, and the development of gene engineering techniques allows the cell type-specific visualization of dendrites and axons as well as somata. Using genetic labeling of particular cell populations combined with immunohistochemistry and imaging at a subcellular spatial resolution, we revealed the “spatial selectivity” of cortical wirings in which synapses are non-uniformly distributed on the subcellular somatodendritic domains in a presynaptic cell type-specific manner. In addition, cortical synaptic dynamics in learning exhibit presynaptic cell type-dependent “temporal selectivity”: corticocortical synapses appear only transiently during the learning phase, while learning-induced new thalamocortical synapses persist, indicating that distinct circuits may supervise learning-specific ephemeral synapse and memory-specific immortal synapse formation. The selectivity of spatial configuration and temporal reconfiguration in the neural circuitry may govern diverse functions in the neocortex.

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Corticocortical innervation subtypes of layer 5 intratelencephalic cells in the murine secondary motor cortex

Cited by 4 publications

References 66 publications

Different effects of I-wave periodicity repetitive TMS on motor cortex interhemispheric interaction

Different effects of I-wave periodicity repetitive TMS on motor cortex interhemispheric interaction

Layer 5 Intratelencephalic Neurons in the Motor Cortex Stably Encode Skilled Movement

Synaptic configuration and reconfiguration in the neocortex are spatiotemporally selective

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