Skip to main content

Synchrony of the Rat Medial Prefrontal Cortex Network During Isoflurane Anaesthesia

  • Conference paper
  • First Online:
Book cover The Basal Ganglia IX

Part of the book series: Advances in Behavioral Biology ((ABBI,volume 58))

Abstract

In the anaesthetized rat, the membrane potential of the prefrontal cortex (PFC) fluctuates between two states of polarization: the up- and down-states. The PFC network strongly governs activity in its target areas such as various basal ganglia structures. The influence of anaesthesia on network dynamics in the prelimbic cortex will therefore have direct consequences for the activity profile of the output structures. In order to investigate the effects of isoflurane anaesthesia on network activity of the PFC, rats were anaesthetized with isoflurane of which the concentration was varied between 1.25 and 2.25%. Local EEG and single-unit activity were recorded simultaneously.

At baseline levels (1.75%), isoflurane anaesthesia induced up-state transitions in the prelimbic cortex visible in the local EEG signal. The up-state deflections in the EEG were determined as reflections of clustered firing of individual prelimbic neurons. 2.25% isoflurane strongly reduced the up-state frequency whereas 1.25% isoflurane allowed the network to shift to a continuous activity mode. These results show that neuronal activity in the medal PFC and therefore its target structures is highly dependent on the level of isoflurane anaesthesia. Considering the similarity between the synaptic targets of isoflurane by which surgical anaesthesia is maintained and the mechanisms involved in initiation, maintenance and cessation of up-states, the up- and down-state fluctuations are a direct result of anaesthesia.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 259.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adrian ED and Matthews BHC (1934) The interpretation of potential waves in the cortex. J Physiol 81: 440–471.

    CAS  PubMed  Google Scholar 

  • Amzica F and Steriade M (1995) Short and long-range neuronal synchronization of the slow (<1 Hz) cortical oscillation. J Neurophysiol 73: 20–38.

    CAS  PubMed  Google Scholar 

  • Berg-Johnsen J and Langmoen IA (1990) Mechanisms concerned in the direct effect of isoflurane on rat hippocampal and human neocortical neurons. Brain Res 507: 28–34.

    Article  CAS  PubMed  Google Scholar 

  • Branchereau P, van Bockstaele EJ, Chan J and Pickel VM (1996) Pyramidal neurons in rat prefrontal cortex show a complex synaptic response to single electrical stimulation of the locus coeruleus region: Evidence for antidromic activation and GABAergic inhibition using in vivo intracellular recording and electron microscopy. Synapse 22: 313–331.

    Article  CAS  PubMed  Google Scholar 

  • Contreras D and Steriade M (1995) Cellular basis of EEG slow rhythms: A study of dynamic corticothalamic relationships. J Neurosci 15: 604–622.

    CAS  PubMed  Google Scholar 

  • Cossart R, Aronov D and Yuste R (2003) Attractor dynamics of network UP states in the neocortex. Nature 423: 283–288.

    Article  CAS  PubMed  Google Scholar 

  • Cowan RL and Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71: 17–32.

    CAS  PubMed  Google Scholar 

  • Criado AB and Gómez de Segura IA (2003) Reduction of isoflurane MAC by fentanyl or remifentanil in rats. Vet Anaesth Analg 30: 250–256.

    Article  CAS  PubMed  Google Scholar 

  • De Wolff MH, Leather HA and Wouters PF (1999) Effects of tramadol on minimum alveolar concentration (MAC) of isoflurane in rats. Br J Anaesth 83: 780–783.

    PubMed  Google Scholar 

  • Douglas RJ, Koch C, Mahowald M, Martin KAC and Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269: 981–985.

    Article  CAS  PubMed  Google Scholar 

  • Gómez de Segura IA, Criado AB, Santos M and Tendillo FJ (1998). Aspirin synergistically potentiates isoflurane minimum alveolar concentration reduction produced by morphine in the rat. Anesthesiology 89: 1489–1494.

    Article  PubMed  Google Scholar 

  • Goto Y and O’Donnell P (2001a) Synchronous activity in the hippocampus and nucleus accumbens in vivo. J Neurosci 21: RC131: 1–5.

    Google Scholar 

  • Goto Y and O’Donnell P (2001b) Network synchrony in the nucleus accumbens in vivo. J Neurosci 21: 4498–4504.

    CAS  PubMed  Google Scholar 

  • Groenewegen HJ and Uylings HB (2000) The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126: 3–28.

    Article  CAS  PubMed  Google Scholar 

  • Hudetz AG and Imas OA (2007) Burst activation of the cerebral cortex by flash stimuli during isoflurane anesthesia in rats. Anesthesiology 107: 983–991.

    Article  CAS  PubMed  Google Scholar 

  • Imas OA, Ropella KM, Ward BD, Wood JD and Hudetz AG (2005) Volatile anesthetics enhance flash-induced gamma oscillations in rat visual cortex. Anesthesiology 102: 937–947.

    Article  CAS  PubMed  Google Scholar 

  • Isomura Y, Sirota A, Özen S, Montgomery S, Mizuseki K, Henze DA and Buzsáki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52: 871–882.

    Article  CAS  PubMed  Google Scholar 

  • Jones MV, Brooks PA and Harrison NL (1992) Enhancement of γ-aminobutyric acid-activated Cl currents in cultured rat hippocampal neurons by three volatile anaesthetics. J Physiol 449: 279–293.

    CAS  PubMed  Google Scholar 

  • Kroeger D and Amzica F (2007) Hypersensitivity of the anesthesia-induced comatose brain. J Neurosci 27: 10597–10607.

    Article  CAS  PubMed  Google Scholar 

  • Lampl I, Reichova I and Ferster D (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361–374.

    Article  CAS  PubMed  Google Scholar 

  • Larsen M and Langmoen IA (1998) The effect if volatile anaesthetics on synaptic release and uptake of glutamate. Toxicol Lett 100: 59–64.

    Article  PubMed  Google Scholar 

  • Larsen M, Grøndahl T, Haugstad T and Langmoen IA (1994) The effect of the volatile anesthetic isoflurane on the Ca2+-dependent glutamate release from rat cerebral cortex. Brain Res 663: 335–337.

    Article  CAS  PubMed  Google Scholar 

  • Larsen M, Hegstad E, Berg-Johnsen J and Langmoen IA (1997) Isoflurane increases the uptake of glutamate in synaptosomes from rat cerebral cortex. Br J Anaesth 78: 55–59.

    CAS  PubMed  Google Scholar 

  • Larsen M, Haugstad TS, Berg-Johnsen J and Langmoen IA (1998) Effect of isoflurane on release and uptake of gamma-aminobutyric acid from rat cortical synaptosomes. Br J Anaesth 80: 634–638.

    CAS  PubMed  Google Scholar 

  • Lewis BL and O’Donnell P (2000) Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential ‘up’ states in pyramidal neurons via D1 dopamine receptors. Cereb Cortex 10: 1168–1175.

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Au JD, Zou HL, Cotton JF and Spencer Yost C (2004) Potent activation of the tandem pore domain K+ channel TRESK with clinical concentrations of volatile anesthetics. Anesth Analg 99: 1715–1722.

    Article  CAS  PubMed  Google Scholar 

  • Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y and Häusser M (2005) Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci 8: 202–211.

    Article  Google Scholar 

  • Luczak A, Bartho P, Marguet SL, Buzsaki G, Harris KD (2007) Sequential structure of neocortical spontaneous activity in vivo. Proc Natl Acad Sci USA 104: 347–352.

    Article  CAS  PubMed  Google Scholar 

  • MacIver BM, Mikules AA, Amagasu SM and Monroe FA (1996) Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 85: 823–834.

    Article  Google Scholar 

  • Mahon S, Vautrelle N, Pezard L, Slaght SJ, Deniau JM, Chouvet G and Charpier S (2006) Distinct patterns of striatal medium spiny neuron activity during the natural sleep-wake cycle. J Neurosci 26: 12587–12595.

    Article  CAS  PubMed  Google Scholar 

  • Milojkovic BA, Radojicic MS and Antic SD (2005) A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J Neurosci 25: 3940–3951.

    Article  CAS  PubMed  Google Scholar 

  • Minami K, Wick M, Stern-Bach Y, Dildy-Mayfield JE, Brozowski SJ, Gonzales EL, Trudell JR and Harris RA (1998) Sites of volatile anesthetic action on kainate (glutamate receptor 6) receptors. J Biol Chem 273: 8248–8255.

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa K and MacIver MB (2001) Agent-selective effects of volatile anesthetics on GABAA receptor-mediated synaptic inhibition in hippocampal interneurons. Anesthesiology 94: 340–347.

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell P and Grace AA (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: Hippocampal gating of prefrontal cortical input. J Neurosci 15: 3622–3639.

    PubMed  Google Scholar 

  • O’Donnell P and Grace AA (1998) Phencyclidine interferes with the hippocampal gating of nucleus accumbens neuronal activity in vivo. Neuroscience 87: 823–830.

    Article  PubMed  Google Scholar 

  • Paxinos G and Watson C (2007) The rat brain in stereotaxic coordinates, 6th Edition, Elsevier, Amsterdam.

    Google Scholar 

  • Pearce RA, Stringer JL and Lothman EW (1989) Effect of volatile anesthetics on synaptic transmission in the rat hippocampus. Anesthesiology 71: 591–598.

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Vives MV and McCormick DA (2000). Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027–1034.

    Article  CAS  PubMed  Google Scholar 

  • Shin WJ and Winegar BD (2003) Modulation of noninactivating K+ channels in rat cerebellar granule neurons by halothane, isoflurane and sevoflurane. Anesth Analg 96: 1340–1344.

    Article  CAS  PubMed  Google Scholar 

  • Steriade M, Gloor P, Llinás RR, Lopes da Silva FH and Mesulam M-M (1990) Basic mechanisms of cerebral rhythmic activities. Electroencephalogr Clin Neurophysiol 76: 481–508.

    Article  CAS  PubMed  Google Scholar 

  • Steriade M, Curró Dossi R and Nuñez A (1991) Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: Cortically induced synchronization and brainstem cholinergic suppression. J Neurosci 11: 3200–3217.

    CAS  PubMed  Google Scholar 

  • Steriade M, Nuñez A and Amzica F (1993a) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: Depolarizing and hyperpolarizing components. J Neurosci 13: 3252–3265.

    CAS  PubMed  Google Scholar 

  • Steriade M, Nuñez A and Amzica F (1993b) Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13: 3266–3283.

    CAS  PubMed  Google Scholar 

  • Steriade M, Contreras D, Curró Dossi R and Nuñe A (1993c) 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.

    CAS  PubMed  Google Scholar 

  • Steriade M, Timofeev I and Grenier F (2001) Natural waking and sleep states: A view from inside neocortical neurons. J Neurophysiol 85: 1969–1985.

    CAS  PubMed  Google Scholar 

  • Stern EA, Jaeger D and Wilson CJ (1998) Membrane potential synchrony of simultaneously recorded striatal siny neurons in vivo. Nature 394: 475–478.

    Article  CAS  PubMed  Google Scholar 

  • Verhaegen M, Todd MM and Warner DS (1992) The influence of different concentrations of volatile anesthetics on the threshold for cortical spreading depression in rats. Brain Res 581: 153–155.

    Article  CAS  PubMed  Google Scholar 

  • Westphalen RI and Hemmings HC (2006a) Volatile anesthetic effects on glutamate versus GABA release form isolated rat cortical nerve terminals: Basal Release. J Pharmacol Exp Ther 316: 208–215.

    Article  CAS  PubMed  Google Scholar 

  • Westphalen RI and Hemmings HC (2006b) Volatile anesthetic effects on glutamate versus GABA release form isolated rat cortical nerve terminals: 4-aminopyridine-evoked release. J Pharmacol Exp Ther 316: 216–223.

    Article  CAS  PubMed  Google Scholar 

  • Wilson CJ and Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220: 67–80.

    Article  CAS  PubMed  Google Scholar 

  • Wilson CJ and Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16: 2397–2410.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Antonius B. Mulder .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this paper

Cite this paper

Stegeman, M., de Boer, M., van der Roest, M., Mulder, A.B. (2009). Synchrony of the Rat Medial Prefrontal Cortex Network During Isoflurane Anaesthesia. In: Groenewegen, H., Voorn, P., Berendse, H., Mulder, A., Cools, A. (eds) The Basal Ganglia IX. Advances in Behavioral Biology, vol 58. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0340-2_11

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-0340-2_11

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-0339-6

  • Online ISBN: 978-1-4419-0340-2

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics