View More View Less
  • 1 Department of Physiology, Tehran, Iran
  • 2 Department of Neuroscience, Tehran, Iran
Restricted access

Purchase article

USD  $25.00

1 year subscription (Individual Only)

USD  $752.00

Abstract

Introduction

During mammalian brain development, neural activity leads to maturation of glutamatergic innervations to locus coeruleus. In this study, fast excitatory postsynaptic currents mediated by N-methyl-d-aspartate (NMDA) receptors were evaluated to investigate the maturation of excitatory postsynaptic currents in locus coeruleus (LC) neurons.

Methods

NMDA receptor-mediated synaptic currents in LC neurons were evaluated using whole-cell voltage-clamp recording during the primary postnatal weeks. This technique was used to calculate the optimum holding potential for NMDA receptor-mediated currents and the best frequency for detecting spontaneous excitatory postsynaptic currents (sEPSC).

Results

The optimum holding potential for detecting NMDA receptor-mediated currents was + 40 to + 50 mV in LC neurons. The frequency, amplitude, rise time, and decay time constant of synaptic responses depended on the age of the animal and increased during postnatal maturation.

Conclusion

These findings suggest that most nascent glutamatergic synapses express functional NMDA receptors in the postnatal coerulear neurons, and that the activities of the neurons in this region demonstrate an age-dependent variation.

  • 1.

    Arami MK, Hajizadeh S, Semnanian S. Postnatal development changes in excitatory synaptic activity in the rat locus coeruleus neurons. Brain Res 2016; 1648: 36571, https://doi.org/10.1016/j.brainres.2016.07.036.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    Arami MK, Semnanian S, Javan M, Hajizadeh S, Sarihi A. Postnatal developmental alterations in the locus coeruleus neuronal fast excitatory postsynaptic currents mediated by ionotropic glutamate receptors of rat. Physiol Pharmacolog 2011; 14: 33748.

    • Search Google Scholar
    • Export Citation
  • 3.

    Arami MK, Sohya K, Sarihi A, Jiang B, Yanagawa Y, Tsumoto T. Reciprocal homosynaptic and heterosynaptic long-term plasticity of corticogeniculate projection neurons in layer VI of the mouse visual cortex. J Neurosci 2013; 33: 778798, https://doi.org/10.1523/JNEUROSCI.5350-12.2013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4.

    Aston-Jones G, Shipley M, Chouvet G, Ennis M, Van Bockstaele E, Pieribone V, . Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology. Prog Brain Res 1991; 88: 4775, https://doi.org/10.1016/S0079-6123(08)63799-1.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Bardoni R, Magherini PC, MacDermott AB. NMDA EPSCs at glutamatergic synapses in the spinal cord dorsal horn of the postnatal rat. J Neurosci 1998; 18: 655867, https://doi.org/10.1523/JNEUROSCI.18-16-06558.1998.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Bekkers JM, Clements JD. Quantal amplitude and quantal variance of strontium‐induced asynchronous EPSCs in rat dentate granule neurons. J Physiol 1999; 516: 22748, https://doi.org/10.1111/j.1469-7793.1999.227aa.x.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Bottjer SW. Silent synapses in a thalamo-cortical circuit necessary for song learning in zebra finches. J Neurophysiol 2005; 94: 3698707, https://doi.org/10.1152/jn.00282.2005.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8.

    Burgard EC, Hablitz JJ. NMDA receptor-mediated components of miniature excitatory synaptic currents in developing rat neocortex. J Neurophysiol 1993; 70: 184152, https://doi.org/10.1152/jn.1993.70.5.1841.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001; 11: 32735, https://doi.org/10.1016/S0959-4388(00)00215-4.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    de Armentia ML, Sah P. Development and subunit composition of synaptic NMDA receptors in the amygdala: NR2B synapses in the adult central amygdala. J Neurosci 2003; 23: 687683, https://doi.org/10.1523/JNEUROSCI.23-17-06876.2003.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Friedman D, Strowbridge BW. Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 2000; 84: 3950, https://doi.org/10.1152/jn.2000.84.1.39.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Friedman HV, Bresler T, Garner CC, Ziv NE. Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 2000; 27: 5769, https://doi.org/10.1016/S0896-6273(00)00009-X.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Gasparini S, Saviane C, Voronin LL, Cherubini E. Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc Natl Acad Sci U S A 2000; 97: 974146, https://doi.org/10.1073/pnas.170032297.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Hsia AY, Malenka RC, Nicoll RA. Development of excitatory circuitry in the hippocampus. J Neurophysiol 1998; 79: 201324, https://doi.org/10.1152/jn.1998.79.4.2013.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Hsieh CY, Chen Y, Leslie FM, Metherate R. Postnatal development of NR2A and NR2B mRNA expression in rat auditory cortex and thalamus. J Assoc Res Otolaryngol 2002; 3: 47987, https://doi.org/10.1007/s1016200220528.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Ishibashi H, Nakahata Y, Eto K, Nabekura J. Excitation of locus coeruleus noradrenergic neurons by thyrotropin‐releasing hormone. J Physiol 2009; 587: 570922, https://doi.org/10.1113/jphysiol.2009.181420.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Ishimatsu M, Williams JT. Synchronous activity in locus coeruleus results from dendritic interactions in pericoerulear regions. J Neurosci 1996; 16: 5196204, https://doi.org/10.1523/JNEUROSCI.16-16-05196.1996.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Keller B, Konnerth A, Yaari Y. Patch clamp analysis of excitatory synaptic currents in granule cells of rat hippocampus. J Physiol 1991; 435: 27593, https://doi.org/10.1113/jphysiol.1991.sp018510.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Kirson ED, Yaari Y. Synaptic NMDA receptors in developing mouse hippocampal neurones: functional properties and sensitivity to ifenprodil. J Physiol 1996; 497: 43755, https://doi.org/10.1113/jphysiol.1996.sp021779.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Koga H, Ishibashi H, Shimada H, Jang I-S, Nakamura TY, Nabekura J. Activation of presynaptic GABA A receptors increases spontaneous glutamate release onto noradrenergic neurons of the rat locus coeruleus. Brain Res 2005; 1046: 2431, https://doi.org/10.1016/j.brainres.2005.03.026.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Koike-Tani M, Saitoh N, Takahashi T. Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J Neurosci 2005; 25: 199207, https://doi.org/10.1523/JNEUROSCI.3861-04.2005.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Komaki A, Shahidi S, Sarihi A, Hasanein P, Lashgari R, Haghparast A, . Effects of neonatal C-fiber depletion on interaction between neocortical short-term and long-term plasticity. Basic Clin Neurosci 2013; 4: 13645.

    • Search Google Scholar
    • Export Citation
  • 23.

    Kourosh Arami M, Sarihi A, Malacoti SM, Behzadi G, Vahabian M, Amiri I. The effect of nucleus tractus solitarius nitric oxidergic neurons on blood pressure in diabetic rats. Iran Biomed J 2006; 10: 159.

    • Search Google Scholar
    • Export Citation
  • 24.

    López‐Gallardo M, Prada C. Spatial and temporal patterns of morphogenesis of hippocampal pyramidal cells: study in the early postnatal rat. Hippocampus 2001; 11: 11831, https://doi.org/10.1002/hipo.1030.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Malenka RC, Nicoll RA. Long-term potentiation–a decade of progress? Science 1999; 285: 187074, https://doi.org/10.1126/science.285.5435.1870.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26.

    Marinelli S, Vaughan CW, Christie MJ, Connor M. Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. J Physiol 2002; 543: 53140, https://doi.org/10.1126/science.285.5435.1870.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Masaki E, Kawamura M, Kato F. Attenuation of gap-junction-mediated signaling facilitated anesthetic effect of sevoflurane in the central nervous system of rats. Anesth Analg 2004; 98: 64752, https://doi.org/10.1213/01.ANE.0000103259.72635.72.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Mayer ML, Westbrook GL, Guthrie PB. Voltage-dependent block by Mg 2+ of NMDA responses in spinal cord neurones. Nature 1984; 309: 26163, https://doi.org/10.1038/309261a0.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Mori H, Mishina M. Structure and function of the NMDA receptor channel. Neuropharmacology 1995; 34: 121937, https://doi.org/10.1016/0028-3908(95)00109-J.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30.

    Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature 1991; 354: 317, https://doi.org/10.1038/354031a0.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Myme CI, Sugino K, Turrigiano GG, Nelson SB. The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J Neurophysiol 2003; 90: 77179, https://doi.org/10.1152/jn.00070.2003.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 1984; 307: 46265, https://doi.org/10.1038/307462a0.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33.

    Oswald A-MM, Reyes AD. Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J Neurophysiol 2008; 99: 29983008, https://doi.org/10.1152/jn.01160.2007.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Paxinos G, Franklin KB. The mouse brain in stereotaxic coordinates. Oxford, UK: Gulf Professional Publishing; 2004.

  • 35.

    Prè D, Nestor MW, Sproul AA, Jacob S, Koppensteiner P, Chinchalongporn V, . A time course analysis of the electrophysiological properties of neurons differentiated from human induced pluripotent stem cells (iPSCs). PLoS One 2014; 9: e103418, https://doi.org/10.1371/journal.pone.0103418.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Rao H, Jean A, Kessler J-P. Postnatal ontogeny of glutamate receptors in the rat nucleus tractus solitarii and ventrolateral medulla. J Auton Nerv Syst 1997; 65: 2532, https://doi.org/10.1016/S0165-1838(97)00031-3.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Renger JJ, Egles C, Liu G. A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 2001; 29: 46984, https://doi.org/10.1016/S0896-6273(01)00219-7.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Sarihi A, Mirnajafi-Zadeh J, Jiang B, Sohya K, Safari M-S, Arami MK, . Cell type-specific, presynaptic LTP of inhibitory synapses on fast-spiking GABAergic neurons in the mouse visual cortex. J Neurosci 2012; 32: 1318999, https://doi.org/10.1523/JNEUROSCI.1386-12.2012.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Van Bockstaele EJ, Colago EE, Aicher S. Light and electron microscopic evidence for topographic and monosynaptic projections from neurons in the ventral medulla to noradrenergic dendrites in the rat locus coeruleus. Brain Res 1998; 784: 12338, https://doi.org/10.1016/S0006-8993(97)01250-X.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Wang H-X, Gao W-J. Cell type-specific development of NMDA receptors in the interneurons of rat prefrontal cortex. Neuropsychopharmacology 2009; 34: 202840, https://doi.org/10.1038/npp.2009.20.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Watt AJ, van Rossum MC, MacLeod KM, Nelson SB, Turrigiano GG. Activity coregulates quantal AMPA and NMDA currents at neocortical synapses. Neuron 2000; 26: 65970, https://doi.org/10.1016/S0896-6273(00)81202-7.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 42.

    Williams J, North R, Shefner S, Nishi S, Egan T. Membrane properties of rat locus coeruleus neurones. Neuroscience 1984; 13: 13756, https://doi.org/10.1016/0306-4522(84)90265-3.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 43.

    Wuarin J-P, Dudek FE. Patch-clamp analysis of spontaneous synaptic currents in supraoptic neuroendocrine cells of the rat hypothalamus. J Neurosci 1993; 13: 232331, https://doi.org/10.1523/JNEUROSCI.13-06-02323.1993.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 44.

    Ye G-l, Yi S, Gamkrelidze G, Pasternak JF, Trommer BL. AMPA and NMDA receptor-mediated currents in developing dentate gyrus granule cells. Brain Res Dev Brain Res 2005; 155: 2632, https://doi.org/10.1016/j.devbrainres.2004.12.002.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Zhang L, Bose P, Warren RA. Dopamine preferentially inhibits NMDA receptor-mediated EPSCs by acting on presynaptic D1 receptors in nucleus accumbens during postnatal development. PLoS One 2014; 9: e86970, https://doi.org/10.1371/journal.pone.0086970.

    • Search Google Scholar
    • Export Citation
  • 46.

    Rezaei Z, Kourosh-Arami M, Azizi H, Semnanian S. Orexin type-1 receptor inhibition in the rat lateral paragigantocellularis nucleus attenuates development of morphine dependence. Neurosci Lett 2020, https://doi.org/10.1016/j.neulet.2020.134875.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Arami MK, Zade JM, Komaki A, Amiri M, Mehrpooya S, Jahanshahi A, . Nitric oxide in the nucleus raphe magnus modulates cutaneous blood flow in rats during hypothermia. Iran J Basic Med Sci 2015; 18: 989992.

    • Search Google Scholar
    • Export Citation