Atypical electrophysiological and behavioral responses to diazepam in a leading mouse model of Down syndrome.
Animals
Diazepam
/ pharmacology
Disease Models, Animal
Down Syndrome
/ drug therapy
Electrophysiological Phenomena
/ drug effects
Female
Long-Term Potentiation
/ drug effects
Male
Maze Learning
/ drug effects
Memory Disorders
/ drug therapy
Mice
Mice, Inbred C57BL
Neuronal Plasticity
/ drug effects
Picrotoxin
/ pharmacology
Seizures
/ chemically induced
Synaptic Transmission
/ drug effects
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
04 05 2021
04 05 2021
Historique:
received:
26
01
2021
accepted:
15
04
2021
entrez:
5
5
2021
pubmed:
6
5
2021
medline:
2
2
2023
Statut:
epublish
Résumé
Mounting evidence implicates dysfunctional GABA
Identifiants
pubmed: 33947925
doi: 10.1038/s41598-021-89011-y
pii: 10.1038/s41598-021-89011-y
pmc: PMC8096846
doi:
Substances chimiques
Picrotoxin
124-87-8
Diazepam
Q3JTX2Q7TU
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9521Références
Mai, C. T. et al. National population-based estimates for major birth defects, 2010–2014. Birth Defects Res. 111, 1420–1435 (2019).
pubmed: 31580536
pmcid: 7203968
doi: 10.1002/bdr2.1589
Basten, I.A., et al. On the design of broad-based neuropsychological test batteries to assess the cognitive abilities of individuals with down syndrome in the context of clinical trials. Brain Sci. 8, 205. https://doi.org/10.3390/brainsci8120205 (2018).
doi: 10.3390/brainsci8120205
pmcid: 6315396
Nadel, L. Down’s syndrome: A genetic disorder in biobehavioral perspective. Genes Brain Behav. 2, 156–166 (2003).
pubmed: 12931789
doi: 10.1034/j.1601-183X.2003.00026.x
Aller-Alvarez, J. S. et al. Myoclonic epilepsy in Down syndrome and Alzheimer disease. Neurologia 32, 69–73 (2017).
pubmed: 25661268
doi: 10.1016/j.nrl.2014.12.008
Foley, K. R. et al. Patterns of depressive symptoms and social relating behaviors differ over time from other behavioral domains for young people with Down syndrome. Medicine (Baltimore) 94, e710 (2015).
doi: 10.1097/MD.0000000000000710
Robertson, J., Hatton, C., Emerson, E. & Baines, S. Prevalence of epilepsy among people with intellectual disabilities: A systematic review. Seizure 29, 46–62 (2015).
pubmed: 26076844
doi: 10.1016/j.seizure.2015.03.016
Vicari, S., Pontillo, M. & Armando, M. Neurodevelopmental and psychiatric issues in Down’s syndrome: Assessment and intervention. Psychiatr. Genet. 23, 95–107 (2013).
pubmed: 23492931
doi: 10.1097/YPG.0b013e32835fe426
Arya, R., Kabra, M. & Gulati, S. Epilepsy in children with Down syndrome. Epileptic Disord. 13, 1–7 (2011).
pubmed: 21398208
doi: 10.1684/epd.2011.0415
Vignoli, A. et al. Epilepsy in adult patients with Down syndrome: A clinical-video EEG study. Epileptic Disord. 13, 125–132 (2011).
pubmed: 21561839
doi: 10.1684/epd.2011.0426
Tasse, M. J. et al. Psychiatric conditions prevalent among adults with down syndrome. J. Policy Pract. Intel. 13, 173–180 (2016).
Kleschevnikov, A. M. et al. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 24, 8153–8160 (2004).
pubmed: 15371516
pmcid: 6729789
doi: 10.1523/JNEUROSCI.1766-04.2004
Costa, A. C. & Grybko, M. J. Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: A model of Down syndrome. Neurosci. Lett. 382, 317–322 (2005).
pubmed: 15925111
doi: 10.1016/j.neulet.2005.03.031
Scott-McKean, J. J. et al. Pharmacological modulation of three modalities of CA1 hippocampal long-term potentiation in the Ts65Dn mouse model of down syndrome. Neural. Plast. 2018, 9235796 (2018).
pubmed: 29849573
pmcid: 5914153
doi: 10.1155/2018/9235796
Fernandez, F. et al. Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 10, 411–413 (2007).
pubmed: 17322876
doi: 10.1038/nn1860
Monash University. Down syndrome trial may hold key to learning. http://compose21.com/study.htm (2013).
NCT01436955. A study of RG1662 in individuals with down syndrome. https://clinicaltrials.gov/ct2/show/NCT01436955 (2011).
NCT02024789. A multi-center, randomized, double-blind, placebo-controlled phase 2 study of the efficacy, safety and tolerability of Rg1662 in adults and adolescents with down syndrome (CLEMATIS). https://clinicaltrials.gov/ct2/show/NCT02024789 (2013).
Deidda, G. et al. Reversing excitatory GABAAR signaling restores synaptic plasticity and memory in a mouse model of Down syndrome. Nat. Med. 21, 318–326 (2015).
pubmed: 25774849
doi: 10.1038/nm.3827
Sigel, E. & Ernst, M. The benzodiazepine binding sites of GABAA receptors. Trends Pharmacol. Sci. 39, 659–671 (2018).
pubmed: 29716746
doi: 10.1016/j.tips.2018.03.006
Costa, A. C. Intracellular chloride accumulation: A possible mechanism for cognitive deficits in Down syndrome. Nat. Med. 21, 312–313 (2015).
pubmed: 25849271
doi: 10.1038/nm.3836
Miles, J. H., Takahashi, N., Muckerman, J., Nowell, K. P. & Ithman, M. Catatonia in Down syndrome: Systematic approach to diagnosis, treatment and outcome assessment based on a case series of seven patients. Neuropsychiatr. Dis. Treat 15, 2723–2741 (2019).
pubmed: 31571888
pmcid: 6759875
doi: 10.2147/NDT.S210613
Schulte, J. T., Wierenga, C. J. & Bruining, H. Chloride transporters and GABA polarity in developmental, neurological and psychiatric conditions. Neurosci. Biobehav. Rev. 90, 260–271 (2018).
pubmed: 29729285
doi: 10.1016/j.neubiorev.2018.05.001
Jongsma, M. L. et al. The influence of diazepam on the electroencephalogram-evoked potential interrelation in rats. Neurosci. Lett. 293, 83–86 (2000).
pubmed: 11027839
doi: 10.1016/S0304-3940(00)01496-8
van Lier, H., Drinkenburg, W. H., van Eeten, Y. J. & Coenen, A. M. Effects of diazepam and zolpidem on EEG beta frequencies are behavior-specific in rats. Neuropharmacology 47, 163–174 (2004).
pubmed: 15223295
doi: 10.1016/j.neuropharm.2004.03.017
Saletu, B., Anderer, P. & Saletu-Zyhlarz, G. M. EEG topography and tomography (LORETA) in the classification and evaluation of the pharmacodynamics of psychotropic drugs. Clin. EEG Neurosci. 37, 66–80 (2006).
pubmed: 16733939
doi: 10.1177/155005940603700205
Gilles, C. & Luthringer, R. Pharmacological models in healthy volunteers: Their use in the clinical development of psychotropic drugs. J. Psychopharmacol. 21, 272–282 (2007).
pubmed: 17591655
doi: 10.1177/0269881107077733
Center for Drug Evaluation and Research (CDER). Guidance for industry: Estimating the maximum safe starting dose in initial clinical trials for therapeutics in adult healthy volunteers. https://www.fda.gov/media/72309/download (2005).
Hoffmann-La Roche. Valium. https://www.accessdata.fda.gov/drugsatfda_docs/label/2016/013263s094lbl.pdf (2016).
Fell, J. & Axmacher, N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011).
pubmed: 21248789
doi: 10.1038/nrn2979
Van Erum, J., Van Dam, D. & De Deyn, P. P. PTZ-induced seizures in mice require a revised Racine scale. Epilepsy Behav. 95, 51–55 (2019).
pubmed: 31026782
doi: 10.1016/j.yebeh.2019.02.029
Chapman, C. A., Perez, Y. & Lacaille, J. C. Effects of GABA(A) inhibition on the expression of long-term potentiation in CA1 pyramidal cells are dependent on tetanization parameters. Hippocampus 8, 289–298 (1998).
pubmed: 9662142
doi: 10.1002/(SICI)1098-1063(1998)8:3<289::AID-HIPO10>3.0.CO;2-X
Wigstrom, H. & Gustafsson, B. Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301, 603–604 (1983).
pubmed: 6298626
doi: 10.1038/301603a0
Dailly, E., Hascoet, M., Colombel, M. C., Jolliet, P. & Bourin, M. Relationship between cerebral pharmacokinetics and anxiolytic activity of diazepam and its active metabolites after a single intra-peritoneal administration of diazepam in mice. Hum. Psychopharmacol. 17, 239–245 (2002).
pubmed: 12404681
doi: 10.1002/hup.408
Hofmann, J.I., Schwarz, C., Rudolph, U., Antkowiak, B. Effects of diazepam on low-frequency and high-frequency electrocortical gamma-power mediated by alpha1- and alpha2-GABAA receptors. Int. J. Mol. Sci. 20, 3486. https://doi.org/10.3390/ijms20143486 (2019).
doi: 10.3390/ijms20143486
pmcid: 6678188
Christian, E. P. et al. EEG-beta/gamma spectral power elevation in rat: a translatable biomarker elicited by GABA(Aalpha2/3)-positive allosteric modulators at nonsedating anxiolytic doses. J. Neurophysiol. 113, 116–131 (2015).
pubmed: 25253471
doi: 10.1152/jn.00539.2013
Rijn, C. M., Jongsma, M. Chronic effects of diazepam on the spectral content of the rat EEG. Neurosci. Res. Commun. 17, 65–69 (1995).
Jensen, O. et al. On the human sensorimotor-cortex beta rhythm: Sources and modeling. Neuroimage 26, 347–355 (2005).
pubmed: 15907295
doi: 10.1016/j.neuroimage.2005.02.008
Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203–225 (2012).
pubmed: 22443509
pmcid: 4049541
doi: 10.1146/annurev-neuro-062111-150444
Whittington, M. A., Traub, R. D., Kopell, N., Ermentrout, B. & Buhl, E. H. Inhibition-based rhythms: Experimental and mathematical observations on network dynamics. Int. J. Psychophysiol. 38, 315–336 (2000).
pubmed: 11102670
doi: 10.1016/S0167-8760(00)00173-2
Faulkner, H. J., Traub, R. D. & Whittington, M. A. Disruption of synchronous gamma oscillations in the rat hippocampal slice: A common mechanism of anaesthetic drug action. Br. J. Pharmacol. 125, 483–492 (1998).
pubmed: 9806331
pmcid: 1565655
doi: 10.1038/sj.bjp.0702113
Cramer, N.P., Xu, X., T, F. H., Galdzicki, Z. Altered intrinsic and network properties of neocortical neurons in the Ts65Dn mouse model of down syndrome. Physiol. Rep. 3, e12655. https://doi.org/10.14814/phy12652.12655 (2015).
doi: 10.14814/phy12652.12655
pubmed: 26702072
pmcid: 4760451
Luczak, A., Bartho, P., Marguet, S. L., Buzsaki, G. & Harris, K. D. Sequential structure of neocortical spontaneous activity in vivo. Proc. Natl. Acad. Sci. USA 104, 347–352 (2007).
pubmed: 17185420
doi: 10.1073/pnas.0605643104
Kuki, T. et al. Contribution of parvalbumin and somatostatin-expressing GABAergic neurons to slow oscillations and the balance in beta-gamma oscillations across cortical layers. Front. Neural Circ. 9, 6 (2015).
Brown, K. N. et al. Clonal production and organization of inhibitory interneurons in the neocortex. Science 334, 480–486 (2011).
pubmed: 22034427
pmcid: 3304494
doi: 10.1126/science.1208884
Sanchez-Vives, M. V. et al. Inhibitory modulation of cortical up states. J. Neurophysiol. 104, 1314–1324 (2010).
pubmed: 20554835
doi: 10.1152/jn.00178.2010
Chakrabarti, L. et al. Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome. Nat. Neurosci. 13, 927–934 (2010).
pubmed: 20639873
pmcid: 3249618
doi: 10.1038/nn.2600
Perez-Cremades, D. et al. Alteration of inhibitory circuits in the somatosensory cortex of Ts65Dn mice, a model for Down’s syndrome. J. Neural. Transm. (Vienna) 117, 445–455 (2010).
doi: 10.1007/s00702-010-0376-9
Zorrilla de San Martin, J. et al. Alterations of specific cortical GABAergic circuits underlie abnormal network activity in a mouse model of Down syndrome. Elife 9, e58731 https://doi.org/10.57554/eLife.58731 (2020).
doi: 10.57554/eLife.58731
pubmed: 32783810
pmcid: 7481006
Dierssen, M. Down syndrome: The brain in trisomic mode. Nat. Rev. Neurosci. 13, 844–858 (2012).
pubmed: 23165261
doi: 10.1038/nrn3314
Lysenko, L. V. et al. Developmental excitatory-to-inhibitory GABA polarity switch is delayed in Ts65Dn mice, a genetic model of Down syndrome. Neurobiol. Dis. 115, 1–8 (2018).
pubmed: 29550538
doi: 10.1016/j.nbd.2018.03.005
Ali, A. B. & Thomson, A. M. Synaptic alpha 5 subunit-containing GABAA receptors mediate IPSPs elicited by dendrite-preferring cells in rat neocortex. Cereb. Cortex 18, 1260–1271 (2008).
pubmed: 17951598
doi: 10.1093/cercor/bhm160
Braudeau, J. et al. Specific targeting of the GABA-A receptor alpha5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J. Psychopharmacol. 25, 1030–1042 (2011).
pubmed: 21693554
pmcid: 3160204
doi: 10.1177/0269881111405366
Schulz, J. M., Knoflach, F., Hernandez, M. C. & Bischofberger, J. Enhanced dendritic inhibition and impaired NMDAR activation in a mouse model of Down Syndrome. J. Neurosci. 39, 5210–5221 (2019).
pubmed: 31000585
pmcid: 6595955
doi: 10.1523/JNEUROSCI.2723-18.2019
Duchon, A. et al. Long-lasting correction of in vivo LTP and cognitive deficits of mice modelling Down syndrome with an alpha5-selective GABAA inverse agonist. Br. J. Pharmacol. 177, 1106–1118 (2020).
pubmed: 31652355
pmcid: 7042104
doi: 10.1111/bph.14903
Martinez-Cue, C., Delatour, B. & Potier, M. C. Treating enhanced GABAergic inhibition in Down syndrome: Use of GABA alpha5-selective inverse agonists. Neurosci. Biobehav. Rev. 46(Pt 2), 218–227 (2014).
pubmed: 24412222
doi: 10.1016/j.neubiorev.2013.12.008
Canolty, R. T. & Knight, R. T. The functional role of cross-frequency coupling. Trends Cogn. Sci. 14, 506–515 (2010).
pubmed: 20932795
pmcid: 3359652
doi: 10.1016/j.tics.2010.09.001
Jensen, O. & Colgin, L. L. Cross-frequency coupling between neuronal oscillations. Trends Cogn. Sci. 11, 267–269 (2007).
pubmed: 17548233
doi: 10.1016/j.tics.2007.05.003
Scheffzuk, C. et al. Global slowing of network oscillations in mouse neocortex by diazepam. Neuropharmacology 65, 123–133 (2013).
pubmed: 23063689
doi: 10.1016/j.neuropharm.2012.09.014
Alemany-Gonzalez, M. et al. Prefrontal-hippocampal functional connectivity encodes recognition memory and is impaired in intellectual disability. Proc. Natl. Acad. Sci. USA 117, 11788–11798 (2020).
pubmed: 32393630
doi: 10.1073/pnas.1921314117
pmcid: 7261130
Lister, R. G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92, 180–185 (1987).
pubmed: 3110839
doi: 10.1007/BF00177912
Coussons-Read, M. E. & Crnic, L. S. Behavioral assessment of the Ts65Dn mouse, a model for Down syndrome: Altered behavior in the elevated plus maze and open field. Behav. Genet. 26, 7–13 (1996).
pubmed: 8852727
doi: 10.1007/BF02361154
Vicari, S. & Carlesimo, G. A. Short-term memory deficits are not uniform in Down and Williams syndromes. Neuropsychol. Rev. 16, 87–94 (2006).
pubmed: 16967345
doi: 10.1007/s11065-006-9008-4
Dowdy-Sanders, N. C. & Wenger, G. R. Working memory in the Ts65Dn mouse, a model for Down syndrome. Behav. Brain Res. 168, 349–352 (2006).
pubmed: 16386318
doi: 10.1016/j.bbr.2005.11.020
Driscoll, L. L. et al. Impaired sustained attention and error-induced stereotypy in the aged Ts65Dn mouse: A mouse model of Down syndrome and Alzheimer’s disease. Behav. Neurosci. 118, 1196–1205 (2004).
pubmed: 15598129
doi: 10.1037/0735-7044.118.6.1196
Hunter, C. L., Bimonte, H. A. & Granholm, A. C. Behavioral comparison of 4 and 6 month-old Ts65Dn mice: Age-related impairments in working and reference memory. Behav. Brain Res. 138, 121–131 (2003).
pubmed: 12527443
doi: 10.1016/S0166-4328(02)00275-9
Blanchard, D. C., Griebel, G. & Blanchard, R. J. Mouse defensive behaviors: Pharmacological and behavioral assays for anxiety and panic. Neurosci. Biobehav. Rev. 25, 205–218 (2001).
pubmed: 11378177
doi: 10.1016/S0149-7634(01)00009-4
Griffin, C. E. 3rd., Kaye, A. M., Bueno, F. R. & Kaye, A. D. Benzodiazepine pharmacology and central nervous system-mediated effects. Ochsner J 13, 214–223 (2013).
pubmed: 23789008
pmcid: 3684331
Duchon, A. et al. Identification of the translocation breakpoints in the Ts65Dn and Ts1Cje mouse lines: Relevance for modeling Down syndrome. Mamm. Genome 22, 674–684 (2011).
pubmed: 21953411
pmcid: 3224224
doi: 10.1007/s00335-011-9356-0
Paxinos, G., Keith, B. J. & Franklin, M. The Mouse Brain in Stereotaxic Coordinates (Elsevier Science, 2007).
Billimoria, R. B., Naik, P. R. & Satoskar, R. S. Effect of diazepam alone and in combination with chlorpromazine or propranolol in experimentally induced convulsions in mice. J. Postgrad.Med. 27, 73–79 (1981).
pubmed: 7277251
Himmel, H. M. Safety pharmacology assessment of central nervous system function in juvenile and adult rats: Effects of pharmacological reference compounds. J. Pharmacol. Toxicol. Methods 58, 129–146 (2008).
pubmed: 18585470
doi: 10.1016/j.vascn.2008.06.001
Buzsáki, G. Rhythms of the Brain (Oxford University Press, 2006).
doi: 10.1093/acprof:oso/9780195301069.001.0001
Kay, S. M. Modern Spectral Estimation: Theory and Application (Prentice-Hall, 1988).
Gonzalez Burgos, G. R., Biali, F. I., Nicola Siri, L. C. & Cardinali, D. P. Effect of gamma-aminobutyric acid on synaptic transmission and long-term potentiation in rat superior cervical ganglion. Brain Res. 658, 1–7 (1994).
pubmed: 7834329
doi: 10.1016/S0006-8993(09)90002-6
Hirai, H., Tomita, H. & Okada, Y. Inhibitory effect of GABA (gamma-aminobutyric acid) on the induction of long-term potentiation in guinea pig superior colliculus slices. Neurosci. Lett. 149, 198–200 (1993).
pubmed: 8386349
doi: 10.1016/0304-3940(93)90770-L
del Cerro, S., Jung, M. & Lynch, G. Benzodiazepines block long-term potentiation in slices of hippocampus and piriform cortex. Neuroscience 49, 1–6 (1992).
pubmed: 1407540
doi: 10.1016/0306-4522(92)90071-9
Higashima, M., Kinoshita, H. & Koshino, Y. Differences in the effects of zolpidem and diazepam on recurrent inhibition and long-term potentiation in rat hippocampal slices. Neurosci. Lett. 245, 77–80 (1998).
pubmed: 9605489
doi: 10.1016/S0304-3940(98)00178-5
Zhu, P. J. et al. Suppression of PKR promotes network excitability and enhanced cognition by interferon-gamma-mediated disinhibition. Cell 147, 1384–1396 (2011).
pubmed: 22153080
pmcid: 3569515
doi: 10.1016/j.cell.2011.11.029
Rodriguez, A. et al. ToxTrac: A fast and robust software for tracking organisms. Methods Ecol. Evol. 9, 460–464 (2018).
doi: 10.1111/2041-210X.12874