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The Journal of Neuroscience, November 15, 1998, 18(22):9517-9528
Synaptic Integration in Striate Cortical Simple Cells
Judith A.
Hirsch1,
José-Manuel
Alonso1,
R. Clay
Reid2, and
Luis M.
Martinez1
1 Laboratory of Neurobiology, The Rockefeller
University, New York, New York, and 2 Department of
Neurobiology, Harvard Medical School, Boston, Massachusetts
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ABSTRACT |
Simple cells in the visual cortex respond to the precise position
of oriented contours (Hubel and Wiesel, 1962 ). This sensitivity reflects the structure of the simple receptive field, which exhibits two sorts of antagonism between on and
off inputs. First, simple receptive fields are divided
into adjacent on and off subregions; second, within each subregion, stimuli of the reverse contrast evoke
responses of the opposite sign: push-pull (Hubel and Wiesel, 1962;
Palmer and Davis, 1981; Jones and Palmer, 1987; Ferster, 1988). We have
made whole-cell patch recordings from cat area 17 during visual
stimulation to examine the generation and integration of excitation
(push) and suppression (pull) in the simple receptive field. The
temporal structure of the push reflected the pattern of thalamic
inputs, as judged by comparing the intracellular cortical responses to
extracellular recordings made in the lateral geniculate nucleus. Two
mechanisms have been advanced to account for the pull-withdrawal of
thalamic drive and active, intracortical inhibition (Hubel and Wiesel,
1962; Heggelund, 1986; Ferster, 1988). Our results suggest that
intracortical inhibition is the dominant, and perhaps sole, mechanism
of suppression. The inhibitory influences operated within a wide
dynamic range. When inhibition was strong, the membrane conductance
could be doubled or tripled. Furthermore, if a stimulus confined to one
subregion was enlarged so that it extended into the next, the sign of
response often changed from depolarizing to hyperpolarizing. In other
instances, the inhibition modulated neuronal output subtly, by
elevating spike threshold or altering firing rate at a given membrane voltage.
Key words:
visual cortex; patch recording in vivo; simple
cell; IPSP; EPSP; spiny stellate cell
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INTRODUCTION |
Cortical sensitivity to patterned
stimuli has its roots in the arrangement of synaptic inputs to simple
cells, whose receptive fields are made of elongated, alternating
on and off subregions. Bright signals confined to
an on subregion are excitatory, whereas dark ones reduce
activity; that is, stimuli of the opposite contrast have a push-pull
effect (Hubel and Wiesel, 1962; Movshon et al., 1978; Heggelund, 1981,
1986; Palmer and Davis, 1981; Jones and Palmer, 1987; Ferster, 1988;
Miller, 1994; Troyer et al., 1998; but see Debanne et al., 1998).
Furthermore, when the receptive field is uniformly illuminated or
darkened, simple cells respond poorly because their subregions have a
mutually antagonistic relationship (Hubel and Wiesel, 1962). Thus, the
output of the simple cell relies on the balance of excitation and
suppression that various stimuli evoke.
We have used the technique of whole-cell recording (Hamill et al.,
1981; Edwards et al., 1989; Blanton et al., 1989) in vivo (Pei et al., 1991; Ferster and Jagadeesh, 1992) to analyze the synaptic
mechanisms that produce visually evoked responses in the receptive
field. First, we examined the origins of excitatory and suppressive
components of the responses to stimuli of reverse contrast flashed
within a single subregion. Then we asked how excitatory and suppressive
mechanisms interact when engaged together, as happens when a stimulus
tilts away from the axis of the field to span neighboring subregions.
Although suppression might result either from the removal of excitation
or from active inhibition, the findings of these studies stress that
active inhibition in the cortical receptive field is strong and
modulates excitatory input both by means of hyperpolarization and
increasing the membrane conductance (Hirsch et al., 1995).
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MATERIALS AND METHODS |
Anesthesia. Adult cats, 2.5-3.5 kg, were
anesthetized with ketamine (10 mg/kg, i.m.) followed by thiopental
sodium (20 mg/kg, i.v.), supplemented as needed. Lidocaine was applied
topically at all incisions or points of pressure. Temperature
(37-38°C), EKG, EEG, and expired CO2 (27-33 mmHg) were
monitored throughout the experiment. Anesthesia was maintained by a
continuous infusion of thiopental sodium (2-4
mg · kg 1 · hr1, i.v.)
adjusted as indicated by the EEG and EKG. After the completion of
surgery, animals were paralyzed [vecuronium bromide (Norcuron) 0.2 mg · kg1 · hr1,
i.v.] and artificially respired.
Surgery. An endotracheal tube was introduced through a
tracheotomy before the animal was placed in a stereotaxic apparatus. Two cortical craniotomies were made; one centered on Horsley-Clark coordinates A6.5-L8.5 gave access to the lateral geniculate nucleus, and the other, centered on Horsley-Clark P3-L2, was enlarged to expose
the longitudinal gyrus. Pupils were dilated with 1% atropine sulfate,
and the nictitating membranes were retracted with 10% phenylephrine.
Eyes were refracted and fitted with contact lenses to focus on a
tangent screen. The position of the area centralis and the optic disk
of each eye was determined with a fundus camera.
Acquisition of visually evoked responses. Intracellular and
extracellular records were collected by a computer running the Discovery software package (Datawave Systems, Longmont, CO),
intracellular records were normally sampled at 3-4 kHz. Each recording
session was also stored on videotape at 11-22 kHz. An AT-vista board
(Truevision, Indianapolis, IN), controlled by the same computer that
received the data generated visual stimuli that were presented on a
computer monitor (frame rate 100, 105, 128, or 140 Hz). Each cycle of
the stimulus protocol consisted of light or dark squares at various contrasts (range, 30-70%) flashed singly for 29-39 msec in
pseudorandom order, 16 times on a 16 × 16 grid (sparse noise; see
Jones and Palmer, 1987). Grid spacing ranged from 0.4 to 0.85° and
square size from 0.4 to 1.7°. Although there was no delay between
sequential stimuli (as one was switched off another was flashed on),
effective squares were usually separated by substantial intervals
because the receptive fields were typically much smaller than the
stimulus grid. Maps of the receptive fields were made by subtracting
responses to dark stimuli from responses to bright stimuli and are
plotted as shaded contours; each successive concentric line indicates a
10% reduction in the strength of response relative to the peak (spikes
inclusive). Receptive fields with separate and adjacent on
and off subregions were classified as simple (Hubel and
Wiesel, 1962; for review, see Skottun et al., 1991). The terms
on and off are equivalent to the terms
bright-excitatory and dark-excitatory used by others (DeAngelis et al.,
1992).
Recording. Patch-pipette resistance was  12 M when
filled with internal solution, in mM; K gluconate 120; NaCl
5; CaCl2 1; MgCl2 1; EGTA 11; GTP 0.2; ATP 2;
HEPES 40; and biocytin 1%, pH 7.3, 290 mOsm (Malinow and Tsein, 1990).
For three cells, 10 mM QX-314 Br (courtesy of Astra) was
included in the pipette. Initial seal resistances were 0.5-1.0 G.
Recordings were made with an Axopatch 200a amplifier and stored as
described above; neither capacitance nor access resistance was
compensated, so fast events were filtered. The bridge was balanced
off-line. The voltage-current relationship was measured before and
after each cycle of the stimulus protocol to monitor changes in the
access and apparent input resistance, threshold for firing, and
membrane time constant. The DC voltage changes produced by constant
current injection during a given cycle of the protocol were taken from
the responses to equivalent current pulses delivered before or after
the cycle. This procedure served to separate drift in the recording
circuit from real changes in the membrane potential that may have
occurred over time. Because the access resistance often increased after
rupture of the membrane (Edwards and Konnerth, 1992), the voltage in
the records was sometimes divided (Stühmer et al., 1983). For
this reason, as well as drift that can occur over the long time courses
of the recording, we do not provide absolute resting potentials.
Extracellular recordings in the lateral geniculate were amplified,
filtered, and collected in parallel with the intracellular recordings.
Histology. After histological processing (Horikawa and
Armstrong, 1988; Hirsch, 1995) labeled neurons were drawn using a
camera lucida, or a computerized three-dimensional reconstruction
system, (Microbrightfield, Cochester, VT). Reconstruction of the
electrode tracks revealed that, with the exception of two dendritic
recordings, our recordings came from the soma.
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RESULTS |
We have recorded from 21 simple cells in the adult cat striate
cortex. Intracellular labeling allowed us to identify many of the cells
from which we recorded; our sample included four layer 6 pyramids, four
pyramids at the borders of layer 4, and nine spiny stellate cells in
layer 4. Recordings lasted from 20 min to 2.75 hr, normally 30 min to 1 hr. The average time constant of the cells was 21 ± 4.2 msec
(range, 15-24 msec). In addition, we have recorded extracellularly
from fifteen cells in the lateral geniculate nucleus and measured their
responses to the same set of visual stimuli used to study cortex.
Synaptic construction of the receptive field
Flash-evoked responses in the simple receptive field
Simple cells responded to the sparse-noise stimulus in a
stereotyped way. Figure 1 shows the
synaptic responses to light and to dark stimuli that fell over the peak
of the off or the on subregion. The inset over
each panel shows the stimulus position in the receptive field (the
off subregion is depicted as concentric bands that grow
darker toward the peak; likewise, the on subregion is mapped by contours whose shade lightens as the strength of response
increases). Each set of traces shows two individual responses to the
stimulus and, beneath these, the averaged responses of all sixteen
trials. A dark square presented to the middle of the off
subregion evoked an initial depolarization capped by a train of action
potentials. The subsequent hyperpolarization and weak depolarization
corresponded to the withdrawal of the dark square (cf. Ohzawa et al.,
1996). Accordingly, a light square flashed at the same site evoked a hyperpolarization followed by a depolarizing wave. The responses evoked
from the on subregion qualitatively mirrored those elicited from the off subregion. Superimposed on this basic
structure, each simple cell had its own distinct behavior. For example,
for the neuron illustrated here, responses to dark stimuli were
stronger than responses to bright ones. Small variations aside, the
push-pull response to squares flashed within a given subregion was
common to all cells, provided the resting potential was near the
threshold for firing.
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Figure 1.
Push and pull in the simple cell response.
Postsynaptic responses evoked by dark or bright stimuli that fell
inside the off or the on subregion of a
simple cell in upper layer 6. Each panel shows two individual responses
to the stimulus with the average of all 16 as the bold
trace beneath. The position and sign of the stimulus is indicated in
the receptive field map (the peak of the on subregion is
light and that of the off subregions is dark; grid
spacing is 0.4°) above each panel. Stimulus duration
is marked by the bold bar under each trace in this and
subsequent figures. A, A dark square flashed in the
off subregion elicited an initial depolarization and
late hyperpolarization, top, whereas a bright square at
the same site evoked a hyperpolarization and subsequent depolarization,
bottom. B, Responses from the
on subregion mirror those from the
off.
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Comparison of the duration of thalamic and cortical responses
Simple cells receive the bulk of the input from the lateral
geniculate nucleus (Lorente de Nó, 1944; Hubel and Wiesel, 1962; LeVay and Gilbert, 1976; Humphrey et al., 1985; Peters and Payne, 1993). To understand better how the primary afferents influence simple
cells, we recorded extracellularly from the lateral geniculate during
presentation of the sparse noise stimulus. Then we compared the
histograms of thalamic activity with the intracellular cortical responses (Table 1). The cortical
depolarization evoked by a stimulus of the appropriate sign (onset
excitation) peaked while the relay cells were firing (onset activity).
Likewise, withdrawal of a stimulus of the opposite sign produced an
excitatory response in cortex (offset excitation) that followed the
course of thalamic activity (offset activity). The complementary
hyperpolarizing phases of the response also tracked thalamic firing,
but had longer delays (2-10 msec) than the excitatory components,
consistent with a synaptic relay through inhibitory interneurons (see
next section of Results). In general, the cortical responses differed from the envelopes of thalamic activity in having somewhat longer durations. The prolongation of cortical responses may have been produced variously by the passive and active properties of the membrane
(Rall, 1977; Hirsch, 1995), input from lagged relay cells (not included
in our sample) (Mastronarde, 1987; Humphrey and Weller, 1988; Cai et
al., 1997), and intracortical synaptic inputs (McGuire et al., 1984;
Saint-Marie and Peters, 1985; Douglas et al., 1991; Peters and Payne,
1993; Ahmed et al., 1994; Hirsch, 1995; Cai et al., 1997).
Mechanisms of inhibition in the simple receptive field
Two distinct mechanisms, one passive and one active, are thought
to contribute to the stimulus-evoked suppression. The idea of a passive
contribution stemmed from the observation that cells in the lateral
geniculate nucleus have high rates of spontaneous activity (Hubel and
Wiesel, 1961) and are excitatory (LeVay and Gilbert, 1976; Hoffman and
Stone, 1971; Ferster and Lindström, 1983; Hagihara et al., 1988).
Thus, they could contribute a tonic depolarizing component to the
resting potential of the simple cell membrane (Hubel and Wiesel, 1962).
Presentation of a stimulus of the unmatched sign would lead to a dip in
the transmembrane voltage of a simple cell as a consequence of
silencing excitatory inputs from the thalamus. Active inhibition could
be accounted for by cortical interneurons driven by thalamic afferents
(Hubel and Wiesel, 1962; Sillito, 1975; Gilbert and Wiesel, 1979;
Heggelund, 1986; Palmer and Davis, 1981; Jones and Palmer, 1987;
Ferster, 1988).
We conducted experiments to examine the relative contributions of these
active and passive mechanisms. Postsynaptic inhibition would be
reflected by an increase in the membrane conductance, whereas the
passive mechanism, withdrawal of excitation, would reduce conductance.
Furthermore, the shape of a waveform produced by active process would
shrink and then reverse sign as the membrane voltage neared and then
moved below the reversal potential of the IPSP
(EIPSP). By contrast, hyperpolarization would
emphasize a withdrawal component because the membrane would be moved
farther way from the reversal potential for excitation
(EEPSP).
One series of experiments evaluated changes in the membrane resistance
during the visually evoked hyperpolarization. For the spiny stellate
cell drawn in Figure
2A, the membrane
conductance nearly doubled during the response to a stimulus of the
inappropriate contrast. A dark stimulus presented to the on
subregion produced a robust hyperpolarization; Figure
2B shows three individual trials of stimulus and the
averaged response in bold. Figure 2C, bottom compares the averaged response at the control voltage (bold
line) with the averaged response to the same stimulus
presented while the membrane was held at a relatively hyperpolarized
level (dotted trace). These two responses, obtained at
two different holding currents, allowed measurement of the change in
conductance during the response, g(t) (Fig.
2C, top). The conductance as a function of time
was calculated as,
where Ip is the amount of current
injected through the electrode during the control (relatively
depolarized) recording and In is the more
hyperpolarized constant current,
Vp(t) and
Vn(t) are the membrane voltages at
these two holding currents, and t is the time before,
during, and after stimulus presentation. The constant K
normalized the conductance so that g(0) = 100%. Figure 3 charts the change in membrane
conductance for three other cells. Typically, the change in conductance
evoked was between 200 and 300%. The top two traces come from
recordings made when QX-314 was present in the recording electrode.
Because QX-314 blocks the slow, potassium-mediated IPSP (Otis et al.,
1993), it is likely that that much of the conductance increase is
caused by the fast, chloride-mediated IPSP.
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Figure 2.
Visually evoked suppression is accompanied by an
increase in the membrane conductance. A, Reconstruction
of the cell, a spiny stellate cell in layer 4. B, A dark
square flashed within the on subregion evoked a brisk
hyperpolarization, as shown in three individual trials of the stimulus
and the average of sixteen trials (bold).
C, Top trace, Plot of conductance during
the visual response: g(t)=
K(Ip  In)/(Vp(t) Vn(t));
g(t) is the normalized conductance
at time t, Ip In is the difference between the values of
constant current injected through the electrode, and
Vp(t) and
Vn(t) are the membrane
voltages recorded while the membrane was held at the relatively
positive and negative levels. The averaged responses obtained at the
control and hyperpolarized levels that were used to calculate
g(t) are shown
below the graph. Grid spacing was 0.85°.
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Figure 3.
The time course of conductance increase
during visually evoked suppression in three simple cells.
A, B, Records from two layer 4 spiny
stellate cells recorded with QX-314 in the electrode (the receptive
field of cell B fell slightly outside of the stimulus
grid). C, Record from a pyramid at the upper border of
layer 4. Grid spacing: A, B, 0. 85°;
C, 0. 4°.
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We evaluated the relative importance of active and passive processes in
generating the visually evoked suppression by determining the voltage
dependence of the response to stimuli of the inappropriate contrast.
The morphology of a spiny stellate cell in which the visually evoked
suppression was reversed is illustrated in Figure 4, top. The soma was located
in the middle of layer 4; the axon projected to the lower half of layer
2+3 and to layer 6. Each panel in this figure shows somatic recordings
made when the membrane was held at different levels of polarization.
While the membrane was depolarized with current, the stimulus evoked
a prominent hyperpolarization (Fig. 4B). When a
moderate amount of hyperpolarizing current was injected, the initial
response was slight if visible at all (Fig. 4C).
Finally, the application of a stronger current changed the sign of the
response from hyperpolarizing to depolarizing (Fig.
4D). Of five cells tested, the IPSP was fully
reversed in two. In the remaining cells, for suppression evoked by the
flashed squares or by moving bars, the equilibrium potential was
reached but the recordings ended before the next opportunity to inject stronger currents. All told, these results indicate that intracortical inhibition was the dominant force in generating suppressive responses evoked by stimuli of the opposite contrast; slight contributions made
by the withdrawal of tonic excitation might have been present but
masked by active processes.
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Figure 4.
Reversal of the visually evoked suppression.
Reconstruction of the cell, a spiny stellate cell in layer 4 (A). Responses to a stimulus of the inappropriate
polarity recorded while the membrane was held at three different levels
of polarization. When the membrane was moderately depolarized, the
initial response was hyperpolarizing (B). When
membrane potential was stepped to more hyperpolarized levels, the
response amplitude diminished (C), and then
reversed (D). Recordings were actually collected
in the order C, B, D;
action potentials were suppressed with 10 mM QX-314. Grid
spacing was 0.85°.
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Interactions between and excitation and inhibition in
simple cells
To examine the interactions between excitation and inhibition we
used stimuli large enough to span the border between subregions, Figure
5. The receptive field of the cell, a
layer 6 pyramid (Fig. 5E), had a strong on
subregion and a weaker off subregion. A small stimulus
confined to the off subregion evoked a strong depolarization (Fig. 5A, left column). The response to a
larger stimulus that spread into a portion of the neighboring
on subregion was hyperpolarizing (Fig. 5A,
right column). These results indicated that the
excitation evoked from the off subregion was overwhelmed by
the inhibition elicited from the on subregion. Similar
interactions were observed in eight cells recorded when the membrane
potential was near the threshold for firing. A wiring diagram
illustrating a circuit that could mediate this interaction is shown in
Figure 5F. The large and small stimuli are sketched over the
fields of two adjacent off-center relay cells that provide
input to a pair of inhibitory and excitatory simple cells. The
receptive fields of the two simple cells overlap but have an inverse
arrangement of on and off subregions. The smaller
size of the on subregion of the inhibitory simple cell
indicates that this subregion is weaker than the off, a
feature that would account for that fact that the cell is well driven by the large, dark stimulus.
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Figure 5.
Antagonism between subregions in the simple
receptive field. A, Left, A small dark
square confined to the off subregion evoked a
depolarization. Right, A larger stimulus that spread
into the on subregion suppressed the excitation driven
through the off subregion. B, The
averaged response to the large square (as in A) shown
beside the averaged response to an identical stimulus flashed while the
membrane was slightly hyperpolarized. The inhibition that dominated the
right trace suppressed the excitation visible in the
left trace. C, Responses to large dark
(left) and bright (right) squares that
avoided the on subregion recorded while the membrane was
at the hyperpolarized level. Left, The excitatory
component of the response to the overlapping stimulus (i.e.,
B, right) matched the excitation evoked
by the dark stimulus that fell inside the off subregion.
Right, The response to the bright stimulus shows that
the membrane voltage had remained above the reversal potential for
inhibition. D, Receptive fields and poststimulus time
histograms from an extracellularly recorded, off center
LGN X cell monitored at the same time as the cortical simple cell. The
large spot (right) drove more spikes than the small one
did (left), although the large spot fell mainly outside
the center. (The subsample of the stimulus grid for the simple cell is
shifted down two pixels from that for the relay cell.)
E, The cell was a pyramid in layer 6. F,
Possible circuit: the receptive field of superimposed inhibitory simple
cell whose subregions are reversed compared with those of patched
neuron, the fields of antecedent thalamic cells and relative stimulus
placement. Grid spacing, 0.4°.
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An alternative possibility to explain the suppressive response is that
the larger square drove fewer thalamic spikes than the smaller one
because the bigger stimulus invaded the suppressive surrounds of the
relay cells. Hence, the response to the large spots might reflect this
reduced excitatory input to the cortex. The records in panels Figures
5B-D provide two lines of evidence that
reduction in thalamic drive does not account for our observations.
The average response to the large dark spot, recorded at the
control level of membrane polarization, was plotted beside the averaged response to the same stimulus presented while the membrane was
slightly hyperpolarized (Fig. 5B). At the hyperpolarized
potential, the membrane was nearer EIPSP and farther from
EEPSP, reducing inhibitory effects while enhancing
excitatory currents. At this hyperpolarized potential, a strong
excitatory component of the response was revealed. Thus, nearer the
threshold for firing, although the net response to the overlapping
stimulus was inhibitory, it did contain a strong excitatory component.
A remaining question was whether or not the depolarization evoked by
the large stimulus was really a reversed IPSP? Figure 5C
shows responses to large bright and dark squares that covered the
off subregion and spilled outside of the receptive field.
The response to bright stimuli flashed within the off
subfield evoked a well defined hyperpolarization; the recording had
remained above EIPSP.
As described earlier, we often place extracellular electrodes in the
lateral geniculate nucleus in addition to the patch pipette in cortex.
These recordings have provided additional evidence that the large spots
did not lead to suppression of geniculate input. Figure 5D
shows the receptive field of an off center thalamic cell
mapped with the small stimulus (left) and the large one
(right). The receptive field of the relay cell was located
at the upper border of the simple field. Plots of spike rate over time
beneath each map show that the large spots were slightly more, rather than less, effective in driving thalamic activity. This occurred even
though the large spot fell mainly outside of the center of the thalamic
receptive field. In fact, we have not yet seen an instance in which the
large spots evoke less activity than the small ones. Our sample
contains over 10 similar records and includes examples from both sizes
of stimulus grid we use [cells were presumed to be X cells based on
the relative size of the receptive field compared with nearby neurons
(Alonso et al., 1996; Reid and Alonso, 1996)]. Our results are
in keeping with earlier studies that found that a substantial amount of
the surround must be recruited to reduce the firing from the center
(Hubel and Wiesel, 1961; Cleland and Lee, 1985; Bullier and Norton,
1987). Presumably, the suppressive mechanisms that regulate the
response would shift from active inhibition to thalamic withdrawal when
larger stimuli that cover more of the surround are used.
The forms of subfield interaction we have described so far can be
explained simply by the hyperpolarizing effects of inhibition. Other
more subtle responses are consistent with a weak shunt, or veto,
mechanism. Figure 6A
shows responses evoked by square that fell within the boundaries of a
single subregion. On the right are responses to a stimulus that edged
from this subregion into an adjacent one. While the initial
depolarizations evoked by the cross-border stimulus were often larger
than the ones produced by the confined square, they often failed to
produce action potentials. The top trace shows a suprathreshold
response, but the threshold voltage was higher than for the two
impulses that followed in the late phase of the response. By contrast,
although the depolarizations evoked from the home subregion were
smaller, they drove spikes or trains of spikes. A similar situation
held for the recording shown in Figure 6, C and
D; that is, the threshold for firing in the response to the
overlapping stimulus was higher. This difference in threshold coincided
with a difference in firing rate. During the initial phase of the
response depicted in the left records, 9 spikes were produced by the
overlapping stimulus and 21 by the confined square, for the cell on the
left, the ratio was 17:25. The two plots inset beneath the traces were
constructed from responses to pulses of depolarizing current injected
through the electrode; they show that spike frequency increased with
current strength. Hence, the dissociation between the synaptically
induced voltage changes and firing rate is unlikely to reflect
intrinsic properties of the neural membrane.
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Figure 6.
Alternate forms of subfield antagonism.
A, B, Responses to stimuli confined to
the home subregion evoked a depolarization that was smaller
(A) but more effective in triggering spikes than
the larger depolarization evoked by a stimulus that just crossed the
border between subregions (B); same cell as in
Figure 1. C, D, A second example of the
slight dissociation between firing rate and threshold seen when
comparing responses evoked within the home subregion
(C) to those evoked by a stimulus that crossed
the border between subregions; same cell as in Figure 3. The
insets beneath the traces show that spike frequency
increased monotonically with injection of direct depolarizing current
pulses for each cell.
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DISCUSSION |
We have examined mechanisms of excitation and inhibition in the
simple cells of the cat primary visual cortex. The temporal structure
of the excitatory components of receptive field largely reflected
thalamic drive, as judged by comparing thalamic firing patterns to the
shape of the depolarizing components of the simple cell response.
Active intracortical inhibition, on the other hand, appeared to play
the dominant role in generating suppressive responses; suppression was
accompanied by a substantial change in the membrane conductance and
could be reversed when the membrane was hyperpolarized with current
injected through the electrode. Thus, it seems that suppression must be
mediated by inhibitory interneurons that contact cells whose subregions
have the opposite polarity (Hubel and Wiesel, 1962; Palmer and Davis,
1981, Jones and Palmer, 1987; Ferster, 1988) rather than by reduction
in the output of thalamocortical synapses. Furthermore, the dynamic
range of inhibitory effects is wide. Inhibition can act powerfully, by
summing with concomitant excitatory input to produce a net
hyperpolarization, or it can act subtly by influencing firing threshold
and rate.
Mechanisms of inhibition
Conductance changes
Our results show directly that inhibition in the simple receptive
field is strong (Sillito, 1975, 1992; Heggelund, 1986; Ferster, 1986,
1988; Bonds, 1989; DeAngelis et al., 1992; Volgushev et al., 1993;
Nelson et al., 1994; Pei et al., 1994; Crook et al., 1997). We have
found that the visually evoked suppression is accompanied by a twofold
to threefold increase in the membrane conductance. It should be
remembered, however, that our stimulus yielded modest responses
compared with those that would be produced by oriented bars or
gratings. Thus, conductance changes larger than those we have measured
should occur routinely. Mechanistic models of normalization processes
in cortex (Heeger, 1992; Carandini and Heeger, 1994; Carandini et al.,
1997) such as the contrast gain control (Sclar and Freeman, 1982;
Ohzawa et al., 1982) call for large, visually evoked changes in the
membrane conductance, which, our results suggest exist.
The presence of a conductance increase was not unexpected (Bernander et
al., 1991) and has been found in other systems. Blockade of spontaneous
inputs to cortical pyramids increases the membrane resistance by
30-70% (Pare et al., 1998). In Purkinje cells, a train of spikes from
just one presynaptic interneuron can reduce input resistance by a third
(Häusser and Clark, 1997). Some earlier studies of the striate
cortex did not detect changes in conductance during visual stimulation
(Douglas et al., 1988; Berman et al., 1991; Ferster and Jagadeesh,
1992), although Ferster (1988) demonstrated an active cortical
component of inhibitory interactions. These differences in measurement
may have come about because some earlier tests were made from cells
impaled with sharp electrodes, which themselves introduce a large
resting leakage conductance (Staley et al., 1992) or from difficulties
associated with the high access resistances involved in patch recording
from tissue (Stühmer et al., 1983; Edwards and Konnerth,
1992).
Independence of excitation and inhibition
The visually evoked suppression could be reversed by current
injection, suggesting that it is mediated by intracortical inhibition. A small part of an earlier study led to the conclusion that withdrawal of thalamic drive contributed strongly to visual responses
(Ferster, 1988). In that study, thalamic afferents were electrically
activated to produce a monosynaptic EPSP and disynaptic IPSP; at the
resting potential, the shock-evoked response lacked a hyperpolarizing component so the resting potential was equated with EIPSP.
Visually driven hyperpolarizations from rest were taken to reflect
thalamic withdrawal because active inhibition was thought to be silent. There are two concerns with this interpretation. First, it seems that
the resting potential was actually above EIPSP;
cells fired spontaneously at that level, whereas
EIPSP, by definition, falls below spike threshold.
Second, recent work has shown that activating the primary afferents
will disynaptically inhibit the geniculate (Lo and Sherman, 1994; Bal
et al., 1995) via feedback from the perigeniculate (Friedlander et al.,
1981; Dubin and Cleland, 1977) as well as the cortex. Thus, the absence
of cortical hyperpolarization after shocks to the primary afferents,
during the time when the geniculate would be silenced by the
perigeniculate, suggests that withdrawal of thalamic input does not
markedly influence the cortical membrane potential.
The results presented here indicate that inhibition in simple cells is
postsynaptic and, therefore, mediated by synapses distinct from those
that provide excitation. The excitation is laid out by thalamocortical
inputs (Hubel and Wiesel, 1962; Tanaka, 1983, 1985; Alonso et al.,
1996; Reid and Alonso, 1996; Ferster et al., 1996; Cai et al.,
1997; Chung and Ferster, 1997; Table 1, this manuscript) and likely
amplified by intracortical inputs (Saint-Marie and Peters, 1985;
Douglas et al., 1991; Ahmed et al., 1994; Hirsch, 1995; Cai et
al., 1997; Chung and Ferster, 1997). Inhibition is largely, or perhaps
wholly, provided by inhibitory neurons apparently driven by stimuli of
the reverse contrast. This separation of excitation and inhibition may
give the cortex a wider dynamic range in which to negotiate its inputs
(Troyer et al., 1998).
Interactions between excitation and inhibition
To understand the synaptic interactions that work to reduce
responsiveness to suboptimal stimuli, we examined the patterns of
excitation and inhibition evoked by stimuli that crossed the border
between subregions. Our results indicate that inhibition regulates
excitatory input in two ways, by means of hyperpolarizing the membrane
or by effectively changing firing threshold or rate.
Net hyperpolarization
In many instances the inhibition driven through one subregion
opposed the excitation driven through the other so strongly that the
net response was hyperpolarizing. This observation bears on previous
work that advanced the idea of cross-orientation inhibition. Several
studies have reported that a cross-oriented bar presented in the simple
receptive field led to inhibition (Bishop et al., 1973; Morrone et al.,
1982; Pei et al., 1994). Our results indicate that subfield antagonism
alone may account for the suppressive action of an orthogonal bar. It
also follows that the structure of the receptive fields of the
presynaptic inhibitory neurons need not be the precise mirror images of
their postsynaptic targets (Fig. 5F, see circuit). That is,
the interneurons can be driven to fire by the same stimuli that
effectively suppress the cells they contact.
Modulation of firing behavior
A second, more subtle, action was revealed when the inhibition was
too weak to hyperpolarize the membrane outright. Instead, the mild
inhibition seemed to elevate slightly the level of somatic depolarization required to produce an action potential or to slow the
rate of firing. In the cat auditory brainstem, intracellular responses
to tonal stimuli also reveal a dissociation between somatic membrane
voltage and spike threshold and rate (Rhode et al., 1983).
Additionally, records from the turtle visual cortex show that temporal
distribution of component IPSPs regulate the efficacy of depolarizing
compound synaptic responses (Colombe and Ulinski, 1996; Mancilla and
Ulinski, 1996). It is possible that the inhibition shunts
somatic excitation before it spreads to the site where the full-blown
spike is produced, presumably in the proximal axon (Colbert and
Johnston, 1996). This scheme is plausible because excitatory synapses
are normally distributed on the dendrites, whereas inhibitory synapses
are dense around the soma and axon hillock (LeVay, 1973; Fairén
et al., 1983; McGuire et al., 1984; Ahmed et al., 1994). Alternatively,
the inhibition could elevate the threshold directly by increasing conductance at the zone of spike initiation (Colbert and Johnston, 1996). Although these effects are small at the level of a single cell,
they may gain weight when propagated through the circuit. Different
rates of firing influence the success of transmission across the
synapse (Thomson and West, 1993; Allen and Stevens, 1994; Dobrunz and
Stevens, 1997; Tsodyks and Markram, 1997) as well as the integration of
inputs by the postsynaptic neuron (Bernander et al., 1991; Shadlen and
Newsome, 1994; Colombe and Ulinski, 1996; Mancilla and Ulinski, 1996;
Häusser and Clark, 1997; Mancilla et al., 1998).
To conclude, the spatial segregation of on and
off responses in the simple receptive field has given the
opportunity to study excitatory and inhibitory inputs separately and to
examine the mechanisms of their interaction when recruited in various
balance. Our aim is to apply what we have learned from simple cells to studies of synaptic integration at higher cortical levels.
| |
FOOTNOTES |
Received May 28, 1998; revised Aug. 27, 1998; accepted Aug. 28, 1998.
This work was supported by National Institutes of Health Grants EY09593
(J.A.H.) and EY05253 (T.N.W.), the Klingenstein Fund (J.A.H., R.C.R.),
and the Human Frontiers Science Program Organization (L.M.M.). We are
grateful to Torsten N. Wiesel for support and guidance during all
phases of the project. Christine A. Gallagher, Kathleen McGowan,
Johanna L. Kornblum, and Komal A. Desai provided superb technical
support and drew the labeled cells, which Peter Peirce photographed
precisely. We thank Sanford M. Simon for improving the manuscript,
Matteo Carandini for advice in analyzing conductance changes, and S. Murray Sherman for helpful criticism of an earlier draft.
Correspondence should be addressed to: Judith A. Hirsch, Box 138, Laboratory of Neurobiology, The Rockefeller University, 1230 York
Avenue, New York, NY 10021.
| |
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Top
Abstract
Introduction
