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The Journal of Neuroscience, 2000, 20:RC54:1-6
This Rapid Communication was received Sept. 17, 1999,
revised Nov. 2, 1999, and accepted Nov. 10, 1999.
RAPID COMMUNICATION
Traveling Slow Waves of Neural Activity: A Novel Form of Network
Activity in Developing Neocortex
Alejandro
Peinado
Department of Neuroscience, Albert Einstein College of Medicine,
Bronx, New York 10461
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ABSTRACT |
Spontaneous neuronal firing during development has the potential to
shape many aspects of neuronal wiring throughout the brain. Bursts of
electrical activity coordinated among large numbers of neurons,
occurring during a brief developmental window, have been described in
many regions of the CNS, including retina, hippocampus, and spinal
cord, but evidence for this type of activity in developing neocortex
has so far been lacking. To identify conditions that may give rise to
patterned spontaneous electrical activity in developing neocortex,
cholinergic agonists were applied to immature rat cortical slices while
large-scale activity was imaged optically with fura-2 AM. Here I show
that activation of muscarinic acetylcholine receptors results in waves
of correlated neural activity. Waves recruit large numbers of neurons,
are slowly propagating, regenerative events involving depolarization
and associated calcium transients, and advance for many millimeters as
a sharp wave front perpendicular to the pial surface, at speeds ranging
between 50 and 300 µm/sec. The expression of waves is restricted
temporally to a brief period in postnatal development, until postnatal
day 6, and spatially to some neocortical areas. The ability of isolated
neocortical networks to generate large-scale patterned activity
endogenously during a period of massive neurite extension and
synaptogenesis raises the possibility that at least in some cortical
areas these processes might be influenced by patterned neuronal firing
generated independently of thalamocortical input.
Key words:
spontaneous activity; waves; neocortex; acetylcholine; muscarinic; calcium; fura-2; voltage-sensitive dyes; patch clamp; imaging
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INTRODUCTION |
The
complex neural circuits of the cerebral cortex and the connections
between them and other parts of the nervous system are constructed over
an extended period, both before and after birth, during which
genetically programmed molecular cues and electrical activity interact
in as yet poorly understood ways to guide axons to their targets and
refine patterns of synaptic connectivity. The role of activity in
circuit formation was first shown in the visual system with the
demonstration that controlled changes in visual experience modify the
pattern of projections from thalamus to cortex in stereotyped ways
(Wiesel, 1982 ). Subsequent to this finding, other investigations have
revealed that activity-dependent developmental processes are operating
and might contribute to circuit formation in sensory pathways even
before the time when sensory stimulation becomes a major driving force
behind the activation of those pathways (Rakic, 1976; Stryker and
Harris, 1986; Sretavan et al., 1988). This apparent paradox has led
more recently to an interest in the presence of endogenous activation
in immature circuits and the spatiotemporal patterns characteristic of
this type of activity. Characterization of the various modes of
endogenous circuit activation now seems essential for understanding the
full extent of the role that activity plays in shaping aspects of
circuit development as diverse as gene expression (Buonanno and Fields, 1999), axonal pathfinding (Catalano and Shatz, 1998; Dantzker and
Callaway, 1998), and circuit refinement (Ruthazer and Stryker, 1996;
Penn et al., 1998; Cook et al., 1999). The results of this study
demonstrate that, at least in vitro, endogenous patterned electrical activity can arise in immature neocortical circuits in
response to cholinergic activation.
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MATERIALS AND METHODS |
Long-Evans rat pups aged 0-10 d (day 0 = day of birth)
were used to prepare 300-µm-thick brain slices. The plane of section was coronal, and slices were made to include the parietal region. No
attempt was made to distinguish among functional areas within parietal
cortex. Slices were incubated in artificial CSF (aCSF) containing fura-2 AM (5 µg/ml) for 1-2 hr at 30°C. Composition of
the aCSF was (in mM): NaCl 125, KCl 2.5, NaHCO3 26, KH2PO4 1.25, MgCl2-6H20 1, CaCl2 2, D-glucose, 10, pH 7.4, bubbled with O2/CO2. Slices
were then placed on a temperature-controlled (30 ± 1°C)
perfusion chamber (rate: 2-3 ml/min.; volume: 200-400 µl) on the
microscope (Zeiss Axioskop FS) stage and viewed with a 20×
water-immersion objective. A 0.5× magnification adapter was placed in
front of the camera to obtain a larger (750 × 750 µm) image
area. Optical recordings were made using a cooled CCD digital camera
(512 EFT, Princeton Instruments) and IPLab Software
(Scanalytics). For single-wavelength acquisition, image sequences
consisted of 700 frames and were acquired continuously for 140 sec (200 msec integration time per frame). Camera was operated on 4 × 4 pixel binning mode. All fluorescence measurements were taken from
regions of interest containing multiple neurons and represent average pixel intensity over time for regions ~50 × 50 µm located in
supragranular layers.
All fura-2 wave activity was recorded at a single excitation wavelength
using a 380 ± 5 nm bandpass filter. Control experiments recorded
using a 360 ± 5 nm excitation filter (isosbestic point for
fura-2) showed no signals in response to cholinergic
agonists. Emission fluorescence was filtered with a 400 nm longpass filter.
For imaging of voltage signals, slices were stained for 5 min with the
voltage-sensitive dye di-4-ANEPPS (Fluhler et al., 1985) (0.66 mg/ml in aCSF) while in the perfusion chamber, and only after a
wave-expressing region had been located using fura-2 imaging. Wave
activity was imaged immediately, after a 5 min wash period, to minimize
artifactual signals attributable to gradual internalization of the dye
and photodynamic damage (Schaffer et al., 1994). For dual
fura-2/di-4-ANEPPS recordings excitation filters (380 ± 5 and
546 ± 5 nm) were alternated every 0.5 sec, and a single emission
filter (590 nm longpass) was used. Neutral density filters were used to
equalize fura-2 and di-4-ANEPPS signal intensities and to minimize photobleaching.
For whole-cell current-clamp recordings, patch pipettes were pulled
from borosilicate glass (3-5 M[SCAP] ) and filled with an internal solution containing (in mM): K gluconate 110, KCl 20, HEPES 10, EGTA 10, CaCl2 1, MgCl2 1, pH 7.2; osmolarity was adjusted to 307 mOsm with sucrose. Signals were amplified with an Axopatch 200A
patch-clamp amplifier (Axon Instruments) and acquired using Synapse
(Synergy Research) and an ITC-16 computer interface (Instrutech Corporation).
Drug application was synchronized to imaging using Synapse and began 10 sec after the start of imaging to allow acquisition of baseline
fluorescence values. The interval between applications was at least 5 min.
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RESULTS |
Fluorescence imaging at low magnification was used to visualize
population activity in coronal slices of immature rat neocortex stained
with the cell-permeant calcium indicator dye fura-2 AM. Under control
conditions, no large-scale patterned activity was observed in immature
neocortical slices. The rationale for testing cholinergic agonists in
neocortex was that in retina, blockade of nicotinic acetylcholine
receptors eliminates spontaneous activity waves, suggesting that
acetylcholine is necessary for their expression (Feller et al., 1996).
To mimic activation of cholinergic inputs to neocortex in slices, where
such inputs are not preserved, the nicotinic and muscarinic cholinergic
agonist carbachol (CCh) was bath-applied for periods varying in length
from 5 to 60 sec while activity was being recorded optically over a
750 × 750 µm area of neocortex.
The results obtained with CCh are described below along with results
obtained with the cholinergic agonist muscarine, which was used to
determine whether the cholinergic involvement was mediated through
muscarinic or nicotinic receptors. Although both nicotinic and
muscarinic receptors are present and functional in immature neocortex
(van Huizen et al., 1994; Roerig et al., 1997), experiments using
muscarine yielded results that are indistinguishable from results
obtained with CCh.
Application of CCh (25 µM) or muscarine (20 µM) to 60 coronal slices that included parietal cortex
resulted in waves being recorded at 93 of 302 cortical sites (31%).
Typically, activity waves originated somewhere outside the camera's
field of view, entered at one edge of the imaged area, and continued
their advance outside this area (Fig.
1A). The direction of
wave advance was always parallel to the pial surface. The wave front,
which is therefore oriented perpendicular to the cortical layering,
moves at speeds that range between 50 and 300 µm/sec (125 ± 64 µm/sec, mean ± SD, n = 60 waves). In several
instances the imaged area happened to include the site of wave
initiation, enabling the initial evolution of a wave to be captured in
200-msec-long snapshots (Fig. 1B). These sequences
show that although agonist is applied throughout the slice, a wave
starts from an event involving a very small number of cells from where
activity radiates outward until a full-fledged horizontally moving
wavefront is attained, sometimes traveling for distances in excess of 3 mm.
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Figure 1.
Cholinergic agonists evoke waves of correlated
calcium transients in developing rat neocortical slices through
activation of muscarinic receptors. A, Time-lapse
sequence of changes in calcium-dependent fura-2 fluorescence during
carbachol (25 µM) superfusion in a P5 slice. Pial edge is
the top right margin. First frame (top
left) shows fura-2 fluorescence staining of imaged cortical
region in coronal section (cut across cortical layers). Subsequent
frames are difference images showing a wave advancing over this area of
cortex. White areas represent cells with largest
fluorescence change relative to prewave levels. Image dimensions
(A, B) are 750 × 750 µm.
B, Initiation of wave at a different cortical site shown
at 200 msec intervals. Dashed line on first frame marks
the pial edge of the slice. White areas represent cells
with fluorescence changes relative to previous frame. C,
Plot of changes in calcium-dependent fura-2 fluorescence over time
recorded at two sites situated 400 µm apart along the path of wave
advance. Arrowheads show beginning and end of 20 µM muscarine chloride application for 60 sec. Calibration
in C: 5%  F/F, 10 sec.
D, Antagonists for the m1 (pirenzepine, 0.1 µM) and m3 (4-DAMP, 2.5 nM) receptor
subtypes, but not the m2 (gallamine, 20 µM) or m4 (MT-3,
10 nM) subtypes, reversibly abolished muscarine-evoked
activity waves. Calibration in D: 5%
F/F, 20 sec.
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Graphic presentation of the time course of calcium-dependent fura-2
fluorescence changes (Fig. 1C) shows that the response to
cholinergic agonist has two phases. First, a few seconds after switching from normal superfusion solution to agonist-containing solution, a small increase (4-10%
F/F) in intracellular calcium occurs in
large numbers of cells throughout the extent of the imaged area. This
phase of the response occurs simultaneously throughout the field of
view, peaks within 5-10 sec, and decays slowly to baseline over the
next minutes even in the continuous presence of agonist, as has been
shown previously (Yuste and Katz, 1991). The second phase of the
response, when it shows up, appears with a highly variable delay and is
significantly larger (10-20% F/F),
possibly because more neurons are involved per sampled area. When the
time course of signals derived from two sites positioned along the
horizontal extent of cortex are aligned, the second phase, but not the
first, consistently shows a lag in onset at one site relative to the
other (Fig. 1C). This calcium transient, corresponding to
the traveling wave, has a fast rise and almost equally fast decay and
invariably rides on the short-latency, lower-amplitude phase of the
cholinergic response.
As expected, the broad spectrum muscarinic antagonist atropine (1 µM) blocked the response to muscarine and CCh
(n = 5 slices). To further narrow the receptor subtype
involved in the muscarinic response, four subtype-selective receptor
antagonists were tested. Antagonists to m1 (pirenzepine, 100 nM; n = 4) and m3 (4-DAMP, 2.5 nM; n = 5) both blocked
muscarine-induced waves in every instance (Fig. 1D).
Antagonists to m2 (gallamine, 20 µM;
n = 3) and m4 (MT-3, 10 nM; n = 2) failed to block
muscarine-induced waves. In the case of MT-3, however, it is unclear
whether, despite a 30 min preincubation, the large toxin (molecular
weight 7289.3 Da) gained sufficient access into the slice.
To investigate the relationship between age and incidence of wave
expression in developing neocortex, CCh or muscarine was applied to
slices from rats aged 0-9 d postnatal (P0-9). Data for each age group
were analyzed in terms of fraction of cortical sites where at least one
wave was elicited on superfusion of agonist (Fig.
2A). Typically (92% of
cases), sites were of one of two types: those in which waves were
elicited repeatedly on repeated agonist application, and those in which
waves could not be elicited despite repeated applications of agonist.
Both types of sites were found to coexist in individual slices until
P6-7. After P7, agonist application induced a short-latency,
small-amplitude response but no waves.
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Figure 2.
Expression of cholinergically induced waves is
restricted developmentally and spatially. A, Histogram
showing the fraction of sites at which one or more waves could be
elicited with cholinergic agonists at each age group. Data include
waves elicited with 25 µM CCh (n = 208) or 20 µM muscarine (n = 94).
Inset, Fura-2 signals from three representative neurons
(identified by their prominent apical dendrite) in response to a 15 sec
application of 50 µM glutamate (horizontal
bar) to a P10 slice demonstrate that the age-related decrease
in waves is not caused by a technical problem with fura-2 signaling.
Vertical bar, 5% F/F.
B, An example of a wave propagation boundary in
developing neocortex. Leftmost frame shows raw fura-2
fluorescence image of cortical area shown in subsequent frames. Note
absence of any obvious cytoarchitectonic boundary. Successive waves
induced in this cortical area (extent of area traversed shown in
green or red) show that boundaries can
exist between subregions of cortex even when both subregions express
wave activity, and that boundaries can be stable over time. Time of
occurrence is shown above each wave. Arrows under each
wave show direction of advance. Image dimensions are 750 × 750 µm.
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The finding that wave-expressing and nonexpressing sites can coexist in
single slices suggests that there are mechanisms within cortex that
restrict the propagation of waves to specific areas. This idea is
supported by 35 recordings in which waves were observed to end within
the field of view (Fig. 2B). Although no obvious cytoarchitectonic discontinuities could be observed at these sites, it
is not possible to determine in fura-2-stained slices whether wave
termination correlates with some functional boundary in cortex. An
interesting feature of wave termination sites in cortex is that they
can be stable for periods in excess of 1 hr (Fig.
2B).
To find out whether cholinergically induced waves involve electrical
activity, three types of experiments were performed. First, muscarine
responses were evoked in slices stained with both fura-2 AM and the
voltage-sensitive dye di-4-ANEPPS. Dual calcium and voltage recordings
in these slices (n = 5) demonstrate that a voltage
signal can be detected that is simultaneous with the high amplitude,
wave-associated calcium signal (Fig.
3A), indicative of
depolarization during waves. In contrast, no measurable voltage signal
is detected in association with the initial, low-amplitude part of the
cholinergic response. Second, current-clamp recordings from individual
neurons also show that during the passage of a wave, neurons fire a
burst of action potentials (Fig. 3B). Finally, a requirement
for depolarization and action potential firing during waves was
demonstrated by experiments in which waves were induced before and
during superfusion with the sodium channel blocker tetrodotoxin (TTX)
(n = 7). TTX eliminates the wave-associated calcium
transient and leaves the initial, smaller calcium response relatively
unaffected (Fig. 3C). The presence of electrical activity during waves suggests that the potential influence of activity waves on
the development of neocortex could go beyond an effect on the local
circuitry to include longer-range projections as well. The TTX
sensitivity of cholinergically induced waves also demonstrates that
this phenomenon is pharmacologically distinct from domains in
developing neocortex (Yuste et al., 1992) and from spreading depression
(Sugaya et al., 1975; Tobiasz and Nicholson, 1982).
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Figure 3.
Cholinergic waves are excitatory events involving
neuronal depolarization and firing. A, Simultaneous
calcium and voltage imaging during cholinergic stimulation. A change in
fluorescence signal, consistent with depolarization, occurs in the
voltage-sensitive dye di-4-ANEPPS (di-4-A) concurrent
with the wave-related calcium transient (second peak in
fura-2 trace). B, Whole-cell current-clamp recording
from a layer 2/3 neuron (bottom trace) obtained during a
muscarine-evoked wave, as shown in the simultaneous fura-2 response
(top trace). C, Blockade of the
wave-related fura-2 fluorescence transient, but not of the slower
cholinergic response, by the sodium channel blocker tetrodotoxin
(TTX, 1 µM). Calibration: 10%
F/F, 10 sec (A);
10% F/F, 25 mV, 10 sec
(B); 10% F/F,
20 sec (C).
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Acetylcholine acting through muscarinic receptors has been shown to
depolarize mature cortical neurons (McCormick, 1993). To test whether
large-scale depolarization of neurons in developing neocortex is a
sufficient stimulus for induction of waves, an excitatory
neurotransmitter, glutamate, was superfused instead of one of the two
cholinergic agonists during calcium imaging at sites previously
determined to express waves with muscarine (n = 5). The
glutamate stimulus, although capable of inducing a significant calcium
response, was unable to induce waves at these sites (Fig.
4A).
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Figure 4.
Ionotropic glutamate receptor activation is
neither necessary nor sufficient for induction of neocortical waves.
A, Comparison of responses to muscarine (20 µM) and glutamate (20 µM) at a single
cortical site. The two traces in each panel are mean fluorescence
values over time from two small regions of interest separated by 400 µm. Unlike muscarine (A1), which induces a traveling
calcium transient, glutamate (A2) induces a calcium
transient that occurs simultaneously throughout the slice (as shown by
superposition of traces from the two regions of interest).
B, Muscarine-induced wave in the presence of APV (25 µM) and CNQX (25 µM). Calibration: 20 msec,
5% F/F.
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To test the involvement of glutamatergic neurotransmission in the
spread of activity during waves, two ionotropic glutamate receptor
antagonists, APV (NMDA; 25 µM) and CNQX (non-NMDA; 25 µM), were bath-applied simultaneously during, as well as
for 10 min before, the application of muscarine (n = 6). As shown in Figure 4B, neurotransmission via
ionotropic glutamate receptors is not required for wave induction or propagation.
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DISCUSSION |
In the present study I have described the most salient features of
a newly discovered type of network activity in immature neocortex,
including its developmental profile, its spatiotemporal characteristics, and the muscarinic receptor subtypes involved in its
induction. Bursting patterns of neural activity similar to that
described here have been demonstrated in other immature neural circuits
including retina (Maffei and Galli-Resta, 1990; Meister et al., 1991),
spinal cord (O'Donovan et al., 1994; Milner and Landmesser, 1999), and
hippocampus (Ben-Ari et al., 1989; Garaschuk et al., 1998; Avignone and
Cherubini, 1999) (for review, see O'Donovan, 1999). Acetylcholine is
often involved in this activity, sometimes via nicotinic (retina,
spinal cord) and sometimes via muscarinic (hippocampus, neocortex)
receptors. As in other brain regions, cholinergic sources in neocortex
are present early (Dori and Parnavelas, 1989).
Much remains to be elucidated about the mechanisms responsible for
activity waves in neocortex. The type(s) of intercellular signaling
involved in wave propagation, for example, remains to be established.
The finding that ionotropic glutamate receptors do not appear to be
necessary is not too surprising in light of knowledge about other
excitatory mechanisms potentially available to immature neocortical
networks, including signaling via glycine, GABAA
and metabotropic glutamate receptors, and gap junctions (Peinado et
al., 1993; Owens et al., 1996; Flint et al., 1998). Unlike glutamate,
these mechanisms are expressed transiently in neocortex. Their
involvement therefore could also account for the developmental profile
of wave activity seen here. To determine what mechanisms are involved
in wave propagation, however, an experimental approach is needed that
can separate effects on wave propagation from effects on wave
initiation, an objective that cannot be accomplished through
application of receptor antagonists to the entire slice as was done here.
The inability of bath-applied glutamate to induce wave activity
suggests that for waves to occur the neural network may need to undergo
a transient change in excitability state in addition to depolarization.
One possibility is a switch into a burst-ready mode, in which neurons
are more likely to burst-fire in response to excitatory input; another
could be an enhancement in neurotransmitter release. Activation of
muscarinic receptors could accomplish either of these by reducing
specific potassium conductances (McCormick, 1993). Even if such an
effect by muscarinic receptors can be demonstrated during wave
activity, however, a complete description of wave physiology is
unlikely to emerge until the wave initiation foci can be characterized
more fully in terms of physiological properties unique to these sites.
The results presented here raise the intriguing possibility that
activity waves in immature neocortex may function in vivo, albeit in as yet unknown ways, as participants in the formation of
cortical circuits. An alternative interpretation of these results, one
that has been favored in interpreting different types of large-scale neuronal bursting behavior induced by GABAA
antagonists, potassium channel blockers, or low
[Mg2+]o, is that
this is an example of epileptic activity that is unlikely to occur
in vivo except as pathology. The possibility that
muscarine-induced waves are also unphysiological cannot be ruled out at
this stage. The evidence from retina and spinal cord, however, suggests
not only that limited seizure-like neuronal bursting at specific stages of cortical development may not be deleterious, but that it might in
fact be useful.
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FOOTNOTES |
Received Sept. 17, 1999; revised Nov. 2, 1999; accepted Nov. 10, 1999.
This work was supported by grants from National Institutes of Health
(MH53345 and NS319899). I thank Drs. Scott Nawy and Don Faber for
helpful discussions.
Correspondence should be addressed to Alejandro Peinado, Department of
Neuroscience, Room 522, Kennedy Center, Albert Einstein College of
Medicine, 1300 Morris Park Avenue, Bronx, NY 10461. E-mail:
peinado{at}aecom.yu.edu.
This article is published in
The Journal of Neuroscience, Rapid Communications Section,
which publishes brief, peer-reviewed papers online, not in print. Rapid
Communications are posted online approximately one month earlier than
they would appear if printed. They are listed in the Table of Contents
of the next open issue of JNeurosci. Cite this article as:
JNeurosci, 2000, 20:RC54 (1-6). The
publication date is the date of posting online at
www.jneurosci.org.
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I. Homma and Y. Masaoka
Breathing rhythms and emotions
Exp Physiol,
September 1, 2008;
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[Abstract]
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M. Minlebaev, Y. Ben-Ari, and R. Khazipov
NMDA Receptors Pattern Early Activity in the Developing Barrel Cortex In Vivo
Cereb Cortex,
July 28, 2008;
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[Abstract]
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M. Milh, A. Kaminska, C. Huon, A. Lapillonne, Y. Ben-Ari, and R. Khazipov
Rapid Cortical Oscillations and Early Motor Activity in Premature Human Neonate
Cereb Cortex,
July 1, 2007;
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[Abstract]
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M. Minlebaev, Y. Ben-Ari, and R. Khazipov
Network Mechanisms of Spindle-Burst Oscillations in the Neonatal Rat Barrel Cortex In Vivo
J Neurophysiol,
January 1, 2007;
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[Abstract]
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R. C. Stacy, J. Demas, R. W. Burgess, J. R. Sanes, and R. O. L. Wong
Disruption and Recovery of Patterned Retinal Activity in the Absence of Acetylcholine
J. Neurosci.,
October 12, 2005;
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[Abstract]
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M. Thoby-Brisson, J.-B. Trinh, J. Champagnat, and G. Fortin
Emergence of the Pre-Botzinger Respiratory Rhythm Generator in the Mouse Embryo
J. Neurosci.,
April 27, 2005;
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[Abstract]
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D. P. Calderon, N. Leverkova, and A. Peinado
Gq/11-Induced and Spontaneous Waves of Coordinated Network Activation in Developing Frontal Cortex
J. Neurosci.,
February 16, 2005;
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[Abstract]
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M. B. Feller
Retinal Waves Drive Calcium Transients in Undifferentiated Retinal Cells. Focus on "Spontaneous Waves in the Ventricular Zone of Developing Mammalian Retina"
J Neurophysiol,
May 1, 2004;
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M. Md. Syed, S. Lee, S. He, and Z. J. Zhou
Spontaneous Waves in the Ventricular Zone of Developing Mammalian Retina
J Neurophysiol,
May 1, 2004;
91(5):
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[Abstract]
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N. C. Spitzer
Coincidence detection enhances appropriate wiring of the nervous system
PNAS,
April 13, 2004;
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[Full Text]
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A. H. Meyer, I. Katona, M. Blatow, A. Rozov, and H. Monyer
In Vivo Labeling of Parvalbumin-Positive Interneurons and Analysis of Electrical Coupling in Identified Neurons
J. Neurosci.,
August 15, 2002;
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[Abstract]
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J. H. Singer, R. R. Mirotznik, and M. B. Feller
Potentiation of L-Type Calcium Channels Reveals Nonsynaptic Mechanisms that Correlate Spontaneous Activity in the Developing Mammalian Retina
J. Neurosci.,
November 1, 2001;
21(21):
8514 - 8522.
[Abstract]
[Full Text]
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A. Peinado
Immature Neocortical Neurons Exist as Extensive Syncitial Networks Linked by Dendrodendritic Electrical Connections
J Neurophysiol,
February 1, 2001;
85(2):
620 - 629.
[Abstract]
[Full Text]
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A. Bansal, J. H. Singer, B. J. Hwang, W. Xu, A. Beaudet, and M. B. Feller
Mice Lacking Specific Nicotinic Acetylcholine Receptor Subunits Exhibit Dramatically Altered Spontaneous Activity Patterns and Reveal a Limited Role for Retinal Waves in Forming ON and OFF Circuits in the Inner Retina
J. Neurosci.,
October 15, 2000;
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[Abstract]
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TOP
ABSTRACT
INTRODUCTION
