Neuron type-specific optogenetic stimulation for differential stroke recovery in chronic capsular infarct
2
조회
0
다운로드
0
인용
0
참고문헌
초록
Cortical neuromodulation (CNM) is widely used to promote recovery after stroke. Despite the beneficial results of CNM, the roles played by different neuron types in the effects of current CNM techniques are unable to be differentiated. Our aim was to use selective optogenetic cortical stimulation to explore how different subpopulations of neuronal cells contribute to poststroke recovery. We transduced the sensory-parietal cortex (SPC) of rats with CamKII-ChR2 (pyramidal neurons), PV-ChR2 (parvalbumin-expressing inhibitory neurons), or hSyn-ChR2 (pan-neuronal population) before inducing photothrombotic capsular infarct lesions. We found that selective stimulation of inhibitory neurons resulted in significantly greater motor recovery than stimulation of excitatory neurons or the pan-neuronal population. Furthermore, 2-deoxy-2-[18F] fluoro-D-glucose microPET (FDG-microPET) imaging revealed a significant reduction in cortical diaschisis and activation of the corticostriatal neural circuit, which were correlated with behavioral recovery in the PV-ChR2 group. The spatial pattern of brain-derived neurotrophic factor (BDNF) expression was evident in the stimulated cortex and underlying cortico-subcortical circuit. Our results indicate that the plasticity of inhibitory neurons is crucial for functional recovery after capsular infarct. Modifying CNM parameters to potentiate the stimulation of inhibitory neurons could improve poststroke outcomes.
Abstract
Cortical neuromodulation (CNM) is widely used to promote recovery after stroke. Despite the beneficial results of CNM, the roles played by different neuron types in the effects of current CNM techniques are unable to be differentiated. Our aim was to use selective optogenetic cortical stimulation to explore how different subpopulations of neuronal cells contribute to poststroke recovery. We transduced the sensory-parietal cortex (SPC) of rats with CamKII-ChR2 (pyramidal neurons), PV-ChR2 (parvalbumin-expressing inhibitory neurons), or hSyn-ChR2 (pan-neuronal population) before inducing photothrombotic capsular infarct lesions. We found that selective stimulation of inhibitory neurons resulted in significantly greater motor recovery than stimulation of excitatory neurons or the pan-neuronal population. Furthermore, 2-deoxy-2-[18F] fluoro-D-glucose microPET (FDG-microPET) imaging revealed a significant reduction in cortical diaschisis and activation of the corticostriatal neural circuit, which were correlated with behavioral recovery in the PV-ChR2 group. The spatial pattern of brain-derived neurotrophic factor (BDNF) expression was evident in the stimulated cortex and underlying cortico-subcortical circuit. Our results indicate that the plasticity of inhibitory neurons is crucial for functional recovery after capsular infarct. Modifying CNM parameters to potentiate the stimulation of inhibitory neurons could improve poststroke outcomes.
참고문헌 (63)
- Jarrasse, N., "Robotic exoskeletons : a perspective for the rehabilitation of arm coordination in stroke patients", Front Hum Neurosci, 8, pp.947~ (2014)
- Meyers, E. C., "Vagus nerve stimulation enhances stable plasticity and gen eralization of stroke recovery", Stroke, 49, pp.710~717 (2018)
- Tosun, A., "Effects of low-frequency repetitive transcranial magnetic stimu lation and neuromuscular electrical stimulation on upper extremity motor recovery in the early period after stroke : a preliminary study", Top Stroke Rehabil, 24, pp.361~367 (2017)
- Boake, C., "Constraint-induced movement therapy during early stroke reha bilitation", Neurorehabil Neural Repair, 21, pp.14~24 (2007)
- Hamoudi, M., "Transcranial Direct current stimulation enhances motor skill learning but not generalization in chronic stroke", Neurorehabil Neural Repair, 32, pp.295~308 (2018)
- Di Pino, G., "Modulation of brain plasticity in stroke : a novel model for neurorehabilitation", Nat Rev Neurol, 10, pp.597~608 (2014)
- Kim, H. I., "Unipolar and continuous cortical stimulation to enhance motor and language deficit in patients with chronic stroke : report of 2 cases", Surg Neurol, 69, pp.77~80 (2008)
- Kuo, H. I., "Acute and chronic effects of noradrenergic enhancement on transcranial direct current stimulation-induced neuroplasticity in humans", J Physiol, 595, pp.1305~1314 (2017)
- Hummel, F., "Improvement of motor function with noninvasive cortical stimulation in a patient with chronic stroke", Neurorehabil Neural Repair, 19, pp.14~19 (2005)
- Nitsche, M. A., "Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans", J Physiol, 553, pp.293~301 (2003)
- Kim, Y. H., "Repetitive transcranial magnetic stimulation-induced cortico motor excitability and associated motor skill acquisition in chronic stroke", Stroke, 37, pp.1471~1476 (2006)
- Zeiler, S. R., "The interaction between training and plasticity in the poststroke brain", Curr Opin Neurol, 26, pp.609~616 (2013)
- Lefebvre, S., "Neural substrates underlying stimulation-enhanced motor skill learning after stroke", Brain, 138, pp.149~163 (2015)
- Murphy, G. G., "Increased neuronal excitability, synaptic plasticity, and learning in aged Kvbeta1.1 knockout mice", Curr Biol, 14, pp.1907~1915 (2004)
- Borchers, S., "Direct electrical stimulation of human cortex- the gold standard for mapping brain functions?", Nat Rev Neurosci, 13, pp.63~70 (2011)
- Cheng, M. Y., "Optogenetic approaches to target specific neural circuits in post-stroke recovery", Neurotherapeutics, 13, pp.325~340 (2016)
- Tennant, K. A., "Optogenetic rewiring of thalamocortical circuits to restore function in the stroke injured brain", Nat Commun, 8, pp.15879~ (2017)
- Cheng, M. Y., "Optogenetic neuronal stimulation promotes functional recovery after stroke", Proc Natl Acad Sci USA, 111, pp.12913~12918 (2014)
- Wahl, A. S., "Optogenetically stimulating intact rat corticospinal tract post stroke restores motor control through regionalized functional circuit formation", Nat Commun, 8, pp.1187~ (2017)
- Vahdat, S., "Brain-wide neural dynamics of poststroke recovery induced by optogenetic stimulation", Sci Adv, 7, pp.eabd9465~ (2021)
- Nam, M. H., "Excessive astrocytic GABA causes cortical hypometabolism and impedes functional recovery after subcortical stroke", Cell Rep, 32, pp.107861~ (2020)
- Kim, D., "Longitudinal changes in resting-state brain activity in a capsular infarct model", J Cereb Blood Flow Metab, 35, pp.11~19 (2015)
- Lee, M. C., "Ultrastructural dendritic changes underlying diaschisis after capsular infarct", J Neuropathol Exp Neurol, 79, pp.508~517 (2020)
- Kim, R. G., "Sensory-parietal cortical stimulation improves motor recovery in severe capsular infarct", J Cereb Blood Flow Metab, 36, pp.2211~2222 (2016)
- Kepecs, A., "Interneuron cell types are fit to function", Nature, 505, pp.318~326 (2014)
- Kim, H. S., "A rat model of photothrombotic capsular infarct with a marked motor deficit : a behavioral, histologic, and microPET study", J Cereb Blood Flow Metab, 34, pp.683~689 (2014)
- Cho, J., "Remodeling of neuronal circuits after reach training in chronic capsular stroke", Neurorehabil Neural Repair, 30, pp.941~950 (2016)
- Stujenske, J. M., "Modeling the spatiotemporal dynamics of light and heat propagation for in vivo optogenetics", Cell Rep, 12, pp.525~534 (2015)
- Song, H., "Capsular stroke modeling based on somatotopic mapping of motor fibers", J Cereb Blood Flow Metab, 37, pp.2928~2937 (2016)
- Song, M., "Optogenetic stimulation of glutamatergic neuronal activity in the striatum enhances neurogenesis in the subventricular zone of normal and stroke mice", Neurobiol Dis, 98, pp.9~24 (2017)
- Arenkiel, B. R., "In vivo light-induced activation of neural circuitry in trans genic mice expressing channelrhodopsin-2", Neuron, 54, pp.205~218 (2007)
- Zhang, F., "Channelrhodopsin-2 and optical control of excitable cells", Nat Methods, 3, pp.785~792 (2006)
- Papp, E. A., "Waxholm Space atlas of the Sprague Dawley rat brain", Neuroimage, 97, pp.374~386 (2014)
- Cox, R. W., "AFNI : software for analysis and visualization of functional magnetic resonance neuroimages", Comput Biomed Res Int J, 29, pp.162~173 (1996)
- Kim, D., "Longitudinal changes in resting-state brain activity in a capsular infarct model", J Cereb Blood Flow Metab, 35, pp.11~19 (2014)
- Stinear, C. M., "Primary motor cortex excitability during recovery after stroke : implications for neuromodulation", Brain Stimul, 8, pp.1183~1190 (2015)
- Gao, Z., "Evaluation of relationships between corticospinal excitability and somatosensory deficits in the acute and subacute phases of stroke", J Integr Neurosci, 22, pp.61~ (2023)
- Harris-Love, M. L., "Neural substrates of motor recovery in severely impaired stroke patients with hand paralysis", Neu rorehabil Neural Repair, 30, pp.328~338 (2016)
- Hodics, T., "Functional neuroimaging in motor recovery after stroke", Top Stroke Rehabil, 12, pp.15~21 (2005)
- Jenkins, I. H., "Motor sequence learning : a study with positron emission tomography", J Neurosci, 14, pp.3775~3790 (1994)
- Ward, N. S., "Neural correlates of motor recovery after stroke : a longitudinal fMRI study", Brain, 126, pp.2476~2496 (2003)
- Hagemann, G., "Increased long-term potentiation in the surround of experimentally induced focal cortical infarction", Ann Neurol, 44, pp.255~258 (1998)
- Day, B. L., "Electric and magnetic stimulation of human motor cortex : surface EMG and single motor unit responses", J Physiol, 412, pp.449~473 (1989)
- Ranck, J. B. Jr., "Which elements are excited in electrical stimulation of mammalian central nervous system: a review", Brain Res, 98, pp.417~440 (1975)
- Shah, A. M., "Optogenetic neuronal stimulation of the lateral cerebellar nucleus promotes persistent functional recovery after stroke", Sci Rep, 7, pp.46612~ (2017)
- Di Lazzaro, V., "Corticospinal activity evoked and modulated by non-invasive stimulation of the intact human motor cortex", J Physiol, 592, pp.4115~4128 (2014)
- Carmichael, S. T., "Brain excitability in stroke : the yin and yang of stroke pro gression", Arch Neurol, 69, pp.161~167 (2012)
- Clarkson, A. N., "AMPA receptor-induced local brain-derived neurotrophic factor signaling mediates motor recovery after stroke", J Neurosci, 31, pp.3766~3775 (2011)
- Kujirai, T., "Corticocortical inhibition in human motor cortex", J Physiol, 471, pp.501~519 (1993)
- Gupta, A., "Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex", Science, 287, pp.273~278 (2000)
- Castillo, P. E., "Long-term plasticity at inhibitory synapses", Curr Opin Neurobiol, 21, pp.328~338 (2011)
- Lefort, S., "Long-term inhibitory plasticity in visual cortical layer 4 switches sign at the opening of the critical period", Proc Natl Acad Sci USA, 110, pp.E4540~E4547 (2013)
- Rosanova, M., "Natural frequencies of human corticothalamic circuits", J Neurosci, 29, pp.7679~7685 (2009)
- Momi, D., "Perturbation of resting-state network nodes preferentially pro pagates to structurally rather than functionally connected regions", Sci Rep, 11, pp.12458~ (2021)
- Grigoras, I. F., "Recent advances in the role of excitation-inhibition balance in motor recovery post-stroke", Fac Rev, 10, pp.58~ (2021)
- Turrigiano, G. G., "Homeostatic plasticity in the developing nervous system", Nat Rev Neurosci, 5, pp.97~107 (2004)
- Paparella, I., "An integrated measure of GABA to characterize post-stroke plasticity", Neuroimage Clin, 39, pp.103463~ (2023)
- Caporale, N., "Spike timing-dependent plasticity : a Hebbian learning rule", Annu Rev Neurosci, 31, pp.25~46 (2008)
- Paille, V., "GABAergic circuits control spike-timing-dependent plasticity", J Neurosci, 33, pp.9353~9363 (2013)
- Takeuchi, N., "Noninvasive brain stimulation for motor recovery after stroke : mechanisms and future views", Stroke Res Treat, 2012, pp.584727~ (2012)
- Mahmud, M., "Differential modulation of excitatory and inhibitory neurons during periodic stimulation", Front Neurosci, 10, pp.62~ (2016)
- Lioumis, P., "Probing modifications of cortical excitability during stroke recovery with navigated transcranial magnetic stimulation", Top Stroke Rehabil, 19, pp.182~192 (2012)
- Klomjai, W., "Basic principles of transcranial magnetic stimulation(TMS)and repetitive TMS(rTMS)", Ann Phys Rehabil Med, 58, pp.208~213 (2015)
