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Dipartimento di Neurofisiologia Sperimentale, Istituto Nazionale Neurologico "Carlo Besta", 20133 Milan, Italy; and Department of Psychology, University of Alberta, Edmonton T6E 4S4, Canada
Submitted 25 November 2002; accepted in final form 5 March 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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,
1930;
Llinas and Paré 1991;
Llinás et al. 1998;
Penfield and Jasper 1954;
Steriade 1997,
2000). The mechanisms of
state-dependent shifts in field/EEG activity presumably underlie different
processing features of the cerebral cortex across behavioral states. Recently,
a slow periodic pattern (named "slow oscillation") has been
described, which exhibits frequencies lower than 1 Hz
(Steriade 2000;
Steriade et al. 1993b). In
both animals and humans, this pattern of activity appears during spontaneous
slow-wave sleep (Achermann and Borbely
1997; Amzica and Steriade
1997; Steriade et al.
1993b), as well as during anesthesia induced by a wide variety of
anesthetics (Lampl et al.
1999; Steriade et al.
1993e). These slow periodic events (SPEs) include delta and faster
rhythms, such as sleep spindles and ultra-fast ripples (80–200 Hz)
(Grenier et al. 2001; Steriade
et al.
1993b,d)
and may represent the K-complexes typically observed in slow sleep EEG (Amzica
and Steriade 1997,
1998). Because of their
behavioral correlates, SPEs have been suggested to be an objective marker for
unconsciousness (Niedermeyer
1999). While studied extensively in the neocortex, SPEs have also
been reported in diverse cortical and subcortical structures including the
hippocampal formation, the entorhinal cortex, the perirhinal cortex, the
neostriatum, and the amygdala
(Buzsáki et al. 1992;
Charpak et al. 1995;
Chrobak and Buzsaki 1996;
Collins et al. 2001;
Wilson and Kawaguchi
1996).
At the neuronal level, SPEs reflect synchronous
depolarization-hyperpolarization sequences
(Lampl et al. 1999;
Steriade et al. 1993e;
Wilson and Kawaguchi 1996)
generated at the level of the local cortical circuitry, since they are present
in the cerveau isolé preparation
(Steriade et al. 1993d), in
isolated cortical slabs (Timofeev et al.
2000), and have more recently been shown in different in vitro
preparations (Sanchez-Vives and McCormick
2000; Wu et al.
2002). Consistent with their state dependency, they are abolished
by stimulation of ascending cholinergic or noradrenergic activating systems,
which produces arousal in the behaving animal
(Steriade et al. 1993a) and
induces long-lasting depolarization in cortical cells
(Metherate et al. 1992;
Steriade et al. 1993a).
In this study, we show that spontaneously developing SPEs that bear
resemblance to the slow (<1 Hz) oscillations described in the intact,
sleeping, or anesthetized brain (Steriade
et al. 1994) can be recorded in the entorhinal cortex of the
isolated adult guinea pig brain maintained in vitro. We further demonstrate
that SPE are reversibly abolished by muscarinic receptor stimulation,
suggesting that they may reflect an activation state similar to that observed
in the sleeping or anesthetized animal.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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,
1998;
Llinás et al. 1981;
Muhlethaler et al. 1993) and
will be only briefly described here. Following deep barbiturate anesthesia
(thiopenthal sodium 20 mg/kg ip), female Hartley guinea pigs (150–250 g;
Charles River, Comerio, Italy) were perfused through the heart with a cold
(4–10°C) carbogenated (95% O2-5% CO2) solution
composed of (in mM) 126 NaCl, 3 KCl, 1.2 KH2PO4, 1.3
MgSO4, 2.4 CaCl2, 26 NaHCO3, 15 glucose, 2.1
HEPES, 0.4 thiourea, 0.5 ascorbic acid, and 3% dextran (MW 70.000). Following
cooling to 15°C, the brain was rapidly and carefully dissected out of the
cranium and was submerged in a recording chamber filled with the same solution
maintained at a temperature of 15°C. Internal perfusion through the
existing brain vasculature at a rate of 5.5 ml/min was achieved by cannulating
the basilar artery. Leaky arterial vessels were ligated, and the brain was
gradually (0.2°C /min) warmed to a final temperature of 32°C. This
protocol was reviewed and approved by the Committee on Animal Care and Use and
by the Ethics Committee of the Istituto Nazionale Neurologico. Extracellular field recordings were made with 1) saline-filled glass micropipettes with a 10 µm tip diameter 2) 16-channel linear silicon probes (50 µm contact separation, kindly provided by Jamille Hetke, of the Center for Neural Communication Technology, University of Michigan, Ann Arbor, MI), or 3) stainless steel microelectrode matrix arrays (1 x 4 or 4 x 4 with 410-µm tip separation: FHC, Bowdoinham, ME). All single-site recordings, unless otherwise noted, were made at a depth of 500 µm from the pial surface. Recordings at multiple sites were carried out simultaneously. Intracellular recordings were made with 1.5 M K+-acetate–filled micropipettes pulled to a final resistance of 80–100 MOhm. Neurons selected for analysis in this study had resting membrane potentials of at least –55 mV and an overshooting spike.
Field signals were amplified at a gain of 1,000 using an AC amplifier (Biomedical Engineering, Thornwood, NY), high-pass filtered at 0.2 Hz, and low-pass filtered at 1,000 Hz. Intracellular signals were amplified at a gain of 10 using a Neuro Data amplifier (IR-283, Cygnus Technology, Delaware Water Gap, PA) and low-pass filtered at 10 KHz. All signals digitized on-line using a National Instruments DAQ board (PCI-6071E) were acquired with customized software developed by Gerardo Biella and were stored on DAT tape (DTR 2602 Biologic, Claix, France) for off-line analysis. Waveforms were sampled on-line at a frequency of 2–20 kHz depending on the band-width of the signal. Single channel spectral analyses were conducted off-line using MATLAB (Mathworks, Natick, MA).
Intracortical stimulation was conducted using thin insulated tungsten bipolar electrodes (FHC). When metal electrodes were used for intracortical recording or stimulation, the location of the electrode tips were marked by small electrolytic lesions. Following completion of experiments, brains were fixed overnight in a 4% paraformaldehyde solution in a 0.1 M sodium phosphate buffer and sectioned by vibratome at 100 µm. Sections were mounted, stained with thionin, and inspected for the location of electrode sites.
Cholinergic agents such as CCh (25–50 µM) and atropine sulfate (ATSO4: 5 µM) were diluted in the perfusion solution. All salts were obtained from BDH (Poole, England) and all drugs were obtained from Sigma (St. Louis, MO). Dextran was obtained from SIFRA (Isola della Scala, Italy).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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To test whether SPEs were generated within the mEC, we performed simultaneous multi-site laminar recordings using 16-channel linear silicon probes with 50 µm inter-site spacing inserted orthogonal to the pial surface of the mEC. Phase reversals of both the fast and slow oscillatory components within single SPEs were observed in the superficial layers (Fig. 2, B and C). Histological analysis of probe tracts demonstrated that the depth of phase reversal corresponded to layer II (Fig. 2A; n = 10). These results confirmed that SPE are generated locally within the mEC and suggest that the superficial network is critical for their generation. Further confirmation of this was gleaned by performing simultaneous field and intracellular recordings of superficial layer principal cells during SPE. As shown in Fig. 3, the occurrence of individual field events corresponded to a slowly developing depolarizing envelope recorded intracellularly (n = 31). Riding on the intracellular depolarization were fast membrane potential oscillations and action potential discharges, which corresponded to the fast oscillations present in the field recordings (Fig. 3B). The long-lasting depolarizing envelope was dependent on the value of the membrane potential, becoming smaller and larger with membrane depolarization and hyperpolarization, respectively (Fig. 3C). Interestingly, as shown in Fig. 3C, the fast membrane potential oscillations during the slow depolarization decreased in amplitude or vanished with membrane hyperpolarization.
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When recording SPEs with multiple single electrodes across the surface of the EC, it was frequently noted (10 of 16 cases) that the onset of activity at some sites preceded that at others, suggesting that such events were actively propagated tangentially across the cortex. To examine intra-EC propagation more systematically, a pair of multielectrode arrays, each consisting of an equally spaced row of four electrodes (1 x 4), was used to record field activity simultaneously across the surface of the EC (n = 8). In all experiments, evidence of SPE propagation could be observed. In three additional experiments, we performed simultaneous field recordings with a 4 x 4 (16 site) matrix electrode. Using this protocol we were able to consistently observe propagation of SPE with variable directions within the same experiment (Fig. 4).
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The tangential propagation of SPE across the surface of the EC may occur
through synaptic interactions between superficial neurons. We tested,
therefore, whether electrical stimulation of the superficial mEC layers,
previously shown to elicit an AMPA-dependent evoked potential
(Dickson et al. 2000a), could
also evoke SPEs. In 8 of 12 experiments, stimulation that evoked a measurable
evoked potential (inset in Fig.
5C) induced and entrained events
(Fig. 5C) similar to
those occurring spontaneously (Fig.
5B). As for SPE, laminar field recordings of these evoked
events using multichannel silicon probes showed depth reversal patterns of
both slow and fast components in the superficial mEC layers (data not
shown).
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One of the characteristics of the slow waves in vivo is that they are
abolished by brain stem activating cholinergic and noradrenergic stimuli
(Belardetti et al. 1977;
Moruzzi and Magoun 1949;
Steriade et al. 1993a). The
mEC receives a prominent cholinergic input
(Alonso and Köhler 1984)
that appears to be necessary for the state-dependent expression of rhythmic
oscillatory activity (theta and gamma) in vivo
(Chrobak and Buzsáki
1998; Dickson
1994; Dickson et al.
1995; Jefferys
1995; Leung 1998;
Mitchell et al. 1982). We have
previously demonstrated that muscarinic receptor activation in the isolated
whole brain preparation induces continuous oscillatory activity at around
25–33 Hz (the gamma range at 32°C) exclusively in the mEC
(Dickson et al. 2000a;
van der Linden et al. 1999),
and we thus sought to test the activation of muscarinic receptors on slow
periodic activity. In all cases examined (n = 19), perfusion of
carbachol (50 µM) gradually abolished SPE
(Fig. 6). With increasing times
of perfusion, the inter-SPE frequency increased and the amplitude of the
events decreased until they eventually disappeared to be replaced by
continuous fast oscillations (expanded trace on the right in
Fig. 6A). Of special
note, when laminar profiles were recorded for both SPE and gamma in the same
experiment with 16-channel silicon probes, the fast oscillatory component of
both types of activity showed identical phase profiles with reversals
localized to layer II (data not shown; n = 3). In four further
experiments, co-perfusion of CCh with the muscarinic antagonist, atropine
sulfate (5 µM), abolished gamma activity and reinstated the SPE
(Fig. 6B).
Intracellular recordings made from superficial layer mEC cells during these
manipulations (n = 3) demonstrated that the gradual abolition of the
slow field events by CCh coincided with a gradual depolarization of the
membrane potential to a level at which the gamma oscillatory activity was
expressed (Fig. 7,
middle). Likewise, the reinstatement of the slow periodic activity by
co-perfusion of CCh and atropine coincided with a return of the membrane
potential toward control levels (Fig.
7, right).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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; Collins et al.
2001) and in other cortical and subcortical regions during deep
anesthesia (Lampl and Yarom
1997; Steriade et al.
1993b,e;
Wilson and Kawaguchi 1996).
SPEs in the EC occurred with a variable periodicity, much lower
(0.02–0.4 Hz) than that observed in the neocortex in vivo (0.7–1
Hz), but similar to recurrent slow events described in ferret neocortex and in
the hippocampus both in vitro
(Sanchez-Vives and McCormick
2000; Zhang et al.
1998) and in vivo (Penttonen
et al. 1999). Such a difference in SPE frequency could be due to
1) the marked level of nervous system depression associated with the
sensorial deprivation of the in vitro condition attained both in slices and in
the isolated brain preparation, 2) the low temperature (32°C)
utilized to substitute for pharmacological anesthesia in our experiments, and
3) a residual effect of the barbiturate anesthesia performed before
brain isolation. Several clinical and experimental studies have demonstrated,
indeed, that body temperature below 32°C considerably reduces brain
metabolism to a functional state that correlates with unconsciousness or
severe impairment of vigilance (Curley and
Irwin 1991; Fischbeck and
Simon 1981; FitzGibbon et al.
1984; Rosin and Exton-Smith
1964).
Our findings suggested that SPE in the EC are locally generated, since they
showed a depth reversal in superficial layers. This is consistent with the
observation that neocortical slow oscillations are local events spontaneously
produced not only in the intact (in vivo) brain
(Steriade et al. 1993e) but
also in the undercut (deafferented) cortical slab
(Timofeev et al. 2000) and in
cortical slices maintained in vitro
(Sanchez-Vives and McCormick
2000; Zhang et al.
1998). Even though the shaping of spontaneous slow neocortical
activity in vivo involves a dynamic interaction with the thalamus
(Timofeev et al. 1996), the
above observations suggest that the necessary events subtending periodic slow
oscillations are generated within the cortex itself in the absence of
subcortical inputs. Such a conclusion is further strengthened by the finding
that extensive thalamic lesions do not abolish the cortical slow rhythm
(Steriade et al. 1993b) and
that the slow oscillations are preserved in the cerveau isolé
preparation (Belardetti et al.
1977; Steriade et al.
1993b).
In vivo studies have suggested that repetitive periodic slow activity in
the neocortex correlates at the intracellular level with alternating
"on" and "off" states. The "on" state is
characterized by threshold level plateau depolarizations topped with
high-frequency neuronal firing and subthreshold oscillations. In contrast, the
"off" state is characterized by membrane hyperpolarization. Both
phases may be generated by active or disfacilatory mechanisms, either synaptic
or intrinsic (Amzica and Steriade
1995; Contreras et al.
1996; Timofeev et al.
2001). Such activity is similar to the two-state behavior observed
in spiny neostriatal neurons in vivo
(Wilson and Kawaguchi 1996),
which is characterized by the sudden shift between two preferred membrane
potential levels, presumably controlled by a nonidentified potassium
conductance. The long-lasting time course of the hyperpolarized period
observed between two SPEs in the mEC (≤20 s) suggest that active inhibitory
events, either synaptic or intrinsic, cannot account exclusively for the
inter-SPE interval. Therefore, it is reasonable to hypothesize that the
depolarization at the onset of SPE is not only mediated by the release of
inhibition, but it is also driven by an active depolarization, possibly
involving synaptic-mediated mechanisms. In support of this hypothesis,
1) intracellular depolarizing responses correlated to SPEs were
increased in amplitude by injections of hyperpolarizing currents, 2)
SPEs propagated tangentially across the surface of the EC possibly through
excitatory associative connections, and 3) SPEs could be elicited by
local EC stimulation that induces synaptic activation of fast glutamatergic
neurotransmission mediated by intra-EC associative fibers
(Dickson et al. 2000b). These
observations are consistent with the study on in vitro slices
(Sanchez-Vives and McCormick
2000), which demonstrated that generation and propagation of slow
population events could be induced by pressure applications of glutamate and
were blocked by antagonists of different synaptic excitatory receptor
subtypes.
While the slow biphasic component of SPE was correlated with the slow
depolarizing envelope recorded intracellularly in superficial EC neurons, the
fast oscillatory field activity of SPE correlated to the production of
high-frequency spiking and membrane potential oscillations, as reported in
vivo (Buzsáki 1992; Grenier et al.
2001; Steriade et al.
1993d). These fast rhythms are assumed to reflect local
synchronization of cortical networks involving recurrent connections between
excitatory principal neurons and inhibitory interneurons
(Grenier et al. 2001), similar
to those involved in the production of fast (gamma) rhythms in vitro
(Dickson et al. 2000a;
Fisahn et al. 1998;
Traub et al. 1996).
Interestingly, in the current study it was observed that the phase reversal of
both the fast oscillatory activity during SPEs and gamma oscillations evoked
by CCh occurred at the same depth, suggesting that they may be dependent on
similar local network mechanisms.
As mentioned in the introduction, slow periodic patterns correlated with
sleep and unconsciousness (Steriade et al.
1993b,c,d,e)
can be disrupted by brain stem stimulation of cholinergic and noradrenergic
nuclei (Moruzzi and Magoun
1949; Steriade and Contreras
1995; Steriade et al.
1993a) and by basal forebrain nuclei activation
(Belardetti et al. 1977;
Cape and Jones 1998). Even
though the nonselective activation determined by in vivo brain stem and
forebrain stimulation does not allow for a precise identification of the type
of neurotransmitters involved, it has been suggested that cortical arousal is
at least partially mediated via the cholinergic ascending pathways. Our
findings demonstrate for the first time in an intact brain that slow periodic
activity of cortical origin is disrupted by cholinergic activation,
pharmacologically induced by exogenous application of a muscarinic agonist.
Interestingly, the disappearance of SPEs coincides with the gradual
development of a fast rhythm that is commonly associated with cortical
activation (Cape and Jones
1998; Metherate et al.
1992; Steriade et al.
1991). During the cortical state transition induced by CCh, the
amplitude of SPEs decreased and their frequency increased, while membrane
potentials of principal cells progressively depolarized and fast oscillations
in the gamma range gradually established. Previous reports from our group,
indeed, have demonstrated that muscarinic activation with CCh consistently
induces fast oscillations that are restricted to the medial part of the EC
without involvement of other cortical regions, such as the lateral EC, the
perirhinal cortex or the neocortex
(Dickson et al. 2000a;
van der Linden et al.
1999).
We conclusively demonstrate that the EC of the isolated brain preparation produces in resting conditions a periodic pattern similar to that observed in cortical brain structures in vivo and in vitro during spontaneous and during pharmacologically induced slow sleep. Furthermore, we demonstrate that these events are reversibly abolished by muscarinic receptor stimulation, suggesting that they are indeed representative of a deactivated state in the whole brain preparation. Since state-dependent shifts in the expression of cortical field activity are thought to reflect different functional modes of processing across different behavioral states, model systems for studying these shifts are extremely valuable. Our findings suggest that the isolated whole brain is a suitable preparation to study the mechanisms of generation and modulation of SPE.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Present address of G. Biella: Dipartimento di Scienze Fisiologiche, Università di Pavia, Italy.
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FOOTNOTES |
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Address for reprint requests: M. de Curtis, Dipartimento Neurofisiologia Sperimentale, Istituto Nazionale Neurologico "Carlo Besta" via Celoria, 11, 20133 Milan, Italy (E-mail: decurtis{at}istituto-besta.it).
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