All Title Author
Keywords Abstract

PLOS ONE  2007 

Synaptic Transmission and Plasticity in an Active Cortical Network

DOI: 10.1371/journal.pone.0000670

Full-Text   Cite this paper   Add to My Lib

Abstract:

Background The cerebral cortex is permanently active during both awake and sleep states. This ongoing cortical activity has an impact on synaptic transmission and short-term plasticity. An activity pattern generated by the cortical network is a slow rhythmic activity that alternates up (active) and down (silent) states, a pattern occurring during slow wave sleep, anesthesia and even in vitro. Here we have studied 1) how network activity affects short term synaptic plasticity and, 2) how synaptic transmission varies in up versus down states. Methodology/Principal Findings Intracellular recordings obtained from cortex in vitro and in vivo were used to record synaptic potentials, while presynaptic activation was achieved either with electrical or natural stimulation. Repetitive activation of layer 4 to layer 2/3 synaptic connections from ferret visual cortex slices displayed synaptic augmentation that was larger and longer lasting in active than in silent slices. Paired-pulse facilitation was also significantly larger in an active network and it persisted for longer intervals (up to 200 ms) than in silent slices. Intracortical synaptic potentials occurring during up states in vitro increased their amplitude while paired-pulse facilitation disappeared. Both intracortical and thalamocortical synaptic potentials were also significantly larger in up than in down states in the cat visual cortex in vivo. These enhanced synaptic potentials did not further facilitate when pairs of stimuli were given, thus paired-pulse facilitation during up states in vivo was virtually absent. Visually induced synaptic responses displayed larger amplitudes when occurring during up versus down states. This was further tested in rat barrel cortex, where a sensory activated synaptic potential was also larger in up states. Conclusions/Significance These results imply that synaptic transmission in an active cortical network is more secure and efficient due to larger amplitude of synaptic potentials and lesser short term plasticity.

References

[1]  Evarts EV (1964) Temporal Patterns of Discharge of Pyramidal Tract Neurons During Sleep and Waking in the Monkey. J Neurophysiol 27: 152–171.
[2]  Hobson JA, McCarley RW (1971) Cortical unit activity in sleep and waking. Electroencephalogr Clin Neurophysiol 30: 97–112.
[3]  Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85: 1969–1985.
[4]  Lorente de Nó R (1938) Analysis of the activity of the chains of internuncial neurons. Journal of Neurophysiology 1: 207–244.
[5]  Steriade M, Deschenes M (1984) The thalamus as a neuronal oscillator. Brain Res 320: 1–63.
[6]  McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20: 185–215.
[7]  Andersen P, Andersson SA (1968) Physiological basis of the alpha rhythm. New York,: Appleton-Century-Crofts.
[8]  Steriade M (2001) Impact of network activities on neuronal properties in corticothalamic systems. J Neurophysiol 86: 1–39.
[9]  Pare D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. J Neurophysiol 79: 1450–1460.
[10]  Castro-Alamancos MA, Connors BW (1996) Cellular mechanisms of the augmenting response: short-term plasticity in a thalamocortical pathway. J Neurosci 16: 7742–7756.
[11]  Boudreau CE, Ferster D (2005) Short-term depression in thalamocortical synapses of cat primary visual cortex. J Neurosci 25: 7179–7190.
[12]  Crochet S, Fuentealba P, Cisse Y, Timofeev I, Steriade M (2006) Synaptic plasticity in local cortical network in vivo and its modulation by the level of neuronal activity. Cereb Cortex 16: 618–631.
[13]  Crochet S, Chauvette S, Boucetta S, Timofeev I (2005) Modulation of synaptic transmission in neocortex by network activities. Eur J Neurosci 21: 1030–1044.
[14]  Sanchez-Vives MV, McCormick DA, Nowak LG (1998) Is synaptic depression prevalent in vivo and does it contribute to contrast adaptation? Los Angeles, CA, USA: Society for Neuroscience.
[15]  Reig R, Gallego R, Nowak LG, Sanchez-Vives MV (2006) Impact of cortical network activity on short-term synaptic depression. Cereb Cortex 16: 688–695.
[16]  Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16: 2397–2410.
[17]  Steriade M, Nunez A, Amzica F (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252–3265.
[18]  Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361–374.
[19]  Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027–1034.
[20]  Lampl I, Reichova I, Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. 22: 361–374.
[21]  Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26: 4535–4545.
[22]  Timofeev I, Contreras D, Steriade M (1996) Synaptic responsiveness of cortical and thalamic neurones during various phases of slow sleep oscillation in cat. J Physiol 494 ( Pt 1): 265–278.
[23]  Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A 100: 13638–13643.
[24]  Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19: 2209–2223.
[25]  Sachdev RN, Ebner FF, Wilson CJ (2004) Effect of subthreshold up and down states on the whisker-evoked response in somatosensory cortex. J Neurophysiol 92: 3511–3521.
[26]  Aghajanian GK, Rasmussen K (1989) Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3: 331–338.
[27]  Sanchez-Vives MV, Nowak LG, McCormick DA (2000) Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20: 4267–4285.
[28]  Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Amsterdam ; Boston: Elsevier Academic Press.
[29]  Koh DS, Burnashev N, Jonas P (1995) Block of native Ca(2+)-permeable AMPA receptors in rat brain by intracellular polyamines generates double rectification. J Physiol 486 ( Pt 2): 305–312.
[30]  Anderson J, Lampl I, Reichova I, Carandini M, Ferster D (2000) Stimulus dependence of two-state fluctuations of membrane potential in cat visual cortex. Nat Neurosci 3: 617–621.
[31]  Varela JA, Sen K, Gibson J, Fost J, Abbott LF, et al. (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17: 7926–7940.
[32]  Zucker RS (1989) Short-Term Synaptic Plasticity. Annual Review of Neuroscience 12: 13–31.
[33]  Dobrunz LE, Stevens CF (1997) Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses. Neuron 18: 995–1008.
[34]  Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384–388.
[35]  Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci U S A 94: 719–723.
[36]  Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355–405.
[37]  Castro-Alamancos MA (2002) Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. The Journal of Physiology Online 539: 567–578.
[38]  Massimini M, Amzica F (2001) Extracellular calcium fluctuations and intracellular potentials in the cortex during the slow sleep oscillation. J Neurophysiol 85: 1346–1350.
[39]  Haider B, Duque A, Hasenstaub AR, Yu Y, McCormick DA (2007) Enhancement of Visual Responsiveness by Spontaneous Local Network Activity in vivo. J Neurophysiol.
[40]  Thomson AM (1997) Activity-dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro. J Physiol 502 ( Pt 1): 131–147.
[41]  Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95: 5323–5328.
[42]  Bernander O, Douglas RJ, Martin KA, Koch C (1991) Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci U S A 88: 11569–11573.
[43]  Destexhe A, Rudolph M, Pare D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739–751.
[44]  Shu Y, Hasenstaub A, Badoual M, Bal T, McCormick DA (2003) Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J Neurosci 23: 10388–10401.
[45]  Rudolph M, Pelletier JG, Pare D, Destexhe A (2005) Characterization of synaptic conductances and integrative properties during electrically induced EEG-activated states in neocortical neurons in vivo. J Neurophysiol 94: 2805–2821.
[46]  Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35: 773–782.
[47]  Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (2002) Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. J Neurosci 22: 8691–8704.
[48]  Waters J, Helmchen F (2006) Background synaptic activity is sparse in neocortex. J Neurosci 26: 8267–8277.
[49]  Fuentealba P, Crochet S, Timofeev I, Steriade M (2004) Synaptic interactions between thalamic and cortical inputs onto cortical neurons in vivo. J Neurophysiol 91: 1990–1998.
[50]  Steriade M, Contreras D, Curro Dossi R, 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. J Neurosci 13: 3284–3299.
[51]  Steriade M, Timofeev I (2003) Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 37: 563–576.
[52]  Nowak LG, Bullier J (1998) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res 118: 489–500.
[53]  Steriade M, Amzica F, Contreras D (1996) Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci 16: 392–417.
[54]  Compte A, Harvey MA, Puccini G, Descalzo VF, Reig R, et al. (2003) Fast, synchronized oscillations during activated states in the cortical microcircuit in vitro. New Orleans, LA, USA: Society for Neuroscience.
[55]  Shu Y, Hasenstaub A, Duque A, Yu Y, McCormick DA (2006) Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441: 761–765.
[56]  Kerr JN, Plenz D (2002) Dendritic calcium encodes striatal neuron output during up-states. J Neurosci 22: 1499–1512.
[57]  Chen D, Fetz EE (2005) Characteristic membrane potential trajectories in primate sensorimotor cortex neurons recorded in vivo. J Neurophysiol 94: 2713–2725.

Full-Text

comments powered by Disqus