Download Direct Inhibition Evoked by Whisker Stimulation in Somatic Sensory

Direct Inhibition Evoked by Whisker Stimulation in Somatic Sensory
(SI) Barrel Field Cortex of the Awake Rat
ROBERT N. S. SACHDEV,1 HEIKE SELLIEN,2 AND FORD F. EBNER3
Institute for Developmental Neuroscience, Vanderbilt University; 2Institute for Molecular Neuroscience, Vanderbilt
University School of Medicine; and 3Department of Psychology, Vanderbilt University, Nashville, Tennessee 37240
1
Received 6 January 2000; accepted in final form 19 May 2000
INTRODUCTION
The cortical representation of each whisker in the rodent
somatic sensory (SI) cortex has been referenced to clusters of
neurons in layer IV (called barrels by Woolsey and Van der
Loos 1970) that respond to deflection of whiskers on the
contralateral face (Welker 1971). Extracellular recordings in
awake-alert (Fanselow and Nicolelis et al. 1999; Fee et al.
1997; Nicolelis et al. 1995; Simons et al. 1992), awake-paralyzed (Simons 1978), and anesthetized (Armstrong-James and
Fox 1987; Ito 1985; Welker 1971) rats show that neurons in
barrels typically respond to principal whisker deflection by
increasing their discharge rate 6 –10 ms after the deflection.
GABAergic inhibition typically follows the excitatory discharge thereby creating an “inhibitory trough” in the cumulative spike profile of a poststimulus time histogram (Carvell and
Address for reprint requests: F. F. Ebner, Dept. of Psychology, 301 Wilson
Hall, 111 21st Ave. South, Vanderbilt University, Nashville, TN 37240 (Email: [email protected]).
www.jn.physiology.org
Simons 1988; Simons 1978, 1985). Deflection of nonprincipal
whiskers in the receptive field (RF) of cortical neurons, the
excitatory “surround” whiskers, also increases cortical discharge rate, but at a longer latency and a lower magnitude than
the principal whisker (Armstrong-James and Fox 1987). Using
a two whisker stimulation paradigm Simons and colleagues
have shown that surround whiskers can produce inhibitory
interactions between neurons in adjacent barrels and septa
(Brumberg et al. 1999; Simons 1985). The response evoked by
principal whisker deflection is much reduced if an adjacent
whisker is deflected 2–50 ms before the principal whisker
(maximum inhibition ⬃20 ms). These results raise the possibility that stimulation of whiskers could directly inhibit the
spontaneous discharge of cortical neurons under some conditions.
Intracellular recordings in vivo from anesthetized rats indicate that the initial response of barrel neurons to whisker
deflection is typically an excitatory postsynaptic potential
(EPSP) (Carvell and Simons 1988; Moore and Nelson 1998;
Zhu and Connors 1999; Zhu and Sakmann 1998). EPSPs are
followed by an inhibitory potential (IPSP); in fact EPSP-IPSPEPSP sequences have been described in several cortical areas,
including rat barrel cortex and cat SI whisker cortex (Hellweg
et al. 1977; Zhu and Connors 1999; also see Kleinfeld and
Delaney 1996). However, another sequence of events following whisker stimulation has also been described. An in vivo
study using whole cell patch recording methods reported that 1
of 24 cortical neurons responded to a single whisker exclusively with IPSPs (Moore and Nelson 1998). Stimulation of
thalamocortical fibers in brain slice preparations have also
evoked solitary IPSPs in SI cortex (Agmon and Connors 1992).
Here we present evidence from extracellular recordings in
awake rats for suppression of spontaneous discharge following
whisker stimulation, without any preceding excitation.
METHODS
All methods were approved by the University Animal Care Committee and were in accordance with NIH approved procedures.
Habituation to restraint
Male rats (n ⫽ 5) were handled every day for a week and placed on
a reduced diet. Rats were habituated to being restrained by wrapping
The costs of publication of this article were defrayed in part by the payment
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0022-3077/00 $5.00 Copyright © 2000 The American Physiological Society
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Sachdev, Robert N. S., Heike Sellien, and Ford F. Ebner. Direct
inhibition evoked by whisker stimulation in somatic sensory (SI)
barrel field cortex of the awake rat. J Neurophysiol 84: 1497–1504,
2000. Whisker deflection typically evokes a transient volley of action
potentials in rat somatic sensory (SI) barrel cortex. Postexcitatory
inhibition is thought to quickly terminate the cortical cell response to
whisker deflection. Using dual electrode extracellular recording in
awake rats, we describe an infrequent type of cell response in which
stimulation of single hairs consistently blocks the ongoing discharge
of neurons without prior excitation (I-only inhibition). Reconstruction
of the recording sites indicates that I-only inhibition occurs most
frequently when the recording site is clearly in the septum or at the
barrel-septum junction. The same cells that respond with I-only inhibition to one whisker can show an excitatory discharge to other
whiskers, usually followed by inhibition. Stimulation of either nose
hairs or the large mystacial vibrissa can evoke I-only inhibition in SI
cortex. I-only inhibition is most commonly observed at low stimulus
frequencies (⬃1 Hz). At stimulus frequencies of ⬎6 Hz, I-only
inhibition typically converts to excitation. We conclude that single
whisker low-frequency stimulation can selectively block the spontaneous discharge of neurons in SI barrel field septa. The observation
that this cell response is found most often in or at the edge of septa and
at relatively long latencies supports the idea that I-only inhibition is
mediated through cortical circuits. We propose that in these cells
inhibition alone or a combination of inhibition and disfacilitation play
a role in suppressing neuronal discharge occasioned by low frequency
contact of the whiskers with the environment.
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Electrodes were advanced in 75 ␮m steps. After cells in 3–5
depths had been sampled, lesions were placed at the bottom of each
electrode penetration (3 ␮A, for 10 s). To distinguish between the
two tracks, one of the two electrodes was advanced by 300 ␮m, the
other was retracted by 300 ␮m, and a second lesion was made. The
animal was killed with carbon dioxide, perfused with 0.1 M
phosphate buffer, and the brain fixed with 4% paraformaldehyde.
Once the brain sank in 30% sucrose, the cortex was removed,
flattened between slides, and cut into 50 ␮m thick sections tangential to the cortical surface on a freezing microtome. Brains were
stained for cytochrome oxidase (Wong-Riley and Welt 1980) and
electrode tracks were reconstructed from serial sections. All data
included in this paper are from animals with electrode tracks
reconstructed and localized in the barrel field. In every case it was
possible to specify whether a recording site was in a barrel or
septum.
Data acquisition and analysis
a towel around the animal and placing them in a loosely fitting cloth
bag. The rat in the bag was slid into a loose fitting plastic tube where
they were offered chocolate milk during the restraint from a lick tube.
Restraint was kept as short as possible, typically 20 –30 min of licking
chocolate milk; rats gained 20 –30 g in a session. Once rats demonstrated that they would lie quietly and drink chocolate milk, they were
prepared for surgery. Rats were anesthetized with pentobarbital sodium (Nembutal, 50 mg/kg) and a craniotomy was made over SI
cortex. Five small holes were made in the skull, three over the
cerebellum and two over rostral locations near the olfactory bulbs.
Holes in the skull were tapped and blunt tipped screws were inserted.
Using dental acrylic, a head post was fixed over the cerebellum
(Bermejo et al. 1996) and a chamber was placed over the craniotomy.
The chamber was sealed by a cap that could be unscrewed to give
daily access to the exposed dura. Once animals recovered from the
surgery, they were reacclimated to the restraint. Animals were monitored during head post restraint to see if they showed any signs of
distress. Animals that frequently moved or made noises when their
head was immobilized were eliminated from this study.
Recording
Rats were awake, quiet, and restrained during recording (Fig. 1).
They were fed chocolate milk during the recording session between
epochs of whisker deflection. Two miniature screw-advance microdrives were mounted into grids fitted over the chambers. When
screwed onto the grids, the microdrives independently advanced single tungsten wire electrodes (FHC) into the cortex. At the outset
electrode tips were separated by roughly 1 mm. As the electrodes
penetrated through the dura, neuronal responses could be heard on an
audio monitor in response to manual stimulation of the whiskers. For
each electrode one whisker was selected as the principal whisker
based on the response magnitude.
At the outset a period of spontaneous discharge was recorded for
each neuron. The principal whisker for each electrode was deflected
(⬃3 mm for 30 ms) at 1 of 8 stimulus frequencies (0.5, 1, 3, 6, 9, 12,
15, and 18 Hz) with an air puff stimulator constructed inhouse (James
Long Company, Caroga Lake, NY). Data were collected for 50 s at all
stimulus frequencies. Air puffs at each frequency in succession were
directed from above the whisker pad. Whiskers were observed
through an operation microscope throughout recording to ensure that
only one whisker moved.
FIG. 2. Autocorrelation histograms. Examples of 4 autocorrelations from 4
of the single units illustrated in the following figures. Bins are 1 ms. A and B:
units whose responses are shown in Fig. 3. C and D: units shown in Fig. 5.
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FIG. 1. Restrained rat preparation. The rat is restrained in a plastic tube
with his head attached via the head post to a metal flange extending forward
from the plastic tube. Two electrodes separated by a millimeter can be
advanced separately using miniature screw advance microdrives.
A head stage (NB Labs) was used to connect a multichannel
connector to the two electrodes on the rat’s head and to a multichannel
neuronal spike data acquisition processor (Plexon, Dallas, TX). All
waveforms from both electrodes were collected and saved for offline
spike sorting. Units were rediscriminated offline using principal components and cluster cutting (Plexon). Stimulus evoked poststimulus
INHIBITION IN BARREL CORTEX
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time histograms and raster displays were constructed from the spike
trains of the discriminated units.
Air travelling from the solenoid to the air outlet required 25 ms, and
neuron response latency was calculated by subtracting 25 ms from the
time to first spike for each trial.
Stimulus
Air puffs controlled for force and duration were used for stimulating the whiskers. The air puff is a supramaximal stimulus with a
ramp-and-hold puff of air (⬃200 mm/s).
STIMULUS LATENCY. Time 0 for the stimulus onset was triggered by
a solenoid opening on the air line several feet from the animal’s face.
RESULTS
The data presented here focus on cells that decreased their
spontaneous discharge in a stimulus-linked fashion. In each
animal, anywhere from 6 to 10 recording sites were tested, and
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FIG. 3. Example of spontaneous discharge inhibition (electrode 2) following C2 whisker stimulation. The recording sites for the 2 electrodes
are shown in A and they show that electrode 1
was on the edge of the C2 barrel while electrode
2 was in the septum between barrels. The C2 and
C1 whiskers were judged to be the principal
whiskers for electrodes 1 and 2, respectively,
based on producing the strongest response to
manual whisker stimulation (B). Stimulation of
the C2 whisker inhibited the spontaneous discharge of the neuron recorded on electrode 2 (C)
as shown in rasters (top) and spike density functions (bottom). The A2 and B1 whiskers were
ineffective in driving either of these cells. The
C2, A2, and B1 whiskers were stimulated at 1 Hz.
Bin size 2 ms with smoothing over 10 bins in the
spike density functions. Note that the time from
the onset of air puff to the time it takes to reach
the whiskers is 25 ms, so 25 ms should be subtracted from the response onset times.
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at each site, multiple units were discriminated from two electrodes. A total of 48 units were discriminated of which 10
responded to whisker stimulation with I-only inhibition. Autocorrelation functions for four units discriminated from four
separate electrodes in two animals are shown in Fig. 2. The
striking feature of these recordings is that whisker stimulation
inhibits cell discharge, without any detectable excitatory discharge. In all recordings, histology showed that the electrode
was on a barrel edge or clearly in a septal zone (Figs. 3A, 4A,
and 5A). Except for a single recording site where stimulation of
a large mystacial whisker (C2) inhibited the spontaneous discharge, the rest of neurons in the sample responded to small
whiskers (nose hair, D6, and D7) that the animal typically does
not move much with suppression of spontaneous activity.
Stimulation of the C2 whisker at a frequency of 1 Hz
inhibited the discharge of neurons recorded from electrode 2
(Fig. 3C, right PSTH) while the neuron on electrode 1 (Fig. 3C,
left PSTH) was excited by C2 stimulation. Inhibition was
restricted to the C2 whisker, as other whiskers (A2 and B1 are
shown) did not evoke the same inhibition in the cortical cell.
In another animal, stimulation of the D6 whisker inhibited
neurons on one electrode, while at the same time weakly
exciting neurons on the other electrode (Fig. 4). Recording
sites for the two electrodes were the edge of E7 whisker barrel
and between C5, D6, and D7 barrels. One electrode had a
receptive field of “F-row” whiskers that have no barrels associated with them, while the principal whisker for electrode 2
was the D6 whisker. At two recording sites, stimulation of the
D6 whisker at 1 Hz inhibited spontaneous discharge of neurons.
Similarly, stimulation of the D7 whisker inhibited neurons at
only one of the recording sites in another animal (not shown).
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FIG. 4. D6 whisker stimulation inhibits spontaneous
discharge. Recording sites for two electrodes are shown in
A, reflecting the fact that electrode 1 was on the edge of
E7 whisker barrel and electrode 2 was between C5, D6,
and D7 barrels. Electrode 1 had a receptive field of F-row
whiskers that have no barrels associated with them, while
the principal whisker for electrode 2 was the D6 whisker.
At both recording sites on electrode 1, stimulation of the
D6 whisker at 1 Hz inhibited the spontaneous discharge
of neurons 1 mm lateral to the D6 barrel, on the edge of
E7 barrel. Bin size 2 ms. Smoothing over 10 bins.
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At the other recording sites in the same animal, the D7 whisker
evoked either no response or an excitatory discharge. Inhibition is not restricted to mystacial whisker stimulation. Nose
hair stimulation can also inhibit and excite neurons in the barrel
field (Fig. 5C).
Effect of stimulus frequency
The neurons just described respond differently at higher
stimulus frequencies. Figures 6, 7, and 8 show a more complicated pattern of modulation that develops at higher stimulus
frequencies. The same neuron shown in Fig. 3 (electrode 2)
shows a modulated pattern of discharge that is double the
stimulus frequency at 12 Hz (Fig. 6). Inhibition begins 15 ms
poststimulus and lasts 125 ms poststimulus. At higher stimulus
frequencies, one-half (5 of 10) of the neurons show a switch
from an apparent inhibitory trough to an excitatory discharge
following the stimulus (Fig. 7). In the other neurons, there is a
mixed excitatory/inhibitory response to the stimulus, where the
neuron is inhibited for a large sequence of trials, but apparently
cannot maintain this response to whisker stimulation (Fig. 6
and 8).
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FIG. 5. Nose hair stimulation inhibits
spontaneous discharge of neurons in the barrel
field cortex. The recording sites in A show that
electrode 1 was on the edge of nose hair barrels and electrode 2 was on the edge of the C4
barrel. When a nose hair, a tuft of 3 hairs near
the nostril, is stimulated the spontaneous discharge of the neuron on the edge of barrel C4
is inhibited as is evident in the rasters and the
spike density functions (C). When C4 is stimulated there is a weak excitatory discharge
followed by an inhibitory and excitatory discharge on the C4 electrode. All stimuli were
presented at 1 Hz. Bin size 2 ms with smoothing over 10 bins.
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Recording site
All recording sites were in SI barrel cortex, either on the
edge of a barrel or in the septum between barrels. In 4 of 5
animals in which whisker stimulation evoked an inhibitory
discharge, the most superficial recording sites were in layer II,
III, or IV. In the remaining animal, whisker stimulation evoked
an inhibitory discharge only in the deepest recording site in
layer V.
DISCUSSION
The principal finding in this study was that whisker stimulation in the awake rat can block spontaneous discharge without evoking prior excitation. This suppression of discharge
occurs at longer latencies than the fastest excitation produced
at low stimulus frequencies. The cells showing I-only inhibition were found only in or at the border of septa.
Very early in the history of recording from single units in cat
SI cortex, Mountcastle (1957) reported that stimulation with an
air puff in the center of the receptive field evoked excitation,
but stimuli directed outside of a neuron’s excitatory receptive
field inhibited spontaneous discharge in cortical cells. An in
vivo study carried out with intracellular methods in cat SI
cortex (Hellweg et al. 1977) showed that the most frequent
response to whisker stimulation was EPSPs followed by IPSPs.
In the center of the receptive field where inhibition was the
strongest, IPSPs occurred after excitation. Outside the center of
the receptive field, however, IPSPs could precede EPSPs. Even
further out in the receptive field, inhibition could occur as the
only response to whisker stimulation. In this study no such
gradation of inhibition has been detected. Specific whiskers
inhibited the spontaneous discharge of neurons when other
whiskers either evoked an excitatory discharge or had no
effect.
In the rat whisker cortex, surround whiskers typically evoke
an excitatory discharge with little evidence of an initial inhibition. In this study, we made no attempt to determine whether
the entire receptive field of a neuron was inhibitory, but clearly
the same neuron whose spontaneous discharge was inhibited
could respond with an excitatory discharge to a neighboring
whisker. A neuron whose response was suppressed by whisker
stimulation could even generate an excitatory discharge to the
same whisker when it was stimulated at a higher stimulus
frequency.
A number of previous studies of the rat vibrissal cortex have
described inhibition that follows excitation (Brumberg et al.
1996; Carvell and Simons 1988; Kyriazi and Simons 1993;
Kyriazi et al. 1996; Simons 1985; Simons and Carvell 1989),
and in addition, there is some evidence for I-only inhibition in
cortical neurons (Hellweg et al. 1977; Moore and Nelson
FIG. 7. Effect of stimulus frequency on the responses of cells at the edge of the E7 barrel. In 2 of 6 recording sites neurons were
inhibited during 1 Hz stimulation of D6 whisker. However, at stimulus frequencies of 12 Hz, neurons at both these recording sites
increased their discharge rate in phase with the stimulus.
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FIG. 6. Effect of different stimulus frequencies on responses of neurons at the edge of the C2 barrel edge and in the septum.
The peak excitatory discharge (electrode 1) occurs 15 ms post stimulus (onset at 8 ms), while the peak inhibition on electrode 2,
is at 25–100 ms (onset at 15 ms). Because the duration of the inhibition lasts longer than the excitation the two neurons fire out
of phase. As the stimulus frequency increases, the duration of the inhibitory trough decreases, while the duration of the excitatory
discharge is relatively stable. Stimulation (12 Hz) evokes a stimulus locked response (see panel with 12 Hz stimulus frequency)
where the neuron is inhibited in some trials and excited in others.
INHIBITION IN BARREL CORTEX
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1998). The excitation-inhibition is very characteristic of the
responses generated by VPM to barrel thalamocortical inputs
when activated by the principal whisker. In the septa between
layer IV barrels there is a dense input from the POm nucleus
rather than VPM (Koralek et al. 1988; Lu and Lin 1993), and
septal cells often respond equally strongly to more than one
whisker (Armstrong-James and Fox 1987). The I-only inhibition has not been analyzed in the same detail, but its relatively
long latency to onset is consistent with being generated by
intracortical circuits rather than thalamocortical activation. An
alternative explanation for both the postexcitatory inhibition
and inhibition alone might be that at least part of the suppression of cortical discharge could be due to disfacilitation (the
removal of drive onto the neuron) and not due to active
inhibition (Contreras et al. 1996; Cowan and Wilson 1994).
Arguments for this view are as follows: 1) input resistance of
cortical neurons is higher during long-lasting hyperpolarizations evoked spontaneously or by thalamic stimulation and 2)
GABAergic inhibitory mechanisms in cortex are relatively
short compared with this inhibition. According to this view,
active inhibition has a role in suppressing neuronal discharge,
but this effect is short in duration, as short as the effect of
excitation in increasing neuronal discharge. More important to
this view, is the removal of all synaptic input, which increases
the neurons input resistance and suppresses the neurons discharge. This study is an extracellular study and cannot distinguish between these possibilities.
Other studies
In this study the majority of neurons responded with excitation followed by inhibition and had similar characteristics to
those reported previously by Simons, Carvell and colleagues
(Brumberg et al. 1996; Simons 1985). Evidence of inhibition
detected extracellularly can be seen 20 ms poststimulus and
can last 100 –150 ms (also see Kleinfeld and Delaney 1996).
Inhibitory interactions in the rat vibrissal S1 cortex have been
studied with a dual whisker stimulation paradigm to look at the
effect of stimulating an adjacent whisker before, after, or
during principal whisker stimulation. These studies have
shown that as the number of stimulated adjacent whiskers
increases, inhibition of principal whisker evoked responses
increases (Brumberg et al. 1996). Adjacent whisker deflection
within 10 –20 ms suppresses the response of a neuron to
principal whisker deflection (Simons 1985). One implication of
these results is that whisker stimulation could have an inhibitory effect on neurons in barrel cortex. This study confirms that
some septal neurons are directly inhibited by whisker stimulation. This study also suggests that the inhibitory effect of low
frequency whisker stimulation can be seen even without dual
whisker stimulation or the application of GABA agonists and
antagonists.
Methodological issues
During whisker stimulation the rat can move its whiskers. It
is possible that the whisker stimulus dependent inhibition described here is related to movement of the whiskers. However,
this possibility can be ruled out at least for some of recording
sites, like the nose hair, because the rat cannot move his nose
hair voluntarily. Waxing and waning of attention as a cause of
whisker stimulus related suppression is harder to rule out.
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FIG. 8. Effect of stimulus frequency on C4 barrel edge when stimulating Nose Hair. At low stimulus frequencies (1– 6 Hz)
neurons that are inhibited fire out of phase with the neurons that are excited by nose hair stimulation, but at higher frequencies
(9 –12 Hz) of stimulation, these neurons fire together.
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R.N.S. SACHDEV, H. SELLIEN, AND F. F. EBNER
Implication
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