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Evidence for electrical synapses between neurons of the nucleus reticularis thalami in the adult brain in vitro

Published online by Cambridge University Press:  06 September 2007

Kate L. Blethyn ,
Stuart W. Hughes  and
Vincenzo Crunelli
Kate L. Blethyn
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, Cardiff, UK
Stuart W. Hughes
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, Cardiff, UK
Vincenzo Crunelli*
Affiliation:
School of Biosciences, Cardiff University, Museum Avenue, Cardiff, UK
*
Correspondence should be addressed to: V. Crunelli, School of Biosciences, Cardiff University, Museum Avenue, Cardiff CF10 3US, UK phone: +44 29 20874091 fax: +44 29 20874986 email: Crunelli@Cardiff.ac.uk
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Abstract

It has been demonstrated in juvenile rodents that the inhibitory neurons of the nucleus reticularis thalami (NRT) communicate with each other via connexin 36-based electrical synapses. However, whether functional electrical synapses persist into adulthood is not fully known. Here we show that in the presence of the metabotropic glutamate receptor agonists, either trans-ACPD (100 μM) or DHPG (100 μM), 15% of neurons in slices of the adult cat NRT maintained in vitro exhibit stereotypical spikelets with several properties that indicate that they reflect action potentials that have been communicated through an electrical synapse. In particular, these spikelets (1) display a conserved, all-or-nothing waveform with a pronounced after-hyperpolarization (AHP), (2) exhibit an amplitude and time to peak that are unaffected by changes in membrane potential, (3) always occur rhythmically with the precise frequency increasing with depolarization, and (4) are resistant to blockers of conventional, fast, chemical synaptic transmission. Thus, these results indicate that functional electrical synapses in the NRT persist into adulthood where they are likely to serve as an effective synchronizing mechanism for the wide variety of physiological and pathological rhythmic activities displayed by this nucleus.

Keywords

Gap junctionsconnexin36mGluRsEEG rhythmssleep spindles
Type
Original Articles
Information
Thalamus & Related Systems , Volume 4 , Issue 1 , March 2008 , pp. 13 - 20
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Amzica, F., Nunez, A. and Steriade, M. (1992) Delta frequency (1-4 Hz) oscillations of perigeniculate thalamic neurons and their modulation by light. Neuroscience 51, 285–294.CrossRefGoogle ScholarPubMed
Bal, T. and McCormick, D.A. (1993) Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. Journal of Physiology (London) 468, 669–691.CrossRefGoogle ScholarPubMed
Bal, T., von Krosigk, M. and McCormick, D.A. (1995) Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. Journal of Physiology (London) 483, 665–685.CrossRefGoogle ScholarPubMed
Belluardo, N., Mudo, G., Trovato-Salinaro, A., Le Gurun, S., Charollais, A., Serre-Beinier, V. et al. (2000) Expression of connexin36 in the adult and developing rat brain. Brain Research 865, 121–138.CrossRefGoogle ScholarPubMed
Blethyn, K.L., Hughes, S.W., Tóth, T.I., Cope, D.W. and Crunelli, V. (2006) Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. Journal of Neuroscience 26, 2474–2486.CrossRefGoogle ScholarPubMed
Condorelli, D.F., Belluardo, N., Trovato-Salinaro, A. and Mudo, G. (2000) Expression of Cx36 in mammalian neurons. Brain Research Brain Research Reviews 32, 72–85.CrossRefGoogle ScholarPubMed
Contreras, D., Curro Dossi, R. and Steriade, M. (1992) Bursting and tonic discharges in two classes of reticular thalamic neurons. Journal of Neurophysiology 68, 973–977.CrossRefGoogle ScholarPubMed
Contreras, D., Curro Dossi, R. and Steriade, M. (1993) Electrophysiological properties of cat reticular thalamic neurones in vivo. Journal of Physiology (London) 470, 273–294.CrossRefGoogle ScholarPubMed
Cox, C.L. and Sherman, S.M. (1999) Glutamate inhibits thalamic reticular neurons. Journal of Neuroscience 19, 6694–6699.CrossRefGoogle ScholarPubMed
Crunelli, V., Tóth, T.I., Cope, D.W., Blethyn, K. and Hughes, S.W. (2005) The ‘window’ T-type calcium current in brain dynamics of different behavioural states. Journal of Physiology 562, 121–129.CrossRefGoogle ScholarPubMed
Deleuze, C. and Huguenard, J.R. (2006) Distinct electrical and chemical connectivity maps in the thalamic reticular nucleus: potential roles in synchronization and sensation. Journal of Neuroscience 26, 8633–8645.CrossRefGoogle ScholarPubMed
Fuentealba, P., Crochet, S., Timofeev, I., Bazhenov, M., Sejnowski, T.J. and Steriade, M. (2004) Experimental evidence and modeling studies support a synchronizing role for electrical coupling in the cat thalamic reticular neurons in vivo. European Journal of Neuroscience 20, 111–119.CrossRefGoogle ScholarPubMed
Fuentealba, P. and Steriade, M. (2005) The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Progress in Neurobiology 75, 125–141.CrossRefGoogle ScholarPubMed
Galarreta, M. and Hestrin, S. (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72–75.CrossRefGoogle ScholarPubMed
Galarreta, M. and Hestrin, S. (2001) Electrical synapses between GABA-releasing interneurons. Nature Reviews Neuroscience 2, 425–433.CrossRefGoogle ScholarPubMed
Gareri, P., Condorelli, D., Belluardo, N., Citraro, R., Barresi, V., Trovato-Salinato, A. et al. (2005) Antiabsence effects of carbenoxolone in two genetic animal models of absence epilepsy (WAG/Rij rats and lh/lh mice). Neuropharmacology 49, 551–563.CrossRefGoogle ScholarPubMed
Gibson, J.R., Beierlein, M. and Connors, B.W. (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79.CrossRefGoogle ScholarPubMed
Hughes, S.W., Blethyn, K.L., Cope, D.W. and Crunelli, V. (2002) Properties and origin of spikelets in thalamocortical neurones in vitro. Neuroscience 110, 395–401.CrossRefGoogle ScholarPubMed
Hughes, S.W. and Crunelli, V. (2005) Hardwiring goes soft: long-term modulation of electrical synapses in the mammalian brain. Cellscience 2, 1–9.Google Scholar
Hughes, S.W., Lőrincz, M., Cope, D.W., Blethyn, K.L., Kekesi, K.A., Parri, H.R. et al. (2004) Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. Neuron 42, 253–268.CrossRefGoogle ScholarPubMed
Huntsman, M.M., Porcello, D.M., Homanics, G.E., DeLorey, T.M. and Huguenard, J.R. (1999) Reciprocal inhibitory connections and network synchrony in the mammalian thalamus. Science 283, 541–543.CrossRefGoogle ScholarPubMed
Lam, Y.W., Nelson, C.S. and Sherman, S.M. (2006) Mapping of the functional interconnections between reticular neurons using photostimulation. Journal of Neurophysiology 96, 2593–2600.CrossRefGoogle ScholarPubMed
Landisman, C.E. and Connors, B.W. (2005) Long-term modulation of electrical synapses in the mammalian thalamus. Science 310, 1809–1813.CrossRefGoogle ScholarPubMed
Landisman, C.E., Long, M.A., Beierlein, M., Deans, M.R., Paul, D.L. and Connors, B.W. (2002) Electrical synapses in the thalamic reticular nucleus. Journal of Neuroscience 22, 1002–1009.CrossRefGoogle ScholarPubMed
Liu, X.B. and Jones, E.G. (2003) Fine structural localization of connexin-36 immunoreactivity in mouse cerebral cortex and thalamus. Journal of Comparative Neurology 466, 457–467.CrossRefGoogle ScholarPubMed
Llinas, R. and Yarom, Y. (1981). Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. Journal of Physiology (London) 315, 549–567.CrossRefGoogle ScholarPubMed
Logan, S.D., Pickering, A.E., Gibson, I.C., Nolan, M.F. and Spanswick, D. (1996) Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. Journal of Physiology (London) 495, 491–502.CrossRefGoogle ScholarPubMed
Long, M.A., Landisman, C.E. and Connors, B.W. (2004) Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. Journal of Neuroscience 24, 341–349.CrossRefGoogle ScholarPubMed
Mulle, C., Madariaga, A. and Deschenes, M. (1986) Morphology and electrophysiological properties of reticularis thalami neurons in cat: in vivo study of a thalamic pacemaker. Journal of Neuroscience 6, 2134–2145.CrossRefGoogle ScholarPubMed
Proulx, E., Leshchenko, Y., Kokarovtseva, L., Khokhotva, V., El-Beheiry, M., Snead, O.C. 3rd et al. (2006) Functional contribution of specific brain areas to absence seizures: role of thalamic gap-junctional coupling. European Journal of Neuroscience 23, 489–496.CrossRefGoogle ScholarPubMed
Slaght, S.J., Leresche, N., Deniau, J.M., Crunelli, V. and Charpier, S. (2002) Activity of thalamic reticular neurons during spontaneous genetically determined spike and wave discharges. Journal of Neuroscience 22, 2323–2334.CrossRefGoogle ScholarPubMed
Sohal, V.S., Huntsman, M.M. and Huguenard, J.R. (2000) Reciprocal inhibitory connections regulate the spatiotemporal properties of intrathalamic oscillations. Journal of Neuroscience 20, 1735–1745.CrossRefGoogle ScholarPubMed
Steriade, M. (2005) Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends in Neurosciences 28, 317–324.CrossRefGoogle ScholarPubMed
Steriade, M. and Contreras, D. (1995) Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. Journal of Neuroscience 15, 623–642.CrossRefGoogle ScholarPubMed
Steriade, M., Contreras, D., Curro Dossi, R. and Nunez, A. (1993) The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks. Journal of Neuroscience 13, 3284–3299.CrossRefGoogle ScholarPubMed
Steriade, M., Deschenes, M., Domich, L. and Mulle, C. (1985) Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. Journal of Neurophysiology 54, 1473–1497.CrossRefGoogle ScholarPubMed
Steriade, M., Domich, L., Oakson, G. and Deschenes, M. (1987) The deafferented reticular thalamic nucleus generates spindle rhythmicity. Journal of Neurophysiology 57, 260–273.CrossRefGoogle ScholarPubMed
Uhlrich, D.J., Cucchiaro, J.B., Humphrey, A.L. and Sherman, S.M. (1991) Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. Journal of Neurophysiology 65, 1528–1541.CrossRefGoogle ScholarPubMed
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D. and Monyer, H. (2000). Connexin expression in electrically coupled postnatal rat brain neurons. Proceedings of the National Academy of Science of the U.S.A. 97, 10260–10265.CrossRefGoogle ScholarPubMed
von Krosigk, M., Bal, T. and McCormick, D.A. (1993) Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261, 361–364.CrossRefGoogle ScholarPubMed