Altered synaptic and electrical properties of lumbar motoneurons in the neurological glial mutant taiep rat
Tóm tắt
Maturation and differentiation of electrical properties of neurons and synaptic transmission are modulated by neuronal interaction. In vitro experiments have shown that these processes also seem to be regulated by signals from non-neuronal elements such as glial cells. It is not known, however, whether glial alterations in intact neural networks may also affect the maturation of electrical properties and synaptic transmission during development. We used the taiep rat, a neurological mutant with a progressive demyelination and astrogliosis, as an experimental model to study the postnatal development of motoneurons in an altered glial environment. Using the patch-clamp technique, we made intracellular recording from motoneurons of Rexed’s lamina IX in spinal cord slices of neonatal rats (postnatal day P4–P10). The electrical properties of normal motoneurons changed significantly with age, showing decreasing input resistance (Rin) and increasing membrane capacity (Cm). The rheobase increased with age, accompanied by an increase of the amplitude and a decrease of the duration of action potentials (APs). In contrast, mutant neurons showed no age-dependent changes of Rin, Cm, or AP characteristics. After blocking inhibitory transmission, intralaminar bipolar stimulation elicited, in both control and taiep motoneurons, fast glutamatergic excitatory postsynaptic potentials (EPSPs). Two types of taiep motoneurons were identified according to the temporal patterns of synaptic responses; (1) taiep
SYN neurons, which showed no significant differences to control motoneurons, and (2) taiep
ASYN neurons, in which the initial EPSP was followed by a variable number of delayed, asynchronous EPSP responses (for up to 300 ms). All these electrophysiological findings suggest that the mutation in taiep rats interfered with the development of the electrical properties of neurons and with the maturation of synaptic transmission, probably due to alterations in the neuron-glia interactions.
Tài liệu tham khảo
Atluri PP, Regehr WG (1998) Delayed release of neurotransmitter from cerebellar granule cells. J Neurosci 18:8214–8227
Bakels R, Kernell D (1993) Average but not continuous speed match between motoneurons and muscle units of rat tibialis anterior. J Neurophysiol 70:1300–1306
Bellinger DL, Anderson WJ (1987) Postnatal development of cell columns and their associated dendritic bundles in the lumbosacral spinal cord of the rat. II. The ventromedial cell column. Brain Res 432:69–82
Blondel O, Collin C, McCarran WJ, Zhu S, Zamostiano R, Gozes I, Brenneman DE, McKay RD (2000) A glia-derived signal regulating neuronal differentiation. J Neurosci 20:8012–8020
Buck CR, Seburn KL, Cope TC (2000) Neurotrophin expression by spinal motoneurons in adult and developing rats. J Comp Neurol 416:309–318
Chávez AE, Roncagliolo M, Kuhrt H, Reichenbach A, Palacios AG (2003) The retinal anatomy and function of the myelin mutant taiep rat. Brain Res 964:144–152
Chen C, Regehr WG (1999) Contributions of residual calcium to fast synaptic transmission. J Neurosci 19:6257–6266
Chuhma N, Ohmori H (2002) Role of Ca2+ in the synchronization of transmitter release at calyceal synapses in the auditory system of rat. J Neurophysiol 87:222–228
Chuhma N, Koyano K, Ohmori H (2001) Synchronisation of neurotransmitter release during postnatal development in a calyceal presynaptic terminal of rat. J Physiol (Lond) 530:93–104
Couve E, Cabello JF, Krsulovic J, Roncagliolo M (1997) Binding of microtubules to transitional elements in oligodendrocytes of the myelin mutant taiep rat. J Neurosci Res 47:573–581
Curfs MH, Gribnau AA, Dederen PJ (1993) Postnatal maturation of the dendritic fields of motoneuron pools supplying flexor and extensor muscles of the distal forelimb in the rat. Development 117:535–541
Dekkers J, Becker DL, Cook JE, Navarrete R (1994) Early postnatal changes in the somatodendritic morphology of ankle flexor motoneurons in the rat. Eur J Neurosci 6:87–97
Desai NS, Rutherford LC, Turrigiano GG (1999) BDNF regulates the intrinsic excitability of cortical neurons. Learn Mem 6:284–291
Duncan ID, Lunn KF, Holmgren B, Urba-Holmgren R, Brignolo-Holmes L (1992) The taiep rat: a myelin mutant with associated oligodendrocytes microtubular defect. J Neurocytol 21:870–884
Eguibar JR, Lopez G, Manjarrez E, Roncagliolo M (1997) The variability of H Reflex responses were differentially affected by pre and post-synaptic mechanism in the rat. Soc Neurosci Abstr 23:409
Emptage NJ, Reid CA, Fine A (2001) Calcium stores in hippocampal synaptic buttons mediate short-term plasticity, store-operated Ca2+ entry, and spontaneous transmitter release. Neuron 29:197–208
Fields RD, Stevens-Graham B (2002) New insights into neuron-glia communication. Science 298:556–562
Fulton BP, Walton K (1986) Electrophysiological properties of neonatal rat motoneurones studied in vitro. J Physiol (Lond) 370:651–768
Gao BX, Ziskind-Conhaim L (1998) Development of ionic currents underlying changes in action potential waveforms in rat spinal motoneurons. J Neurophysiol 80:3047–3061
Gardiner PF (1993) Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. J Neurophysiol 69:1160–1170
Gonzalez M, Collins WF (1997) Modulation of motoneuron excitability by brain-derived neurotrophic factor. J Neurophysiol 77:502–506
Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100
Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2:185–193
Holmgren B, Urba-Holmgren R, Riboni L, Vega-Saenz de Miera EC (1989) Sprague Dawley rat mutant with tremor, ataxia, tonic immobility episodes, epilepsy and paralysis. Lab Anim Sci 39:226–228
Isaacson JS, Walmsley B (1995) Counting quanta: direct measurements of transmitter release at a central synapse. Neuron 15:875–884
Konnerth A, Keller BU, Lev-Tov A (1990) Patch clamp analysis of excitatory synapses in mammalian spinal cord slices. Pflugers Arch 417:285–290
Krsulovic J, Couve E, Roncagliolo M (1999) Dysmyelination, demyelination and reactive astrogliosis in the optic nerve of the taiep rat. Biol Res 32:253–262
Kudo N, Yamada T (1985) Development of the monosynaptic stretch reflex in the rat: an in vitro study. J Physiol (Lond) 369:127–144
Leon Chavez BA, Guevara J, Galindo S, Luna J, Ugarte A, Villegas O, Mena R, Eguibar JR, Martinez-Fong D (2001) Regional and temporal progression of reactive astrocytosis in the brain of the myelin mutant taiep rat. Brain Res 1:152–155
Lev-Tov A, Pinco M (1992) In vitro studies of prolonged synaptic depresion in the neonatal rat spinal cord. J Physiol (Lond) 447:149–169
Lu B, Chow A (1999) Neurotrophins and hippocampal synaptic transmission and plasticity. J Neurosci Res 58:76–87
Mauch DH, Nägler K, Schumacher S, Goritz C, Muller EC, Otto A, Pfrieger FW (2001) CNS synaptogenesis promoted by glia-derived cholesterol. Science 294:1354–1357
Mazzanti M, Haydon PG (2003) Astrocytes selectively enhance N-type calcium current in hippocampal neurons. Glia 41:128–136
Mu X, Silos-Santiago I, Carroll SL, Snider WD (1993) Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J Neurosci 13:4029–4041
Nägler K, Mauch DH, Pfrieger FW (2001) Glia-derived signals induce synapse formation in neurones of the rat central nervous system. J Physiol (Lond) 533:665–679
Pinco M, Lev-Tov A (1993) Modulation of monosynaptic excitation in the neonatal rat spinal cord. J. Neurophysiol 70:1151–1158
Roncagliolo M, Benitez J, Eguibar JR (2000a) Progressive deterioration of central components of auditory brainstem responses during postnatal development of the myelin mutant taiep rat. Audiol Neurootol 5:267–275
Roncagliolo M, Leon C, Silva J, Eguibar JR (2000b) The recovery cycle of excitability in isolated optic nerve of myelin mutant taiep rats during postnatal development. J. Physiol (Lond) 523P:54P
Rumpel E, Behrends JC (1999) Sr2+-dependent asynchronous evoked transmission at rat striatal inhibitory synapses in vitro. J Physiol (Lond) 514:447–458
Seebach BS, Mendell LM (1996) Maduration in properties of motoneurons and their segmental input in the neonatal rat. J Neurophysiol 76:3875–3885
Ullian E, Sapperstein S, Christopherson K, Barres BA (2001) Control of synapses number by glia. Science 291:657–661
Viana F, Bayliss DA, Berger AJ (1994) Postnatal changes in rat hypoglossal motoneuron membrane properties. Neuroscience 59:131–148
Vinay L, Brocard F, Pflieger JF, Simeoni-Alias J, Clarac F (2000) Perinatal development of lumbar motoneurons and their inputs in the rat. Brain Res Bull 53:635–647
Yan Q, Elliott JL, Matheson C, Sun J, Zhang L, Mu X, Rex KL and Snider WD (1993) Influences of neurotrophins on mammalian motoneurons in vivo. J Neurobiol 24:1555–1557
Yoshimura M, Nishi S (1993) Blind patch-clamp recordings from substantia gelatinosa neurons in adult rat spinal cord slices: pharmacological properties of synaptic currents. Neuroscience 53:519–526
Ziskind-Conhaim L (1988) Electrical properties of motoneurons in the spinal cord of rat embryos. Dev Biol 128:21–29
