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1 Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218 2 Department of Biology, University of Utah, Salt Lake City, Utah 84112-0840
Submitted 26 March 2003; accepted in final form 9 May 2003
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ABSTRACT |
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INTRODUCTION |
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; Kim and Connors
1993; Magee and Johnston
1995; Turner et al.
1994). Correspondingly, these channels have been implicated in a
variety of functions beyond the classical role of generating axonal action
potentials (for review, see Reyes
2001). Specifically, dendritic voltage-gated sodium channels may
amplify synaptic inputs (Crill
1999; Gonzalez-Burgos and
Barrionuevo 2001; Lipowski et
al. 1996), actively promote propagation of action potentials into
dendrites (Stuart and Sakmann
1994), boost "graded" transmission in nonspiking
neurons (Zenisek et al. 2001),
and contribute to the bursting properties of central neurons
(Magee and Carruth 1999;
Turner et al. 1994).
The influences of dendritic sodium channels on the input–output
functions of neurons have been investigated primarily in vitro
(Hausser et al. 2000).
Accelerated by the use of wholecell patch recording methods
(Blanton et al. 1989;
Edwards et al. 1989), these
studies have provided valuable insight into the distributions of voltage-gated
channels and their regional effects on the transmission of electrical signals
in dendrites. Comparatively little is known, however, concerning the roles
that these dendritic channels play in the processing of information in vivo.
As with in vitro studies, in vivo intracellular investigations of this
question have been greatly aided by development of whole cell patch recording
methods (Rose and Fortune
1996).
The electrosensory system of gymnotiform fish is an excellent model for
exploring the role of voltage-gated sodium channels in information processing
in vivo. In social communication, Eigenmannia intermittently produce
brief interruptions or frequency modulations of their electric organ
discharges (EOD) (Hopkins
1974). The brief time course of these signals, coupled with the
comparatively long time constants of central neurons, make it likely that
amplification processes are needed to ensure transmission of this information
to higher centers. Active membrane properties, possibly involving
voltage-gated sodium channels, could mediate such amplification. These
channels have been found on the apical dendrites of pyramidal neurons in the
electrosensory lateral line lobe (firstorder central electrosensory area)
(Turner et al. 1994), where
they contribute to the oscillatory properties of these cells and amplify
excitatory postsynaptic potentials (EPSPs) arising from inputs to the apical
dendrites (Berman et al. 2001).
Little is known, however, about the potential roles of voltage-gated
Na+ channels in other electrosensory neurons.
Previous whole cell intracellular recordings from neurons in the upper
layers of the midbrain torus semicircularis suggest that active membrane
properties amplify EPSPs triggered by sensory stimuli
(Fortune and Rose 1997a). In
these recordings, postsynaptic potential (PSP) amplitude was amplified in an
all-or-none fashion at resting potential or with low levels, typically less
than –0.2 nA, of negative current clamp. The duration of these
all-or-none (regenerative) PSP components was either variable or constant
across temporal frequency of stimulation, depending on the cell type. The
variable-duration (VD) form principally amplified the responses of cells to
low temporal frequencies of stimulation, whereas the constant-duration (CD)
type enhanced the responses to higher temporal frequencies. CD all-or-none
EPSPs (approximately 20–60 ms in duration, 20–40 mV in amplitude)
were often elicited, under negative current clamp, in the absence of spikes.
We interpret these findings as indicating that the soma and spike initiation
zone were sufficiently hyperpolarized to prevent action potential generation,
and that the all-or-none CD EPSP components were most likely generated at
electrotonically distant sites in the dendrites; current injected at the soma
likely produced less hyperpolarization of these dendritic compartments.
In this study, we tested the hypothesis that voltage-gated sodium channels
contribute to the all-or-none PSP components of toral neurons by making
whole-cell intracellular recordings, in vivo, with patch-type pipettes that
contained either QX-314 or QX-222. These quatenary ammonium derivatives block
voltage-gated sodium channels when applied to the inside of neurons
(Narahashi et al. 1972;
Strichartz 1973), and have
been used in intracellular studies of central neurons
(Connors and Prince 1982).
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METHODS |
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,b;
Heiligenberg and Rose 1985;
Rose and Call 1993;
Rose and Fortune 1999). Fish,
approximately 1 yr old, of the genus Eigenmannia were used. Animal
husbandry, anesthesia, and surgical procedures were performed under the
guidelines established by the Society for Neuroscience.
For experiments, a fish's EOD was measured and then attenuated
(
1000-fold) by intramuscular injection of Flaxedil (4 µg/g fish).
Additional injections of Flaxedil were made during the experiment as necessary
to maintain the attenuation of the EOD. The fish's EOD was replaced by a
sinusoidal mimic (S1) that was delivered through electrodes placed at the tail
and in the mouth. The amplitude and frequency of the S1 were adjusted to
approximate the fish's EOD before the injection of Flaxedil. Additional
electrosensory stimuli were delivered through an array of carbon electrodes
that surrounded the fish. Water temperature was held near 25°C.
At the conclusion of the experiment, not more than 4 h after the first neuron was filled, animals were deeply anesthetized by flow of 4% wt/vol urethan across the gills. Animals were perfused transcardially with saline-heparin solution followed by 4% wt/vol paraformaldehyde in 0.2 M phosphate buffer (pH = 7.4). After perfusion, the brain was removed and stored at 4°C overnight in the paraformaldehyde solution. Sections, 100 µm thick, were cut on a vibratome and reacted using an avidin-biotin peroxidase kit (Elite PK-6100; Vector Laboratories, Burlingame, CA). Sections were dehydrated, cleared in xylenes, mounted on slides, and coverslipped.
Intracellular recording procedures
"Whole cell" recordings were made with patch-type pipettes, as
described in detail by Rose and Fortune
(1996). Seal resistances of 1
G
or more were typically achieved. Intracellular recordings were made
from neurons in the dorsal 5 layers of the torus semicircularis of adult
Eigenmannia. Patch pipettes for intracellular recording were
constructed from borosilicate capillary glass (A-M systems No. 5960; 1 mm OD,
0.58 mm ID) using a Flaming-Brown type puller (model P-97; Sutter
Instruments). Electrodes were pulled to resistances between 15 and 25
M. Electrode tips were back-filled with a solution (pH = 7.4)
consisting of (values in mM) 100 potassium acetate or potassium gluconate, 2
KCl, 1 MgCl2, 5 EGTA, 10 HEPES, 20 KOH, either QX-314 (bromide
salt, 1–40 mM) or QX-222 (chloride salt, 2 mM), and biocytin at a
concentration to bring the final osmolarity to approximately 285 mosmol.
Biocytin and the QX compounds were replaced by mannitol in the solution used
to fill pipette shanks.
Electrodes were mounted in a Plexiglas holder with a "pressure" port. This port allowed the application of pressure pulses (40–80 ms, 40 psi) from a Picospritzer (General Valve) or the manual application of suction or pressure from a 30-ml syringe. The electrode was advanced in 1.5-µm steps (Burleigh 6000 microdrive) through the dorsal 5 layers of the torus. Responses were amplified using an electrometer (model 767; World Precision Instruments, Sarasota, FL) and stored on videotape at 40 kHz with 16-bit resolution (model 3000; Vetter Instruments).
Initially, recordings were made at several levels of negative holding
current (generally less than –0.3 nA). This procedure enabled us to
determine whether voltage-dependent conductances contributed to
stimulus-driven PSPs; in experiments where QX drugs were placed into the
recording electrode, the negative current also limited the diffusion of the
positively charged QX compounds into the cell. In experiments without QX
drugs, sinusoidal current, 0.1 nA peak-to-peak, was injected into the neuron
by the recording electrode. Current sinusoids matched the temporal structure
of sensory stimuli, ranging from 2 to 30 Hz. In recordings with QX drugs, the
negative holding current was removed after the baseline recording period.
Sensory stimulation was continued, thereby eliciting large, all-or-none
depolarizations and spiking. These depolarizations appear to accelerate the
progression of sodium channel blockade. The amplitude of spikes was monitored
to determine the activity of QX drugs in the neuron. In cases where spike
amplitude did not drop within 2 min, positive current (<0.2 nA) was applied
for 
1 min to facilitate QX transfer into the neuron. At the conclusion of
each intracellular recording, neurons were filled with biocytin by applying 1
to 2 nA of positive DC for 1 to 3 min.
Sensory stimuli
The search stimulus was designed to elicit responses from both ampullary and tuberous neurons in the torus. The ampullary component of the search stimulus was a linear frequency sweep (2–30 Hz, 10-s duration, 1–2 mV/cm at the fish's head) that was added to the S1 and presented through the electrodes in the mouth and at the tail. The tuberous component was the S1 and a sine wave (S2) 4 Hz higher than the S1 frequency. The S2 was delivered concurrently through one pair of the array of carbon electrodes surrounding the fish. Addition of the S2 and the S1 resulted in broad-field amplitude and phase modulations at a rate equal to the difference in frequencies of the S1 and S2; the modulation frequency is known as the "beat rate."
Once a recording was established, the best stimulus (ampullary or tuberous)
and the stimulus orientation were determined. Stimulus orientation was chosen
to elicit the strongest and most consistent responses from the neuron. The
data presented here and in previous reports (Fortune and Rose
1997a,b;
Rose and Fortune 1999)
indicate that the temporal filtering properties of ampullary and tuberous
neurons in the torus are highly similar.
Responses were first recorded while the stimulus frequency (ampullary) or beat rate (tuberous) was linearly scanned from about 2 to 30 Hz. These "sensory scans" were 5 s in duration. Subsequently communication-like stimuli were delivered. These stimuli were generated by "interrupting" an ongoing sinusoidal signal at intervals of about 50 ms. During each interruption, the signal voltage was held briefly at the level that existed when the interrupt command occurred. The "hold voltage" was varied gradually from positive to negative values.
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RESULTS |
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In a previous study, about 1/3 of neurons recorded in the dorsal 5 layers
of the torus showed marked "all-or-none" (regenerative) EPSPs in
response to electrosensory stimuli (Fortune
and Rose 1997a). In the present study, these PSPs were identified
by recording at several levels of negative current clamp (0.0 to –0.4
nA) while presenting an electrosensory stimulus. The stimulus-related PSP
amplitude in those neurons with regenerative components dropped dramatically
when the negative holding current was increased beyond a particular value;
compare recordings at –0.3-nA versus –0.4-nA current clamp
(Fig. 1A). As in
previous studies, regenerative PSPs were divided in two classes, constant
duration (CD, Fig. 1) and
variable duration (VD, Fig. 2).
Stimulus-related PSP amplitudes in neurons without significant regenerative
components, however, increased as the level of negative current clamp was
increased.
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As reported previously (Fortune and Rose
1997a), the duration, measured at 1/2 maximum amplitude, of CD
PSPs varied little with respect to the periodicity (frequency or beat rate) of
the sensory stimulus (Fig. 1).
CD PSPs range from 20 to 60 ms across neurons. In contrast, VD PSP duration
varied inversely relative to the sensory stimulus periodicity; low stimulus
frequencies (4 Hz) elicited longer-duration VD PSPs (150 ms) and high
frequencies (30 Hz) elicited shorter-duration PSPs (10 ms).
Induction of regenerative PSPs by current injection
To determine whether regenerative PSP components could be elicited by membrane depolarization, sinusoidal current, 0.1 nA peak-to-peak, was injected into three neurons with CD PSPs and three neurons with VD PSPs. Sinusoidal current injection closely matched the temporal structure of the sensory stimuli shown in Fig. 1A. The DC offset (holding current) of this sinusoidal signal was between +0.05 nA and –0.4 nA in each experiment.
Sinusoidal current injection into neurons with CD PSPs elicited regenerative depolarizations that appear to be identical to those elicited by sensory stimuli (Fig. 1A). Sinusoidal current injection failed, however, to trigger regenerative depolarizations in neurons that showed VD PSPs in response to sensory stimulation.
One neuron appeared to have both VD- and CD-type PSPs
(Fig. 2). In this neuron low
stimulus frequencies elicited long, variable-duration PSPs, and higher
stimulus frequencies elicited shorter, constant-duration PSPs
(Fig. 2A). Typically,
VD PSPs are not elicited by stimulation frequencies of greater than about 10
Hz, whereas CD PSPs are most common at 15 to 30 Hz. Interestingly, subsequent
sinusoidal current injection elicited regenerative PSPs with short (50
ms) durations, even at low stimulation frequencies
(Fig. 2B), and did not
elicit the variable-duration PSPs. Comparison of PSPs elicited by sensory
stimulation and voltage responses elicited by current injection suggest that
the long-duration PSPs seen in response to low temporal-frequency sensory
stimuli were composed of a combination of CD and VD type regenerative PSPs
(Fig. 2, inset).
Behavioral significance of regenerative PSPs
To determine whether social communication signals ("chirps") elicit CD PSPs, synthesized chirps, short interruptions of a sinusoidal signal, were presented. Such stimuli were effective in eliciting CD PSPs and spikes (Fig. 3). Responses were largest when the interruption consisted of holding the voltage of the stimulating signal at its most negative value (see stimulus traces, Fig. 3). The time course of these PSPs was largely independent of the duration of these stimulus "interruptions" (compare traces in Fig. 3, A and B).
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At a current clamp level of –0.2 nA, 2.5- and 5-ms interruptions (stimulus voltage held at most negative value) reliably elicited regenerative PSPs and spikes. At a holding current of –0.4 nA, however, the shorter interruptions failed to elicit spikes on 7 of 8 presentations; a representative recording is shown in the bottom panel of Fig. 3A. At this holding current, 5-ms interruptions triggered regenerative PSPs and spikes on 4 out of 8 presentations. The components of stimulus-driven PSPs that were contributed by active membrane properties can be viewed by comparing the amplitudes of PSPs that were elicited by the 2.5- and 5-ms interruptions (bottom panels).
Previous experiments (Fortune and Rose 1997) demonstrated that low temporal-frequency stimuli, such as those that elicit the jamming avoidance response (JAR), also can elicit VD PSPs.
Effects of QX drugs
QX drugs were applied intracellularly to 17 neurons with regenerative PSP components; 6 cells had CD-type PSPs and 11 had VD types. The QX drugs eliminated spikes in all classes of neurons, including neurons without regenerative PSPs. At 1- to 2-mM concentrations (pipette) of these drugs, spike amplitude and rate diminished over periods from as little as 2 min to more than 20 min in these recordings. Elimination of spikes was accelerated in many neurons when positive current was injected into the cell to increase spiking activity.
In neurons with CD PSPs, there was a concomitant decrease in the amplitude and rate of occurrence of the regenerative components and spikes. Constant-duration PSPs and spikes were completely, or almost completely, eliminated in all 6 neurons in <20 min (Fig. 4). The shapes of the remaining PSPs were similar to those recorded at negative-current clamp values sufficient for eliminating regenerative PSP components; the latter recordings were made before the QX drugs had taken effect.
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In all neurons with VD PSPs, spikes were eliminated but VD PSPs were not (Fig. 5). VD PSPs were qualitatively unchanged after the application of QX drugs. These PSPs were larger, however, after QX delivery, apparently because of a small increase in the cells' input resistance. The durations and the insensitivity to current injection of VD PSPs appeared unchanged in recordings of more than 30 min after the elimination of spikes by the QX drugs. The all-or-none nature of these VD-type PSP components is evident in the recordings at –0.1-nA current clamp, where they are elicited on some stimulus cycles, but not on others. This amplification of PSP amplitude is absent at –0.2-nA current clamp.
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DISCUSSION |
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)
revealed prominent all-or-none (regenerative) EPSP components that amplified
their low-pass or band-pass temporal filtering properties; hyperpolarization
eliminated these components. Such results could be attributed to a
positive-feedback network process, requiring the activity of the neuron that
was being recorded, or active membrane properties of the neuron itself.
Because hyperpolarization also eliminated spiking, it was difficult to
distinguish between these two possibilities. On the grounds that regenerative
PSPs were often elicited either in the absence of spiking or before the
occurrence of spikes, we speculated that they resulted from active membrane
properties and not a positive-feedback network.
Intracellular delivery of QX-314 or QX-222 eliminated spiking but failed to
attenuate the amplitude of the VD all-or-none PSP components; thus, VD PSPs
cannot result from positive feedback. The CD PSPs, however, were eliminated by
the application of QX drugs. This result is consistent with both mechanisms:
either a positive feedback network or voltage-gated Na+ channels.
Because the CD PSPs could also be triggered by current injection in the
absence of spiking, however, they appear to be the result of active membrane
properties (Golding et al.
1999). These lines of evidence thus support the hypothesis that
voltage-gated Na+ channels are responsible for the CD-type
PSPs.
Based on the differences in the frequency dependency and time course of regenerative PSPs, we previously proposed to divide these in two distinct physiological classes. This conclusion is strengthened by our present findings that QX drugs eliminated the CD regenerative-type PSPs, but not VD PSPs. These findings also suggest that voltage-gated sodium channels are primarily responsible for CD PSPs.
The validity of this latter conclusion depends on the selectivity of QX
compounds for blocking voltage-gated sodium channels. At concentrations of 10
mM, QX-314 has been shown to partially block (<45% of control)
low-threshold calcium currents in hippocampal pyramidal neurons
(Talbot and Sayer 1996). In
other studies, however, QX-314 effectively blocked sodium currents without
attenuating calcium currents (Seamans et
al. 1997). Although the origins of these differences are unclear,
collectively they suggest that these drugs at low concentrations should not
appreciably attenuate calcium currents. In our study, QX-314 and QX-222 at
concentrations of 1–2 mM completely eliminated the constantduration,
regenerative PSP components. If these depolarizations were primarily a result
of the activity of calcium currents, then, at most, only a partial reduction
should have been observed. The possibility still remains, however, that
high-threshold calcium conductances are also activated by depolarizations that
result from the opening of voltage-gated sodium channels
(Svoboda et al. 1999); QX
agents, in blocking sodium channels, could preclude the normal opening of
high-threshold calcium channels. Thus, although we cannot entirely rule out a
contribution of calcium conductances, it appears that voltage-gated sodium
channels are primarily responsible for generating these large PSP
components.
The sodium channel–dependent, regenerative potentials of toral
neurons are highly similar to those recorded in vivo from burst-type neurons
in the somatosensory cortex of rats (Zhu
and Connors 1999). In whole cell recordings in both systems, fast,
small spikes often "ride" on much larger regenerative potentials,
suggesting that the latter are generated in the dendrites. In vitro studies of
cortical neurons suggest that these dendritic, regenerative potentials are
mediated by sodium and calcium conductances
(Kim and Connors 1993).
What properties of the conductances that result in VD PSPs can we infer
from the available evidence? VD PSPs do not likely result from Na+
conductances because they were not blocked by the application of QX drugs. VD
PSPs were also not triggered by voltage fluctuations alone. Evidence from this
study and from previous work (Fortune and Rose 2000) demonstrate that VD PSPs
are elicited by stimuli that include concurrent synaptic input. We speculate,
therefore, that the conductances underlying VD PSPs require both synaptic
input and depolarization for activation. These properties are consistent with
the hypothesis that N-methyl-D-aspartate receptors
(NMDARs) generate the conductances that result in appearance of VD PSPs. NMDAR
immunoreactivity has been described in the dorsal layers of the torus in a
related species, Apteronotus leptorhynchus
(Bottai et al. 1997;
Maler and Monaghan 1991;). The
hypothesis that VD PSPs are mediated by NMDARs is best tested using in vitro
recordings of neurons in living brain slices, where the application of
transmitters and receptor agonists can be used to directly assess and
characterize the ionic and synaptic bases for the PSPs.
The role of dendritic sodium channels and regenerative potentials
Dendritic sodium channels have been demonstrated in many types of central
neurons (for review, see Hauser et al. 2000). These channels are, in many
cases, distributed along the dendritic axis in a nonuniform and cell-specific
manner, and generate dendritic spikes. There are two schools of thought
pertaining to how these dendritic spikes are triggered during information
processing. In one model, dendritic sodium channels sustain back propagation
of axonal and/or somatic spikes into the dendrites. A competing, although not
mutually exclusive, model posits that sodium channel–dependent spikes
are triggered by synaptic input and thus serve to amplify relevant patterns of
synaptic input. Although these spikes may be generated in vitro after afferent
stimulation, it is unclear whether such potentials actually occur in the
intact system in response to normal patterns of synaptic input
(Kamondi et al. 1998).
Ultimately, recordings from these neurons under in vivo conditions of normal
information processing are needed to resolve this debate.
In the electrosensory system, these regenerative potentials can be
triggered by sensory stimulation and serve to amplify biologically meaningful
synaptic input (Fortune and Rose
1997a). This amplification enhances the band-pass temporal
frequency selectivity of some electrosensory neurons in the midbrain. Most
important, signals that these fish use in social communication (particularly
reproductive behavior), for instance, brief cessations of the fish's EODs, are
particularly effective in triggering the regenerative, presumably dendritic,
sodium "spikes" in midbrain neurons. These in vivo findings thus
support the hypothesis that regenerative, sodium channel–dependent
dendritic potentials can be elicited by particular patterns of biologically
meaningful synaptic input to neurons, and serve to amplify this
information.
We cannot ascertain from the in vivo recordings, however, whether voltage-gated sodium channels amplify distal synaptic inputs to dendrites versus those to the proximal dendrites and/or soma. In vitro intracellular recordings with patch-type pipettes are needed to directly identify the distribution of these channels and resolve this issue.
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DISCLOSURES |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests: E. S. Fortune, Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles Street, Baltimore, MD 21218 (E-mail: eric.fortune{at}jhu.edu).
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M. J. Chacron Nonlinear Information Processing in a Model Sensory System J Neurophysiol, May 1, 2006; 95(5): 2933 - 2946. [Abstract] [Full Text] [PDF]
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