Acute stress differently modulates interneurons excitability and synaptic plasticity in the primary motor cortex of wild-type and SOD1

SOD1G93A mutation acute stress amyotrophic lateral sclerosis primary motor cortex

Journal

The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262

Informations de publication

Date de publication:
31 Aug 2024
Historique:
received: 28 06 2023
accepted: 12 07 2024
medline: 1 9 2024
pubmed: 1 9 2024
entrez: 31 8 2024
Statut: aheadofprint

Résumé

Primary motor cortex (M1) network stability depends on activity of inhibitory interneurons, for which susceptibility to stress was previously demonstrated in limbic regions. Hyperexcitability in M1 following changes in the excitatory/inhibitory balance is a key pathological hallmark of amyotrophic lateral sclerosis (ALS). Using electrophysiological approaches, we assessed the impact of acute restraint stress on inhibitory interneurons excitability and global synaptic plasticity in M1 of the SOD1

Identifiants

pubmed: 39216080
doi: 10.1113/JP285210
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Université de Bordeaux (University of Bordeaux)
ID : GPR BRAIN-2030

Informations de copyright

© 2024 The Author(s). The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.

Références

Ahima, R., Krozowski, Z., & Harlan, R. E. (1991). Type I corticosteroid receptor‐like immunoreactivity in the rat CNS: Distribution and regulation by corticosteroids. Journal of Comparative Neurology, 313(3), 522–538.
Ahima, R. S., & Harlan, R. E. (1990). Charting of type II glucocorticoid receptor‐like immunoreactivity in the rat central nervous system. Neuroscience, 39(3), 579–604.
Ahima, R. S., Tagoe, C. N. B., & Harlan, R. E. (1992). Type II corticosteroid receptor‐like immunoreactivity in the rat cerebellar cortex: Differential regulation by corticosterone. Neuroendocrinology, 55(6), 683–694.
Apicella, A. J., Wickersham, I. R., Seung, H. S., & Shepherd, G. M. G. (2012). Laminarly orthogonal excitation of fast‐spiking and low‐threshold‐spiking interneurons in mouse motor cortex. Journal of Neuroscience, 32(20), 7021–7033.
Arancibia, S., Payet, O., Givalois, L., & Tapia‐Arancibia, L. (2001). Acute stress and dexamethasone rapidly increase hippocampal somatostatin synthesis and release from the dentate gyrus hilus. Hippocampus, 11(4), 469–477.
Aroniadou, V. A., & Keller, A. (1993). The patterns and synaptic properties of horizontal intracortical connections in the rat motor cortex. Journal of Neurophysiology, 70(4), 1553–1569.
Bakken, T. E., Jorstad, N. L., Hu, Q., Lake, B. B., Tian, W., Kalmbach, B. E., Crow, M., Hodge, R. D., Krienen, F. M., Sorensen, S. A., Eggermont, J., Yao, Z., Aevermann, B. D., Aldridge, A. I., Bartlett, A., Bertagnolli, D., Casper, T., Castanon, R. G., Crichton, K., Daigle, T. L., Dalley, R., Dee, N., Linnarsson, S., & Lein, E. S. (2021). Comparative cellular analysis of motor cortex in human, marmoset and mouse. Nature, 598(7879), 111–119.
Bhattacharjee, S., Kashyap, R., Abualait, T., Annabel Chen, S. H., Yoo, W. K., & Bashir, S. (2021). The role of primary motor cortex: More than movement execution. Journal of Motor Behavior, 53(2), 258–274.
den Bos, M., Higashihara, M., Geevasinga, N., Menon, P., Kiernan, M. C., & Vucic, S. (2018). Imbalance of cortical facilitatory and inhibitory circuits underlies hyperexcitability in ALS. Neurology, 91(18), e1669–e1676.
Broqua, P., Baudrie, V., Laude, D., & Chaouloff, F. (1992). Influence of the novel antidepressant tianeptine on neurochemical, neuroendocrinological, and behavioral effects of stress in rats. Biological Psychiatry, 31(4), 391–400.
Brunet, A., Stuart‐Lopez, G., Burg, T., Scekic‐Zahirovic, J., & Rouaux, C. (2020). Cortical circuit dysfunction as a potential driver of amyotrophic lateral sclerosis. Frontiers in Neuroscience, 14, 363.
Buynitsky, T., & Mostofsky, D. I. (2009). Restraint stress in biobehavioral research: Recent developments. Neuroscience and Biobehavioral Reviews, 33(7), 1089–1098.
Calcagnotto, M. E. (2016). Interneurons: Role in maintaining and restoring synaptic plasticity. Frontiers in Psychiatry, 7, 86.
Campos, A. C., Fogaça, M. V., Aguiar, D. C., & Guimarães, F. S. (2013). Animal models of anxiety disorders and stress. Revista Brasileira de Psiquiatria (Sao Paulo, Brazil: 1999), 35 Suppl 2, S101‐111.
Cengiz, B., Fidanci, H., Kiyak Keçeli, Y., Baltaci, H., & KuruoĞlu, R. (2019). Impaired short‐ and long‐latency afferent inhibition in amyotrophic lateral sclerosis. Muscle & Nerve, 59(6), 699–704.
Chaouloff, F., Hemar, A., & Manzoni, O. (2007). Acute stress facilitates hippocampal CA1 metabotropic glutamate receptor‐dependent long‐term depression. Journal of Neuroscience, 27(27), 7130–7135.
Chen, R., Lozano, A. M., & Ashby, P. (1999). Mechanism of the silent period following transcranial magnetic stimulation. Experimental Brain Research, 128(4), 539–542.
Chung, S. W., Hill, A. T., Rogasch, N. C., Hoy, K. E., & Fitzgerald, P. B. (2016). Use of theta‐burst stimulation in changing excitability of motor cortex: A systematic review and meta‐analysis. Neuroscience and Biobehavioral Reviews, 63, 43–64.
Chung, Y. H., Joo, K. M., Nam, R. H., Cho, M. H., Kim, D. J., Lee, W. B., & Cha, C. I. (2005). Decreased expression of calretinin in the cerebral cortex and hippocampus of SOD1G93A transgenic mice. Brain Research, 1035(1), 105–109.
Clark, R. M., Brizuela, M., Blizzard, C. A., & Dickson, T. C. (2018). Reduced excitability and increased neurite complexity of cortical interneurons in a familial mouse model of amyotrophic lateral sclerosis. Frontiers in Cellular Neuroscience, 12, 328.
Concerto, C., Patel, D., Infortuna, C., Chusid, E., Muscatello, M. R., Bruno, A., Zoccali, R., Aguglia, E., & Battaglia, F. (2017). Academic stress disrupts cortical plasticity in graduate students. Stress (Amsterdam, Netherlands), 20(2), 212–216.
Coxon, J. P., Peat, N. M., & Byblow, W. D. (2014). Primary motor cortex disinhibition during motor skill learning. Journal of Neurophysiology, 112(1), 156–164.
Dallé, E., & Mabandla, M. V. (2018). Early life stress, depression and Parkinson's disease: A new approach. Molecular Brain, 11(1), 18.
Davies, C. H., Starkey, S. J., Pozza, M. F., & Collingridge, G. L. (1991). GABA autoreceptors regulate the induction of LTP. Nature, 349(6310), 609–611.
Deschênes, M., Veinante, P., & Zhang, Z. W. (1998). The organization of corticothalamic projections: Reciprocity versus parity. Brain Research Reviews, 28(3), 286–308.
Diamond, D. M., & Rose, G. M. (1994). Stress impairs LTP and hippocampal‐dependent memory. Annals of the New York Academy of Sciences, 746, 411–414.
Donato, F., Rompani, S. B., & Caroni, P. (2013). Parvalbumin‐expressing basket‐cell network plasticity induced by experience regulates adult learning. Nature, 504(7479), 272–276.
Donoghue, J. P., & Parham, C. (1983). Afferent connections of the lateral agranular field of the rat motor cortex. Journal of Comparative Neurology, 217(4), 390–404.
Dum, R. P., Levinthal, D. J., & Strick, P. L. (2019). The mind–body problem: Circuits that link the cerebral cortex to the adrenal medulla. Proceedings of the National Academy of Sciences of the United States of America, 116(52), 26321–26328.
Duman, R. S., Sanacora, G., & Krystal, J. H. (2019). Altered connectivity in depression: GABA and glutamate neurotransmitter deficits and reversal by novel treatments. Neuron, 102(1), 75–90.
Fan, K. M., Qiu, L. J., Ma, N., Du, Y. N., Qian, Z. Q., Wei, C. L., Han, J., Ren, W., Shi, M. M., & Liu, Z. Q. (2019). Acute stress facilitates LTD induction at glutamatergic synapses in the hippocampal CA1 region by activating μ‐opioid receptors on GABAergic neurons. Frontiers in Neuroscience, 13, 71.
Fee, C., Banasr, M., & Sibille, E. (2017). Somatostatin‐positive gamma‐aminobutyric acid interneuron deficits in depression: Cortical microcircuit and therapeutic perspectives. Biological Psychiatry, 82(8), 549–559.
Fogaça, M. V., & Duman, R. S. (2019). Cortical GABAergic dysfunction in stress and depression: New insights for therapeutic interventions. Frontiers in Cellular Neuroscience, 13, 87.
Fujiki, M., Kawasaki, Y., & Fudaba, H. (2020). Continuous theta‐burst stimulation intensity dependently facilitates motor‐evoked potentials following focal electrical stimulation of the rat motor cortex. Frontiers in Neural Circuits, 14, 585624.
Gellner, A. K., Sitter, A., Rackiewicz, M., Sylvester, M., Philipsen, A., Zimmer, A., & Stein, V. (2022). Stress vulnerability shapes disruption of motor cortical neuroplasticity. Translational Psychiatry, 12(1), 91.
Glavin, G. B., Paré, W. P., Sandbak, T., Bakke, H. K., & Murison, R. (1994). Restraint stress in biomedical research: an update. Neuroscience and Biobehavioral Reviews, 18(2), 223–249.
Golini, E., Rigamonti, M., Iannello, F., De Rosa, C., Scavizzi, F., Raspa, M., & Mandillo, S. (2020). A non‐invasive digital biomarker for the detection of rest disturbances in the SOD1G93A mouse model of ALS (preprint). Frontiers in Neuroscience, 14, 896.
Gonzalez Deniselle, M. C., Liere, P., Pianos, A., Meyer, M., Aprahamian, F., Cambourg, A., Di Giorgio, N. P., Schumacher, M., De Nicola, A. F., & Guennoun, R. (2016). Steroid profiling in male wobbler mouse, a model of amyotrophic lateral sclerosis. Endocrinology, 157(11), 4446–4460.
Gouwens, N. W., Sorensen, S. A., Baftizadeh, F., Budzillo, A., Lee, B. R., Jarsky, T., Alfiler, L., Baker, K., Barkan, E., Berry, K., Bertagnolli, D., Bickley, K., Bomben, J., Braun, T., Brouner, K., Casper, T., Crichton, K., Daigle, T. L., Dalley, R., de Frates, R. A., Dee, N., Desta, T., & Zeng, H. (2020). Integrated morphoelectric and transcriptomic classification of cortical GABAergic cells. Cell, 183(4), 935–953.e19.
Graybeal, C., Kiselycznyk, C., & Holmes, A. (2011). Stress‐induced deficits in cognition and emotionality: A role for glutamate. In J. F. Cryan, A. Reif (Eds.), Behavioral neurogenetics. Current topics in behavioral neurosciences (pp. 189–207). Springer Berlin Heidelberg.
Grèzes, J., Valabrègue, R., Gholipour, B., & Chevallier, C. (2014). A direct amygdala‐motor pathway for emotional displays to influence action: A diffusion tensor imaging study. Human Brain Mapping, 35(12), 5974–5983.
Gu, Y., Tran, T., Murase, S., Borrell, A., Kirkwood, A., & Quinlan, E. M. (2016). Neuregulin‐dependent regulation of fast‐spiking interneuron excitability controls the timing of the critical period. Journal of Neuroscience, 36(40), 10285–10295.
Gunes, Z. I., Kan, V. W. Y., Ye, X., & Liebscher, S. (2020). Exciting complexity: The role of motor circuit elements in ALS pathophysiology. Frontiers in Neuroscience, 14. https://doi.org/10.3389/fnins.2020.00573
Gurney, M. E., Pu, H., Chiu, A. Y., Dal Canto, M. C., Polchow, C. Y., Alexander, D. D., Caliendo, J., Hentati, A., Kwon, Y. W., & Deng, H. X. (1994). Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science, 264(5166), 1772–1775.
Han, Q., Cao, C., Ding, Y., So, K. F., Wu, W., Qu, Y., & Zhou, L. (2015). Plasticity of motor network and function in the absence of corticospinal projection. Experimental Neurology, 267, 194–208.
He, J. L., Fuelscher, I., Coxon, J., Chowdhury, N., Teo, W. P., Barhoun, P., Enticott, P., & Hyde, C. (2019). Individual differences in intracortical inhibition predict motor‐inhibitory performance. Experimental Brain Research, 237(10), 2715–2727.
Helm, J., Akgul, G., & Wollmuth, L. P. (2013). Subgroups of parvalbumin‐expressing interneurons in layers 2/3 of the visual cortex. Journal of Neurophysiology, 109(6), 1600–1613.
Hentschke, H., Raz, A., Krause, B. M., Murphy, C. A., & Banks, M. I. (2017). Disruption of cortical network activity by the general anaesthetic isoflurane. British Journal of Anaesthesia, 119(4), 685–696.
Hess, G., & Donoghue, J. P. (1996). Long‐term depression of horizontal connections in rat motor cortex. European Journal of Neuroscience, 8(4), 658–665.
Hoeijmakers, L., Ruigrok, S. R., Amelianchik, A., Ivan, D., van Dam, A. M., Lucassen, P. J., & Korosi, A. (2017). Early‐life stress lastingly alters the neuroinflammatory response to amyloid pathology in an Alzheimer's disease mouse model. Brain, Behavior, and Immunity, 63, 160–175.
Imas, O. A., Ropella, K. M., Ward, B. D., Wood, J. D., & Hudetz, A. G. (2005). Volatile anesthetics disrupt frontal‐posterior recurrent information transfer at gamma frequencies in rat. Neuroscience Letters, 387(3), 145–150.
Jadavji, N. M., & Metz, G. A. (2008). Sex differences in skilled movement in response to restraint stress and recovery from stress. Behavioural Brain Research, 195(2), 251–259.
Jefferson, S. J., Feng, M., Chon, U. R., Guo, Y., Kim, Y., & Luscher, B. (2020). Disinhibition of somatostatin interneurons confers resilience to stress in male but not female mice. Neurobiology of Stress, 13, 100238.
Jiang, S. S., Gong, M. N., Rao, W., Chai, W., Chen, W. Z., Zhang, X., Nie, H. B., & Xu, R. S. (2023). 5‐Hydroxytryptamine: A potential therapeutic target in amyotrophic lateral sclerosis. Neural Regeneration Research, 18(9), 2047.
Joëls, M., & Baram, T. Z. (2009). The neuro‐symphony of stress. Nature Reviews Neuroscience, 10(6), 459–466.
Joffe, M. E., Maksymetz, J., Luschinger, J. R., Dogra, S., Ferranti, A. S., Luessen, D. J., Gallinger, I. M., Xiang, Z., Branthwaite, H., Melugin, P. R., Williford, K. M., Centanni, S. W., Shields, B. C., Lindsley, C. W., Calipari, E. S., Siciliano, C. A., Niswender, C. M., Tadross, M. R., Winder, D. G., & Conn, P. J. (2022). Acute restraint stress redirects prefrontal cortex circuit function through mGlu5 receptor plasticity on somatostatin‐expressing interneurons. Neuron, 110(6), 1068–1083.e5.
Kavushansky, A., Ben‐Shachar, D., Richter‐Levin, G., & Klein, E. (2009). Physical stress differs from psychosocial stress in the pattern and time‐course of behavioral responses, serum corticosterone and expression of plasticity‐related genes in the rat. Stress (Amsterdam, Netherlands), 12(5), 412–425.
Kawaguchi, Y. (1997). Selective cholinergic modulation of cortical GABAergic cell subtypes. Journal of Neurophysiology, 78(3), 1743–1747.
Khademullah, C. S., Aqrabawi, A. J., Place, K. M., Dargaei, Z., Liang, X., Pressey, J. C., Bedard, S., Yang, J. W., Garand, D., Keramidis, I., Gasecka, A., Côté, D., De Koninck, Y., Keith, J., Zinman, L., Robertson, J., Kim, J. C., & Woodin, M. A. (2020). Cortical interneuron‐mediated inhibition delays the onset of amyotrophic lateral sclerosis. Brain, 143(3), 800–810.
Kim, J., Hughes, E. G., Shetty, A. S., Arlotta, P., Goff, L. A., Bergles, D. E., & Brown, S. P. (2017). Changes in the excitability of neocortical neurons in a mouse model of amyotrophic lateral sclerosis are not specific to corticospinal neurons and are modulated by advancing disease. Journal of Neuroscience, 37(37), 9037–9053.
Kim, J. J., Foy, M. R., & Thompson, R. F. (1996). Behavioral stress modifies hippocampal plasticity through N‐methyl‐D‐aspartate receptor activation. Proceedings of the National Academy of Sciences of the United States of America, 93(10), 4750–4753.
Kita, H., & Kitai, S. T. (1990). Amygdaloid projections to the frontal cortex and the striatum in the rat. Journal of Comparative Neurology, 298, 40–49.
Kolasinski, J., Hinson, E. L., Divanbeighi Zand, A. P., Rizov, A., Emir, U. E., & Stagg, C. J. (2019). The dynamics of cortical GABA in human motor learning. The Journal of Physiology, 597(1), 271–282.
Larson, J., & Munkácsy, E. (2015). Theta‐burst LTP. Brain Research, 1621, 38–50.
LeDoux, J. (2003). The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology, 23(4–5), 727–738.
LeDoux, J. E. (1994). Emotion, memory and the brain. Scientific American, 270(6), 50–57.
LeDoux, J. E., Cicchetti, P., Xagoraris, A., & Romanski, L. M. (1990). The lateral amygdaloid nucleus: Sensory interface of the amygdala in fear conditioning. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 10(4), 1062–1069.
Lemon, R. N. (2008). Descending pathways in motor control. Annual Review of Neuroscience, 31, 195–218.
Levshina, I. P., Mats, V. N., Pasikova, N. V., & Shuikin, N. N. (2009). Comparison of the behavior of rats after immobilization with structural changes in the motor cortex. Neuroscience and Behavioral Physiology, 39(9), 915–919.
Lolait, S. J., Stewart, L. Q., Jessop, D. S., Young, W. S., & O'Carroll, A. M. (2007). The hypothalamic‐pituitary‐adrenal axis response to stress in mice lacking functional vasopressin V1b receptors. Endocrinology, 148(2), 849–856.
Lourenço, J., Pacioni, S., Rebola, N., van Woerden, G. M., Marinelli, S., DiGregorio, D., & Bacci, A. (2014). Non‐associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons. PLoS Biology, 12(7), e1001903.
Ma, Y. (2006). Distinct subtypes of somatostatin‐containing neocortical interneurons revealed in transgenic mice. Journal of Neuroscience, 26(19), 5069–5082.
Maekawa, S., Al‐Sarraj, S., Kibble, M., Landau, S., Parnavelas, J., Cotter, D., Everall, I., & Leigh, P. N. (2004). Cortical selective vulnerability in motor neuron disease: a morphometric study. Brain, 127(Pt 6), 1237–1251.
Maffei, A. (2011). The many forms and functions of long term plasticity at GABAergic synapses. Neural Plasticity, 2011, 1–9.
Maguire, J. (2014). Stress‐induced plasticity of GABAergic inhibition. Frontiers in Cellular Neuroscience, 8, 157.
Marker, R. J., Stephenson, J. L., Kluger, B. M., Curran‐Everett, D., & Maluf, K. S. (2014). Modulation of intracortical inhibition in response to acute psychosocial stress is impaired among individuals with chronic neck pain. Journal of Psychosomatic Research, 76(3), 249–256.
Markram, H., Toledo‐Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nature Reviews Neuroscience, 5(10), 793–807.
Marlier, L. N., Csikós, T., Rebaudengo, N., Borboni, P., Patacchioli, F. R., Angelucci, L., Privat, A., & Lauro, R. (1995). Distribution of glucocorticoid receptor mRNA in the rat spinal cord. Neuroreport, 6(16), 2245–2249.
Maroun, M., & Richter‐Levin, G. (2003). Exposure to acute stress blocks the induction of long‐term potentiation of the amygdala–prefrontal cortex pathway in vivo. Journal of Neuroscience, 23(11), 4406–4409.
Maruyama, S., Fukunaga, M., Sugawara, S. K., Hamano, Y. H., Yamamoto, T., & Sadato, N. (2021). Cognitive control affects motor learning through local variations in GABA within the primary motor cortex. Scientific Reports, 11(1), 18566.
Matisz, C. E., Badenhorst, C. A., & Gruber, A. J. (2021). Chronic unpredictable stress shifts rat behavior from exploration to exploitation. Stress (Amsterdam, Netherlands), 24(5), 635–644.
McColgan, P., Joubert, J., Tabrizi, S. J., & Rees, G. (2020). The human motor cortex microcircuit: Insights for neurodegenerative disease. Nature Reviews Neuroscience, 21(8), 401–415.
McEwen, B. S., Nasca, C., & Gray, J. D. (2016). Stress effects on neuronal structure: Hippocampus, amygdala, and prefrontal cortex. Neuropsychopharmacology, 41(1), 3–23.
Menon, P., Geevasinga, N., van den Bos, M., Yiannikas, C., Kiernan, M. C., & Vucic, S. (2017). Cortical hyperexcitability and disease spread in amyotrophic lateral sclerosis. European Journal of Neurology, 24(6), 816–824.
Menon, P., Kiernan, M. C., & Vucic, S. (2015). Cortical hyperexcitability precedes lower motor neuron dysfunction in ALS. Clinical Neurophysiology, 126(4), 803–809.
Metz, G. A. (2007). Stress as a modulator of motor system function and pathology. Reviews in the Neurosciences, 18(3–4), 209–222.
Metz, G. A., Jadavji, N. M., & Smith, L. K. (2005). Modulation of motor function by stress: A novel concept of the effects of stress and corticosterone on behavior. European Journal of Neuroscience, 22(5), 1190–1200.
Metz, G. A. S., Schwab, M. E., & Welzl, H. (2001). The effects of acute and chronic stress on motor and sensory performance in male Lewis rats. Physiology & Behavior, 72(1–2), 29–35.
Michelson, N. J., & Kozai, T. D. Y. (2018). Isoflurane and ketamine differentially influence spontaneous and evoked laminar electrophysiology in mouse V1. Journal of Neurophysiology, 120(5), 2232–2245.
Molyneaux, B. J., Arlotta, P., Menezes, J. R. L., & Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nature Reviews Neuroscience, 8(6), 427–437.
Morecraft, R. J., McNeal, D. W., Stilwell‐Morecraft, K. S., Gedney, M., Ge, J., Schroeder, C. M., & van Hoesen, G. W. (2007). Amygdala interconnections with the cingulate motor cortex in the rhesus monkey. Journal of Comparative Neurology, 500(1), 134–165.
Morimoto, M., Morita, N., Ozawa, H., Yokoyama, K., & Kawata, M. (1996). Distribution of glucocorticoid receptor immunoreactivity and mRNA in the rat brain: An immunohistochemical and in situ hybridization study. Neuroscience Research, 26(3), 235–269.
Musazzi, L., Milanese, M., Farisello, P., Zappettini, S., Tardito, D., Barbiero, V. S., Bonifacino, T., Mallei, A., Baldelli, P., Racagni, G., Raiteri, M., Benfenati, F., Bonanno, G., & Popoli, M. (2010). Acute stress increases depolarization‐evoked glutamate release in the rat prefrontal/frontal cortex: The dampening action of antidepressants. PLoS ONE, 5(1), e8566.
Naka, A., Veit, J., Shababo, B., Chance, R. K., Risso, D., Stafford, D., Snyder, B., Egladyous, A., Chu, D., Sridharan, S., Mossing, D. P., Paninski, L., Ngai, J., & Adesnik, H. (2019). Complementary networks of cortical somatostatin interneurons enforce layer specific control. eLife, 8, e43696.
Nihei, K., McKee, A. C., & Kowall, N. W. (1993). Patterns of neuronal degeneration in the motor cortex of amyotrophic lateral sclerosis patients. Acta Neuropathologica, 86(1), 55–64.
Okamoto, K., Kihira, T., Kondo, T., Kobashi, G., Washio, M., Sasaki, S., Yokoyama, T., Miyake, Y., Sakamoto, N., Inaba, Y., & Nagai, M. (2009). Lifestyle factors and risk of amyotrophic lateral sclerosis: A case‐control study in Japan. Annals of Epidemiology, 19(6), 359–364.
Oliván, S., Calvo, A. C., Rando, A., Muñoz, M. J., Zaragoza, P., & Osta, R. (2015). Comparative study of behavioural tests in the SOD1G93A mouse model of amyotrophic lateral sclerosis. Experimental Animals, 64(2), 147–153.
Page, C. E., & Coutellier, L. (2019). Prefrontal excitatory/inhibitory balance in stress and emotional disorders: Evidence for over‐inhibition. Neuroscience and Biobehavioral Reviews, 105, 39–51.
Parkin Kullmann, J. A., Hayes, S., & Pamphlett, R. (2018). Is psychological stress a predisposing factor for amyotrophic lateral sclerosis (ALS)? An online international case‐control study of premorbid life events, occupational stress, resilience and anxiety. PLoS ONE, 13(9), e0204424.
Patacchioli, F. R., Monnazzi, P., Scontrini, A., Tremante, E., Caridi, I., Brunetti, E., Buttarelli, F. R., & Pontieri, F. E. (2003). Adrenal dysregulation in amyotrophic lateral sclerosis. Journal of Endocrinological Investigation, 26(12), RC23–RC25.
Pearson, K. (2000). Motor systems. Current Opinion in Neurobiology, 10(5), 649–654.
Piirainen, S., Youssef, A., Song, C., Kalueff, A. V., Landreth, G. E., Malm, T., & Tian, L. (2017). Psychosocial stress on neuroinflammation and cognitive dysfunctions in Alzheimer's disease: The emerging role for microglia? Neuroscience and Biobehavioral Reviews, 77, 148–164.
Rocher, C. (2004). Acute stress‐induced changes in hippocampal/prefrontal circuits in rats: Effects of antidepressants. Cerebral Cortex, 14(2), 224–229.
Saba, L., Viscomi, M. T., Caioli, S., Pignataro, A., Bisicchia, E., Pieri, M., Molinari, M., Ammassari‐Teule, M., & Zona, C. (2016). Altered functionality, morphology, and vesicular glutamate transporter expression of cortical motor neurons from a presymptomatic mouse model of amyotrophic lateral sclerosis. Cerebral Cortex, 26(4), 1512–1528.
Sadahiro, M., Demars, M. P., Burman, P., Yevoo, P., Zimmer, A., & Morishita, H. (2020). Activation of somatostatin interneurons by nicotinic modulator lypd6 enhances plasticity and functional recovery in the adult mouse visual cortex. Journal of Neuroscience, 40(27), 5214–5227.
Sale, M. V., Ridding, M. C., & Nordstrom, M. A. (2008). Cortisol inhibits neuroplasticity induction in human motor cortex. Journal of Neuroscience, 28(33), 8285–8293.
Salerno, A., & Georgesco, M. (1998). Double magnetic stimulation of the motor cortex in amyotrophic lateral sclerosis. Electroencephalography and Clinical Neurophysiology, 107(2), 133–139.
Samarut, É., Swaminathan, A., Riché, R., Liao, M., Hassan‐Abdi, R., Renault, S., Allard, M., Dufour, L., Cossette, P., Soussi‐Yanicostas, N., & Drapeau, P. (2018). γ‐Aminobutyric acid receptor alpha 1 subunit loss of function causes genetic generalized epilepsy by impairing inhibitory network neurodevelopment. Epilepsia, 59(11), 2061–2074.
Sanes, J. N., & Donoghue, J. P. (2000). Plasticity and primary motor cortex. Annual Review of Neuroscience, 23, 393–415.
Sanger, T. D., Garg, R. R., & Chen, R. (2001). Interactions between two different inhibitory systems in the human motor cortex. The Journal of Physiology, 530(Pt 2), 307–317.
Solomon, J. A., Tarnopolsky, M. A., & Hamadeh, M. J. (2011). One universal common endpoint in mouse models of amyotrophic lateral sclerosis. PLoS One, 6(6), e20582.
Sotiropoulos, I., & Sousa, N. (2016). Tau as the converging protein between chronic stress and Alzheimer's disease synaptic pathology. Neurodegenerative Diseases, 16(1–2), 22–25.
Spataro, R., Volanti, P., Vitale, F., Meli, F., Colletti, T., Di Natale, A., & La Bella, V. (2015). Plasma cortisol level in amyotrophic lateral sclerosis. Journal of the Neurological Sciences, 358(1–2), 282–286.
Stengel, A., & Taché, Y. F. (2017). Activation of brain somatostatin signaling suppresses CRF receptor‐mediated stress response. Frontiers in Neuroscience, 11, 231.
Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J. I., Obata, K., & Kaneko, T. (2003). Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67‐GFP knock‐in mouse. Journal of Comparative Neurology, 467(1), 60–79.
Teleńczuk, B., Dehghani, N., Le Van Quyen, M., Cash, S. S., Halgren, E., Hatsopoulos, N. G., & Destexhe, A. (2017). Local field potentials primarily reflect inhibitory neuron activity in human and monkey cortex. Scientific Reports, 7, 40211.
Thomson, A. M. (2003). Interlaminar connections in the neocortex. Cerebral Cortex, 13(1), 5–14.
Tremblay, R., Lee, S., & Rudy, B. (2016). GABAergic interneurons in the neocortex: From cellular properties to circuits. Neuron, 91(2), 260–292.
Troncoso, J., Múnera, A., & Delgado‐García, J. M. (2007). Learning‐dependent potentiation in the vibrissal motor cortex is closely related to the acquisition of conditioned whisker responses in behaving mice. Learning & Memory (Cold Spring Harbor, N.Y.), 14(1), 84–93.
Tungtur, S. K., Wilkins, H. M., Rogers, R. S., Badawi, Y., Sage, J. M., Agbas, A., Jawdat, O., Barohn, R. J., Swerdlow, R. H., & Nishimune, H. (2021). Oxaloacetate treatment preserves motor function in SOD1G93A mice and normalizes select neuroinflammation‐related parameters in the spinal cord. Scientific Reports, 11(1), 11051.
van den Bos, M. A. J., Higashihara, M., Geevasinga, N., Menon, P., Kiernan, M. C., & Vucic, S. (2018). Imbalance of cortical facilitatory and inhibitory circuits underlies hyperexcitability in ALS. Neurology, 91(18), e1669–e1676.
van Versendaal, D., & Levelt, C. N. (2016). Inhibitory interneurons in visual cortical plasticity. Cellular and Molecular Life Sciences, 73(19), 3677–3691.
van Wamelen, D. J., Wan, Y. M., Ray Chaudhuri, K., & Jenner, P. (2020). Stress and cortisol in Parkinson's disease. In International review of neurobiology (pp. 131–156). Elsevier.
Vouimba, R. M., Yaniv, D., Diamond, D., & Richter‐Levin, G. (2004). Effects of inescapable stress on LTP in the amygdala versus the dentate gyrus of freely behaving rats. European Journal of Neuroscience, 19(7), 1887–1894.
Vucic, S., Cheah, B. C., & Kiernan, M. C. (2009). Defining the mechanisms that underlie cortical hyperexcitability in amyotrophic lateral sclerosis. Experimental Neurology, 220(1), 177–182.
Vucic, S., Nicholson, G. A., & Kiernan, M. C. (2008). Cortical hyperexcitability may precede the onset of familial amyotrophic lateral sclerosis. Brain, 131(Pt 6), 1540–1550.
Welniarz, Q., Dusart, I., & Roze, E. (2017). The corticospinal tract: Evolution, development, and human disorders: Corticospinal tract human disorders. Developmental Neurobiology, 77(7), 810–829.
Werhahn, K. J., Kunesch, E., Noachtar, S., Benecke, R., & Classen, J. (1999). Differential effects on motorcortical inhibition induced by blockade of GABA uptake in humans. The Journal of Physiology, 517(Pt 2), 591–597.
Wischnewski, M., & Schutter, D. (2015). Efficacy and time course of theta burst stimulation in healthy humans. Brain Stimulation, 8(4), 685–692.
Wu, C. W., Chiu, W. T., Hsieh, T. H., Hsieh, C. H., & Chen, J. J. J. (2018). Modulation of motor excitability by cortical optogenetic theta burst stimulation. PLoS ONE, 13(8), e0203333.
Xu, L., Anwyl, R., & Rowan, M. J. (1997). Behavioural stress facilitates the induction of long‐term depression in the hippocampus. Nature, 387(6632), 497–500.
Yamada, J., Furukawa, T., Ueno, S., Yamamoto, S., & Fukuda, A. (2007). Molecular basis for the GABAA receptor‐mediated tonic inhibition in rat somatosensory cortex. Cerebral Cortex, 17(8), 1782–1787.
Yang, J., Han, H., Cao, J., Li, L., & Xu, L. (2006). Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus, 16(5), 431–436.
Zhang, W., Zhang, L., Liang, B., Schroeder, D., Zhang, Z., Cox, G. A., Li, Y., & Lin, D. T. (2016). Hyperactive somatostatin interneurons contribute to excitotoxicity in neurodegenerative disorders. Nature Neuroscience, 19(4), 557–559.
Zheng, G., Zhang, X., Chen, Y., Zhang, Y., Luo, W., & Chen, J. (2007). Evidence for a role of GABAA receptor in the acute restraint stress‐induced enhancement of spatial memory. Brain Research, 1181, 61–73.

Auteurs

Zoé Mazurie (Z)

Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), CNRS, UMR 5287, University of Bordeaux, Bordeaux, France.

Pascal Branchereau (P)

Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), CNRS, UMR 5287, University of Bordeaux, Bordeaux, France.

Daniel Cattaert (D)

Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), CNRS, UMR 5287, University of Bordeaux, Bordeaux, France.

Nadia Henkous (N)

Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), CNRS, UMR 5287, University of Bordeaux, Bordeaux, France.

Catherine Savona-Baron (C)

Present address: BoRdeaux Institute of onCology (BRIC), INSERM U1312, University of Bordeaux, Bordeaux, France.

Rose-Marie Vouimba (RM)

Institut de Neurosciences Cognitives et Intégratives d'Aquitaine (INCIA), CNRS, UMR 5287, University of Bordeaux, Bordeaux, France.

Classifications MeSH