Two-Dimensional Coincidence Detection in the

Vibrissa/Barrel Field
Krista M. Rodgers, Alexander M. Benison and Daniel S. Barth
J Neurophysiol 96:1981-1990, 2006. First published Jun 21, 2006; doi:10.1152/jn.00404.2006

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Hemispheric Mapping of Secondary Somatosensory Cortex in the Rat
A. M. Benison, D. M. Rector and D. S. Barth
J Neurophysiol, January 1, 2007; 97 (1): 200-207.
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Two-Dimensional Coincidence Detection in the Vibrissa/Barrel Field
Krista M. Rodgers, Alexander M. Benison, and Daniel S. Barth
Department of Psychology, University of Colorado, Boulder, Colorado
Submitted 17 April 2006; accepted in final form 16 June 2006
Rodgers, Krista M., Alexander M. Benison, and Daniel S. Barth.
Two-dimensional coincidence detection in the vibrissa/barrel field. J
Neurophysiol 96: 1981–1990, 2006. First published June 21, 2006;
doi:10.1152/jn.00404.2006. Coincidence detection in visual and au-
ditory cortex may also be critical for feature analysis in somatosen-
sory cortex. We examined its role in the rat posteromedial barrel
subfield (PMBSF) using high-resolution arrays of epipial electrodes.
Five vibrissae, forming an arc, row, or diagonal, were simultaneously
or asynchronously stimulated to simulate contact with a straight edge
of different angles at natural whisking velocities. Results indicated
supralinear responses for both slow-wave and fast oscillations (FOs,
about 350 Hz) at intervibrissa delays ⬍2 ms. FO represented the
earliest and most precisely tuned response to coincident vibrissa
displacement. There was little difference in the spatiotemporal pattern
of slow-wave or FO responses in the row, arc, or diagonal. This
equivalence of function suggests that the PMBSF may be capable of
working as a two-dimensional integrative array, processing spatial
features based on coincidence detection despite the direction that the
vibrissae pass across an object.
INTRODUCTION
Spatiotemporally structured stimuli, such as a figure moving
across the retina or a low-frequency sound arriving at the left
and right cochlea at slightly different times, provide essential
information about object presence, location, and in the case of
vision, information about form, based solely on the timing with
which subsections of the receptive surface are coincidentally
excited (Carr 1993; Lee and Blake 1999; Usher and Donnelly
1998). In the visual system, temporal synchronization of neu-
ronal responses between regions of retinotopically organized
sensory cortex has been postulated as a fundamental mecha-
nism by which salient stimulus features may be dynamically
bound together (Engel et al. 1992; Singer 1993; Singer and
Gray 1995) and has been demonstrated to occur with millisec-
ond accuracy in the CNS (Konig et al. 1996; Singer et al.
1996). Temporal coincidence detection on a much finer time
scale of microseconds occurs in the auditory cortex and is
essential for coding intraaural time differences required for
sound localization (Carr 1993).
Coincidence detection may also be critical for feature anal-
ysis in the somatosensory system (Roy and Alloway 2001).
Perhaps the most attractive candidate for exploring this possi-
bility is the rodent vibrissa system. The somatosensory system
of rodents is dominated by afferent input from the vibrissae,
which serve as a primary means of close range environmental
exploration. Approximately half of the primary somatosensory
cortex consists of an orderly array of cellular columns, or
“barrels” (usually referred to as the posteromedial barrel sub-
field or PMBSF), in register with the macrovibrissae on the
Address for reprint requests and other correspondence: D. S. Barth, Depart-
ment of Psychology, University of Colorado, Campus Box 345, Boulder, CO
80309-0345 (E-mail: dbarth@psych.colorado.edu).
www.jn.org 0022-3077/06 $8.00 Copyright © 2006 The American Physiological Society
J Neurophysiol 96: 1981–1990, 2006.
First published June 21, 2006; doi:10.1152/jn.00404.2006.
contralateral face. As rats examine an object in the environ-
ment, they repeatedly whisk the vibrissae forward as a unified
array, establishing rapid spatiotemporal patterns of contact
(Sachdev et al. 2001) that presumably result in similarly rapid
spatiotemporal patterns of neuronal activity within and be-
tween the barrels of the PMBSF. Although the rodent vibrissa
system is thought to perform a number of complementary
tasks, including texture discrimination (Andermann et al. 2004;
Arabzadeh et al. 2004, 2005; Carvell and Simons 1990; Guil-
mage-Robles et al. 1989; Neimark et al. 2003) and spatial
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sampling such as gap detection, distance discrimination, and
head-centered orientation (Harris et al. 1999; Hutson and
Masterson 1986; Krupa et al. 2001; Sachdev et al. 2000;
Schiffman et al. 1970; Shuler et al. 2002; Vincent 1912),
behavioral and physiological studies suggest that the mac-
rovibrissae may also provide information about object features
such as edge orientation and shape (Benison et al. 2006;
Carvell and Simons 1990; Harvey et al. 2001; Simons 1995).
Features extracted by whisking might be uniquely identified
by coincident contact of multiple whiskers with an object as it
sweeps across the two-dimensional vibrissa array. Such coin-
cidence detection in the PMBSF would require a highly accu-
rate temporal relationship between vibrissa displacement and
cortical response, which has been clearly indicated by single-
unit studies of single and multiple vibrissa stimulation (Ego-
Stengel et al. 2005; Sachdev et al. 2001; Shimegi et al. 1999,
2000; Simons 1985; Simons and Carvell 1989). In addition, we
recently demonstrated temporal fidelity in field potentials re-
corded with epipial electrode arrays placed on the surface of
the PMBSF (Barth 2003; Benison et al. 2006). The precise
timing of field potentials across the PMBSF permits classifi-
cation and reconstruction of object orientation and shape based
solely on submillisecond timing patterns in the barrels (Beni-
son et al. 2006). Of particular interest are very fast oscillations
(FOs, about 350 Hz) that accompany the classic field potential
slow wave in somatosensory cortex (Barth 2003; Jones and
Barth 1999a; Jones et al. 2000; Kandel and Buzsaki 1997;
Staba et al. 2003, 2004, 2005) because these have been shown
to exhibit phase-sensitive interactions between barrels with
submillisecond precision and exert a strong influence on the
probability of cell firing (Barth 2003).
However, there were several limitations of our previous
study of multivibrissa interactions (Benison et al. 2006) based
mainly on the stimulus paradigm used. First, only five vibrissae
aligned dorsoventrally (“arc”) were stimulated, providing no
insight into how spatiotemporal information may be integrated
between arcs. Second, the stimulus consisted of a straight edge
rotating on a smooth drum. The vibrissae could not be placed
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1981
1982 K. M. RODGERS, A. M. BENISON, AND D. S. BARTH
individually on the drum to record their separate responses and
then replaced in the same location as a group to examine
multivibrissa responses. Thus we could not estimate supralin-
ear and sublinear responses in this study because we could not
obtain an accurate linear model for comparison (i.e., a model
constructed from the linear combination of single vibrissa
responses). Finally, slight misalignment of the vibrissae on the
x-axis (axis of rotation) resulted in asynchronous contact even
for upright edges (which should simultaneously strike an arc of
vibrissae). This misalignment may have had the effect of
obscuring the potential impact of simultaneous stimuli (coin-
cidence detection) while at the same time potentially masking
distinct phase-sensitive interactions of FO.
The purpose of the present study was to examine the possi-
ble role of coincidence detection in identifying stimulus fea-
tures in the PMBSF. Stimuli consisted of precisely timed
displacement of groups of five vibrissae aligned in an arc,
rostrocaudally (“row”), or along a diagonal. The timing of
vibrissa stimulation was under independent computer control
and set to simulate the vibrissae moving at a physiologically
realistic speed and contacting a straight edge of various angular
orientations, producing either simultaneous or varying degrees
of asynchronous displacements. To identify preferred stimuli,
we recorded population field potentials from the entire PMBSF
with high-resolution arrays of epipially placed electrodes and
examined possible supra- and sublinear responses as a function
of simulated stimulus angle. FO and slow-wave responses were
analyzed separately to obtain information about their poten-
tially unique contribution to coincidence detection.
METHODS
Animals and surgery
All procedures were conducted within the guidelines established by
the University of Colorado Institutional Animal Care and Use Com-
mittee. Adult male Sprague–Dawley rats (n ⫽ 4, 250 – 400 g) were
anesthetized to surgical levels using an intraperitoneal injection of
urethane (1.25 g/kg body weight) and a mixture of xylazine (14
mg/kg) and acepromazine (2.3 mg/kg). Animals were placed on a
regulated heating pad to maintain normal body temperature (37°C).
Anesthesia levels were maintained throughout the experiment so that
the corneal and flexor withdrawal reflexes could barely be elicited. A
unilateral craniotomy was performed over the right hemisphere ex-
tending from bregma to lambda and from the midsagittal suture to the
lateral aspect of the temporal bone, exposing a wide region of the
parietotemporal cortex. The dura was reflected and the exposed cortex
regularly doused with Ringer solution containing (in mM): NaCl 135,
KCl 3, MgCl 2, and CaCl 2, pH 7.4 at 37°C. At the conclusion of the
experiment, animals were killed by anesthesia overdose without ever
regaining consciousness.
Stimulation
Vibrissae on the left mystacial pad were trimmed to 2 cm and
displaced about 300 ␮m (0.1 ms in duration, 1-s interstimulus inter-
val) by inserting them into the ends of 6-cm stainless steel hypodermic
tubes attached to laboratory-built solenoids (Barth 2003; Jones and
Barth 1999b). Prior calibration of vibrissa displacement produced by
these solenoids revealed no notable afteroscillations at the latency or
frequency of fast or slow evoked potential components reported here
(Barth 2003). Three groups of five vibrissae were studied (Fig. 2),
forming a single arc (A3–E3), diagonal (A1–E5), or row (C1–C5).
Within each group, the timing of sequential pulses delivered to the
J Neurophysiol • VOL 96 • OCTOBER 2006 •
five solenoids simulated a straight edge moving at 0.2 mm/ms, to
approximate natural whisking velocities observed in behaving animals
(Sachdev et al. 2001). Simulated angles for each group were refer-
enced to 0°, which represented a straight edge simultaneously striking
the five vibrissae in a direction perpendicular to their axis of orien-
tation (i.e., moving in the caudal, dorsocaudal, or dorsal direction for
the arc, diagonal, or row, respectively). The timing of sequential
vibrissa displacement was computed to simulate angles of ⫾45, 30,
20, 10, 5, 1, and 0° in one experimental condition and angles of ⫾6,
5, 4, 3, 2, 1, and 0° in a second condition, to obtain finer spatial and
temporal resolution. Because the velocity of the simulated straight
edge was 0.2 mm/ms, this resulted in delays between adjacent vibris-
sae of 25, 14.4, 9.1, 4.4, 2.18, and 0.44 ms in the first condition and
2.63. 2.18, 1.75, 1.31, 0.87, and 0.44 ms in the second condition. For
example, a ⫹45° straight edge moving caudally through the arc of
vibrissae was simulated by displacing vibrissa E3 first, followed at
25-ms intervals by D3, C3, B3, and A3. An opposite A3–E3 sequence
simulated ⫺45°. Lead vibrissae for positive angles in the diagonal and
row were E5 and C5, respectively.
Evoked potential recording
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Epipial maps of the vibrissa-evoked SEP (somatosensory-evoked
potential) complex were recorded using a flat multichannel electrode
array consisting of 64 silver wires arranged in a 8 ⫻ 8 grid (tip
diameter: 100 ␮m; interelectrode spacing: 500 ␮m) covering a 3.5 ⫻
3.5-mm area of the cortical surface in a single placement. Surface field
potentials were referenced to a silver ball electrode secured over the
contralateral frontal bone, amplified (⫻1,000), analog filtered (band-
pass cutoff ⫽ ⫺6 dB at 1 to 3,000 Hz, rolloff ⫽ 5 dB/octave), and
digitized at 10 kHz.
Data collection and analysis
At the outset of each experiment, SEPs evoked by individually
stimulating each of 25 macrovibrissae (arcs 1–5 and rows A–E) were
averaged (n ⫽ 100; duration ⫽ 500 ms). Bicubic spline interpolated
maps of the initial positive SEP deflection (Fig. 1C), representing the
most focal response before intracortical spread (Fig. 1B, inset), were
computed for all 25 single vibrissa responses and the array positioned
such that these maps were aligned across animals; x–y coordinates for
all 25 single vibrissa response maxima were logged and averaged
across animals. Average loci were used to construct a template of the
PMBSF for subsequent illustration (Fig. 1, D and E).
For each vibrissa group (arc, diagonal, or row) and condition (⫾45
or ⫾6° angle ranges), 100 trials (500 ms) were randomly sampled at
each of the 13 simulated angles and later sorted and averaged. Data
were analyzed separately for the slow-wave (1- to 100-Hz digital
band-pass) or fast oscillatory (FO; 250- to 1,000-Hz digital band-pass)
components. Digital filtering was performed forward and backward in
time to eliminate phase shifts using a second-order Butterworth
response to minimize the possibility of ringing that could contaminate
FO. Interpolated maps of root-mean-squared (RMS) power in the
slow-wave or FO frequency bands were plotted as a function of
simulated stimulus angle. A linear model of SEPs for each angle was
also computed by summing the appropriately time-shifted SEPs
(based on the sequential intervibrissa delays used for simulation)
obtained from the separate principal vibrissae for a given group (i.e.,
single vibrissae SEPs for A3–E3 during the arc condition). RMS
power at each electrode was compared with the linear model and
tested for significant supra- or sublinear responses using paired t-tests
with significance set to P ⱕ 0.05. RMS power within the slow-wave
and FO frequency bands was also averaged across the electrode array
and plotted as a function of stimulus angle. Because power consis-
tently declined with deviations from 0° (simultaneous) stimulation,
the angles at which power dropped to half-amplitude were determined
for each condition and frequency band and tested for significant
www.jn.org
 COINCIDENCE DETECTION IN THE BARREL FIELD
differences, again using paired t-tests with significance set to P ⱕ
0.05. Results are reported as means (⫾SE) unless otherwise noted.
RESULTS
The 25 macrovibrissae form a 5 ⫻ 5 array, with arcs
typically labeled 1–5 on the caudorostral axis and rows labeled
J Neurophysiol • VOL
1983
A–E on the dorsoventral axis (Fig. 1A). The somatotopic
representation of these vibrissae in the contralateral PMBSF
consists of a similar array of distinct cellular aggregates with a
similar caudorostral organization of the vibrissa arcs but an
inverted dorsoventral organization of the rows. The 8 ⫻ 8
epipial electrode array was consistently aligned to the PMBSF
across animals using SEPs evoked by stimulating each of the
25 vibrissae separately. For example, stimulation of the C3
vibrissa (Fig. 1A, blue dot) evoked a typical positive/negative/
positive slow wave of maximum amplitude at its corresponding
barrel (Fig. 1B, labeled P1/N1/P2 in the inset to reflect the
polarity and sequence of the temporal components). The ear-
liest visually identifiable positive deflection at the rising phase
of the P1 (Fig. 1B, inset) yielded the most focal interpolated
amplitude maps (Fig. 1C) preceding intracortical spread. These
maps were used to locate each barrel in the PMBSF based on
locus of maximum response. Loci of barrels within the
PMBSF, determined from single-vibrissa SEPs, were averaged
across animals (SE ⫽ 0.19 mm; n ⫽ 4) and used as a template
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for further illustration (Fig. 1, D and E).
Sequential stimulation of a vibrissa arc (A3–E3), starting
with vibrissa A3 and an intervibrissa delay of 25 ms (simulat-
ing a straight edge set at 45° from vertical and moving caudally
at 0.2 mm/ms with a 5-mm intervibrissa separation on the
rostrocaudal and dorsoventral axis), produced multiple slow
waves in the SEP (Fig. 1D, blue traces). The earliest response
recorded from an electrode near barrel A3 (Fig. 1Da, arrow)
was followed by several additional lower-amplitude slow
waves separated by the 25-ms intervibrissa stimulus interval.
The SEP slow waves recorded near vibrissa D3 were largest in
amplitude at the latency of D3 stimulation (Fig. 1Db, arrow)
FIG. 1. Somatosensory-evoked potential (SEP) slow waves evoked by
multivibrissa stimulation of the A3–E3 arc. A: 25 macrovibrissae form an
approximately square array on the mystacial pad consisting of 5 arcs labeled
1–5 on the caudorostral axis and 5 rows labeled A–E on the dorsoventral axis.
Stimulated vibrissa C3 is marked with a blue dot in this example. B: displace-
ment of C3 results in an SEP slow wave of largest amplitude in 4 electrodes
of the 8 ⫻ 8 electrode epipial recording array. Single vibrissa slow wave
always consisted of a positive/negative/positive series of amplitude peaks,
labeled P1/N1/P2 to indicate their polarity and sequence of occurrence (inset).
C: initial positive deflection (inset) was mapped across the array using bicubic
spline interpolation and the locus of maximum amplitude used to locate the
underlying principal barrel (C3 in this example). This procedure was repeated
for the remaining 24 vibrissa. x–y coordinates of the 25 barrels derived from
single vibrissa SEPs were averaged across animals to form a template of the
posteromedial barrel subfield (PMBSF) for subsequent illustration (D and E;
circles). D: in this example, a straight edge canted at ⫺45° from the dorso-
ventral axis of the arc and moving caudally at a velocity of 0.2 mm/ms was
simulated. An edge at this angle would strike the A3 vibrissa first and then
B3–E3 in sequence, with an intervibrissa delay of 25 ms (based on the
assumption of a 5-mm separation between vibrissae). Evoked response (blue
traces) and linear model (red traces) revealed multiple slow waves, reflecting
sequential deflection of the vibrissae. Earliest response was from an electrode
near the principal barrel for A3 (enlarged in a) with an initial slow wave (blue
trace, arrow) that closely matched the linear model (red trace, “⫽”). Subse-
quent slow waves were also recorded at this site, reflecting the 25-ms interval
between displacements of adjacent vibrissae in the arc. These were notably
attenuated and sublinear (“⫺”) compared with the model, as were later slow
waves such as those recorded from a electrode near vibrissa/barrel D3 (b). E:
stimuli simulating a 0° straight edge involved simultaneous stimulation of all
5 vibrissae, resulting in a simplification of SEP morphology to a triphasic
P1/N1/P2 form. Enlargements of traces near barrels B3 (a) and E3 (b) indicate
that the P1 was sublinear (
⫺”), whereas both the N1 and P2 were supralinear
(“⫹”). Supralinearity was common for simultaneous or near-simultaneous
vibrissa stimulation and was typically largest at electrode sites adjacent to the
principal barrels for a given group (i.e., c and d).
96 • OCTOBER 2006 • www.jn.org
1984 K. M. RODGERS, A. M. BENISON, AND D. S. BARTH
but were also present in lower amplitude during preceding and
subsequent vibrissa stimulation in the sequence. A notable
feature of the asynchronous SEP was marked attenuation of
sharp wave amplitude following response to the first (A3)
vibrissa deflection (Fig. 1D, a and b). To quantify this atten-
uation, a linear model (Fig. 1D, red traces) was computed for
comparison. The linear model consisted of the sum of appro-
priately time-shifted single-vibrissa SEPs (recorded separately
J Neurophysiol • VOL
for isolated deflections of vibrissae A3–E3). Only the initial
slow wave produced by A3 matched the linear model (Fig.
1Da, “⫽”). Subsequent slow waves throughout the array were
attenuated to roughly 50% of the linear model (Fig. 1D, a and
b, “⫺”). Simultaneous stimulation of vibrissae A3–E3, simu-
lating an upright straight edge at 0° to the orientation of the arc,
produced a simpler SEP morphology that was similar to the
P1/N1/P2 slow wave evoked by single-vibrissa stimulation but
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96 • OCTOBER 2006 • www.jn.org
 COINCIDENCE DETECTION IN THE BARREL FIELD 1985

spread across the principal vibrissa barrels (Fig. 1E, blue
traces). However, the evoked response still differed from the
linear model (Fig. 1E, red traces). The initial P1 was typically
sublinear (Fig. 1E, a and b, “⫺”), whereas the N1 and subse-
quent P2 were typically supralinear (Fig. 1E, a and b, “⫹”).
Supralinear responses were particularly evident at electrode
sites surrounding the principal vibrissae (Fig. 1E, c and d).
Maps of slow-wave power, averaged across animals at all
electrode sites during arc stimulation, indicated maximum
responses with simultaneous (0°) or near-simultaneous (⫾1°)
vibrissa deflections (Fig. 2A, top row). Significant supralinear
responses (Fig. 2A, top row, white dots; P ⱕ 0.05) occurred at
electrode sites immediately surrounding areas of maximum
response during simultaneous 0° stimulation and with 0.44-ms
interbarrel delays simulating ⫾1°. Several electrodes near
barrel E3 showed supralinear responses at interbarrel delays as
long as 4.4 ms (⫹10°), although, at this and longer interbarrel
delays extending to 25 ms (⫾45°), the predominant response
was attenuated and typically sublinear (Fig. 2A, top row: black
SEPs from an electrode site near barrel C3 during ⫾6° stim-
ulation of the arc in one animal. In this example, the P1 was
sublinear and the N1 was slightly supralinear at all angles.
However, close examination of the P1 during simultaneous
stimulation (0°) revealed small, high-frequency FOs superim-
posed on this component and on the falling limb of the N1 (Fig.
3C). In this example, FOs in the wideband trace consisted of
slight rises and dips just preceding and following the crest of
the P1 that were aligned with successive FO waves in the 250-
to 1,000-Hz filtered trace (Fig. 3C; Composite). FO bursts of
similar latency relative to the P1 were recorded in all animals,
with an average period of 2.9 ⫾ 0.3 ms (or 345 ⫾ 38 Hz).
Interbarrel delays in the range of ⫾2.63 ms produced by ⫾6°
stimulation in this example would be expected to bring FO out
and then almost back into phase because the half-period (180°
out of phase) was 1.45 ms. FOs did indeed demonstrate a
marked phase sensitivity (Fig. 3B), with the largest and supra-
linear responses at 0 and ⫹1° (0.44 ms), minimum responses at
⫾3– 4° (⫾1.31–1.75 ms), and partial recovery of amplitude at

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dots; P ⱕ 0.05). Stimulation of the A1–E5 diagonal (Fig. 2A,
middle row) and C1–C5 row (Fig. 2A, bottom row) yielded
similar results, with a window of about ⫾0.4-ms interbarrel
delay (⫾1°) where simultaneous and near-simultaneous stim-
ulation produced maximum and usually supralinear responses
at electrode sites on and flanking the principal barrels. Outside
this window (⫾5– 45° or ⫾2.18 –25 ms), responses were con-
siderably attenuated and sublinear at most sites. Stimulation
simulating a straight edge ranging from ⫺6 to ⫹6° in 1°
increments (⫾2.63-ms interbarrel delays in 0.44-ms incre-
ments) provided a more precise view of changes in sharp wave
power with small changes in interbarrel delays (Fig. 2B). In all
three stimulation conditions (arc, diagonal, and row), the larg-
est slow-wave responses occurred during simultaneous stimu-
lation (0°) and were supralinear in electrodes adjacent to the
maximum response. Arc and diagonal stimulation (Fig. 2B, top
and middle rows, respectively) also produced large and often
supralinear responses at interbarrel delays ⱕ1.75 ms (diagonal)
and 2.63 ms (arc) that corresponded to 4 and 6°, respectively.
Responses during row stimulation differed in that supralinear
responses were confined almost entirely to simultaneous (0°)
stimulation with attenuation and sublinear responses becoming
apparent at interbarrel delays of ⫾0.87–1.31 ms (⫾2–3°).
As depicted in the example of Fig. 1E, when supralinear
responses were evoked, they were confined to the N1 and P2.
In all animals, the P1 was either linear or sublinear. This effect
is depicted again in Fig. 3A, displaying wideband (1–1,000 Hz)
⫾6° (⫾2.63 ms). Full in-phase recovery would not be expected
until a delay of 2.9 ms, which was not examined here.
Compared with the slow wave, averaged power maps of FOs
indicated that they were consistently more confined to the
principal barrels in all stimulation conditions (Fig. 2, C and D).
During asynchronous stimulation at ⫾45° (Fig. 2C), FO am-
plitude dropped rapidly at angles of ⫾1° (interbarrel delays of
⫾0.44 ms) with supralinear responses (Fig. 2C, white dots;
P ⱕ 0.05) largely confined to this temporal window. As with
the slow-wave, attenuated and sublinear responses predomi-
nated at angles ⬎ ⫾5° (2.18 ms; Fig. 2C; black dots; P ⱕ
0.05). Similar to the example of Fig. 3, submillisecond phase
sensitivity was apparent in the power maps when smaller 1°
(0.44-ms) angular increments were simulated (Fig. 2D). The
largest FO responses were evoked by 0° (simultaneous) and
⫾1° angles (⫾0.44 ms), reached a minimum at ⫾3– 4°
(⫾1.31–1.75 ms), and appeared to be recovering amplitude at
⫾6° (⫾2.63 ms). Supralinear responses were most prevalent
during simultaneous or near-simultaneous stimulation (how-
ever, note ⫹2 to ⫹5° conditions during both arc and row
stimulation, where supralinear responses appear to cluster
around the earliest vibrissa contacted).
Power was averaged across all 64 electrodes in the array to
simplify direct comparison of changes in FO and slow-wave
amplitude as a function of simulated stimulus angle and inter-
barrel delay (Fig. 4). With a range of ⫾45° stimulation, FO
displayed the steepest decline in power with increasing angle

FIG. 2. Maps of power for slow waves (1–100 Hz) and fast oscillations (FOs; 250 –1,000 Hz) for the different vibrissa groups. A: power was computed as
the root-mean-squared (RMS) amplitude of digitally filtered SEPs, averaged across animals and mapped as a function of stimulation angle (⫾45° range)
separately for the Arc (A3–E3, top row), Diagonal (A1–E5, middle row), and Row (C1–C5, bottom row) vibrissa groups. In all 3 groups, slow-wave power was
largest throughout the array at 0°, with significant (P ⱕ 0.05) supralinear responses (white dots) in electrodes adjacent to the principal barrels (black circles).
Supralinear responses were also recorded from several electrodes during asynchronous stimulation at ⫺1 and ⫹1–10° for arc, ⫺1 and ⫹1 and ⫹10° for diagonal,
and ⫺1° for row stimulation groups. However, RMS power declined rapidly with intervibrissa delays ⬎2 ms and approached half-peak amplitude at angles of
⫾5° in all groups. At greater angles, sublinear responses (black dots) predominated. At greater angles, a pattern emerged where the response of the initial vibrissa
contacted (i.e., A3 for ⫺45° or E3 for ⫹45° of the arc) to be largest, with marked suppression of subsequently displaced vibrissae. B: same as A, but showing
maps for a ⫾6° range of angles in 1° increments. In all vibrissa groups, supralinear responses were confined to a window of several degrees flanking 0°. Sublinear
responses at angles ⬎ ⫾1° were particularly notable during row stimulation. C: compared with the slow wave, FO power was more constrained to the principal
barrels for each group. Significant supralinear responses were most pronounced throughout the array during 0° stimulation of arcs and rows, but were also present
during diagonal vibrissa stimulation. Similar to the slow wave, sublinear responses predominated with angles ⬎ ⫾5°. D: however, in contrast to the slow wave,
FO declined with angle much more sharply, reaching half-peak amplitude (compared with the maximum 0° response) at ⫾2°. As noted in the example of Fig.
3, FO power displayed a phase sensitivity in all vibrissa groups, approaching minima at ⫾3– 4°, where the 1.31- to 1.75-ms intervibrissa delays are close to the
1.45 ms required to bring FO out of phase between barrels. In all groups, FO amplitude began to recover at ⫾6° with 2.63-ms intervibrissa delay, close to the
2.9-ms delay required to bring FO fully back into phase.

J Neurophysiol • VOL 96 • OCTOBER 2006 • www.jn.org

1986 K. M. RODGERS, A. M. BENISON, AND D. S. BARTH
(Fig. 4A, red traces). The total angular window widths (sym-
metrical about 0°) at which FO amplitude had dropped to
half-peak amplitude were 5.59 ⫾ 0.25, 6.91 ⫾ 0.94, and 3.5 ⫾
0.1° for arc, diagonal, and row stimulation, respectively (Fig.
4A, light red traces). Half-amplitude angular windows for FO
were significantly narrower for the row versus arc stimulation
conditions (P ⫽ 0.011), and the grand average across condi-
tions was 5.3 ⫾ 0.2° (Fig. 4A, dark red trace). The half-
amplitude angular window computed for the sharp wave was
consistently broader than FO, averaging 15.9 ⫾ 0.46° (Fig. 4A,
dark blue trace) and equaling 19.3 ⫾ 1, 17.45 ⫾ 2, and
J Neurophysiol • VOL
11.18 ⫾ 0.71° for arc, diagonal, and row stimulation, respec-
tively. Again, row stimulation produced a significantly smaller
angular window than the arc (P ⫽ 0.002). The more rapid
decline of FO with stimulation angle compared with the slow
wave was significant across conditions (P ⬍ 0.00003) as it was
for the separate arc, diagonal, and row conditions (P values of
0.005, 0.019, and 0.006, respectively).
Similar differences between FO and slow-wave amplitude
were observed when finer 1° changes in stimulus angle were
examined (Fig. 4B). Here, the half-amplitude angular width of
FO (Fig. 4B, dark red trace) averaged 2.69 ⫾ 0.06°, which was
significantly smaller (P ⫽ 0.000015) than 6.33 ⫾ 0.15° for the
slow wave (Fig. 4B, dark blue trace). Angular widths of FO
and slow wave for the arc, diagonal, and row stimulation
conditions were 2.8 ⫾ 0.12, 3.1 ⫾ 0.22, 2.1 ⫾ 0.19, and 6.5 ⫾
0.45, 7.3 ⫾ 0.61, 5.1 ⫾ 0.35, respectively, with FO (Fig. 4B,
light red traces) significantly smaller than the slow wave (Fig.
4B, light blue traces) in each condition (P values of 0.007,
0.009, and 0.031, respectively). No significant differences in
Downloaded from jn.physiology.org on January 24, 2007
half-amplitude angle widths were observed between conditions
within the FO or slow-wave frequency bands when examined
separately. As in the example of Fig. 3, FO power appeared to
reach a minimum in all animals at ⫾3– 4° and begin to recover
at ⫾6°. The spacing of interbarrel delays between the FO
minima was close to the average FO period of 2.9 ms.
DISCUSSION
Sublinear responses, feedforward inhibition, and
temporal integration
Temporal integration in somatosensory cortex is shaped
largely by inhibition. Slow- or long-latency inhibition (Con-
nors et al. 1988) corresponds to a long period (50 –100 ms) of
maximum response suppression in somatosensory cortex noted
in paired stimulus paradigms (Gardner and Costanzo 1980;
FIG. 3. Phase-sensitive interactions of FOs (about 350 Hz) superimposed
on the initial P1 slow wave. A: wide-band (1–1,000 Hz) SEPs from an
electrode site near barrel C3 during a ⫾6° range of arc stimulation in one
animal. At all angles, the P1 of the evoked slow wave (blue traces) was less
than the linear model (red traces), whereas the N1 was supralinear. Wide-band
filtering revealed FO superimposed on the P1 and beginning of the N1,
particularly evident at 0° stimulation (see C). B: in contrast to the P1, which
was sublinear at all angles, superimposed FOs were maximum and supralinear
at 0 and ⫹1°. FO also displayed distinct phase-sensitive interactions corre-
sponding to submillisecond changes in intervibrissa delays. At ⫾3– 4°, in-
tervibrissa delays were 1.31–1.75 ms, which was close to half the period (1.45
ms in this example) required to bring FO exactly out of phase. These angles
produced minimum amplitude FO, with partial recovery of amplitude at ⫾6°
(⫾6.6° stimulation would be required to produce the 2.9-ms intervibrissa
delays required to bring FO fully back into phase). C: black trace depicts
essentially unfiltered data (1–3,000 Hz) from the 0° stimulation condition. Blue
trace beneath this shows the same data filtered for 1–250 Hz, providing an
estimation of what the P1 would look like without FO. Below this, the 2 traces
are superimposed as a composite to better examine deviations of FO waves
about the slow wave. To highlight these deviations, they are filled in with
either red or green, depending on their polarity. Below this is a difference
waveform computed by subtracting the slow waveform from the wide-band
one. This shows clear FO, also colored alternatively with red and green for
comparison to the composite. Area under each FO wave in the difference
waveform is (by the way it was computed) exactly the same as the respective
colored areas on the composite drawing. Finally, the red trace at the bottom
shows 250 –1,000 band-pass–filtered data used for subsequent analysis of FO,
which is exactly the same as the difference waveform and reveals no filter
artifact.
96 • OCTOBER 2006 • www.jn.org
 COINCIDENCE DETECTION IN THE BARREL FIELD
FIG. 4. Comparison of FO and slow-wave power as a function of stimulus
angle. A: total power was estimated by averaging RMS amplitude in the FO or
slow-wave frequency bands (1–100 and 250 –1,000 Hz, respectively) across all
electrodes in the array. In all 3 stimulus conditions, FO power (separate
vibrissa groups ⫽ thin red traces; average across groups ⫽ thick red trace) fell
to half-maximum amplitude by ⫾2–3°, yielding an average “half-amplitude
window” of 5.3° or 2.3-ms intervibrissa delay. This was one third the
half-amplitude angle of the slow wave (separate vibrissa groups ⫽ thin blue
traces; average across groups ⫽ thick blue trace) at 15.9° or 7-ms intervibrissa
delay. B: FOs maintained this higher temporal resolution when examined in the
⫾6° angular range. Here, the half-amplitude window for FO was 2.69°
(1.18-ms delay) compared with 6.33° (2.6-ms delay) for the slow wave.
Submillisecond phase sensitivity is still notable in total FO power, with
minima separated by the average FO period of 2.9 ms, when FO would be
expected to be out of phase between barrels, and a partial recovery at ⫾6°
(2.63-ms intervibrissa delay) as the FO come back into phase between barrels.
Submillisecond phase sensitivity was not observed in slow wave power for any
of the vibrissa groups.
Hellweg et al. 1977; Mountcastle et al. 1957; Shimegi et al.
1999; Simons 1985; Simons and Carvell 1989; Steriade 1984;
Steriade et al. 1979), exceeding all but the maximum in-
tervibrissa delays examined in the present study. Our data
indicate a more rapid decline in cortical responsiveness, most
pronounced at intervibrissa delays of 10 –15 ms, that is most
likely attributable to fast feedforward inhibition (Connors et al.
1988). This conclusion is supported by observation that the
onset of rapid suppression is typically delayed in the PMBSF
by application of the ␥-aminobutyric acid type A (GABAA)
blocker bicuculline (Berger and Luscher 2003). Unit studies of
paired vibrissa stimulation in rats, typically reveal a time-
dependent suppression after initial stimulation that is maxi-
mum at about 10 –20 ms (Shimegi et al. 1999; Simons 1985;
J Neurophysiol • VOL 96 • OCTOBER 2006 •
1987
Simons and Carvell 1989), similar to intervibrissa delays
yielding minimum responses in the present study. Feedforward
inhibition is also typically more widely distributed than exci-
tation, consistent with the widespread suppression and signif-
icant sublinear responses observed for simulated stimulus an-
gles ⬎ ⫾10° in the present results. Finally, recent evidence
combining direct cortical responses to electrical stimulation
with subsequent vibrissa stimulation suggests that intracortical
inhibitory pathways play a minimal role in interbarrel-suppres-
sive effects, and that either widespread thalamocortical feed-
forward inhibition or intrathalamic inhibition may be involved
(Civillico and Contreras 2005, 2006). There is compelling
evidence that rapid feedforward inhibition results from mono-
synaptic thalamocortical input to inhibitory interneurons, in
tandem with excitatory input to the pyramidal cells, establish-
ing a brief window of excitability before inhibitory suppression
(Gabernet et al. 2005; Sun et al. 2006; Swadlow 2003, 2002).
Such a narrow window of excitability would suggest that
pyramidal cells are maximally responsive to closely timed
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excitatory inputs in that only these stimuli would be given a
chance to bring cells to threshold. Supporting this conclusion
are unit recordings indicating that regular spiking units (RSUs,
probably pyramidal cells) show peak facilitation with simulta-
neous multivibrissa stimulation (Shimegi et al. 1999) and drop
off rapidly in response amplitude with increases in intervibrissa
delays greater than a couple of milliseconds, similar to the
rapid decline of both FO and slow-wave power in the present
study.
Supralinear responses, excitation, and temporal integration
Within the brief window of excitation imposed by feedfor-
ward inhibition, our data indicate that short intervibrissa delays
(⬍2 ms) produce significant supralinear responses in wide
areas of the PMBSF for both slow-wave and FO power
measurements. These results are in agreement with a number
of unit studies demonstrating response facilitation with closely
timed stimuli (Ego-Stengel et al. 2005; Erchova et al. 2003;
Ghazanfar and Nicolelis 1997; Shimegi et al. 1999, 2000). It is
thus puzzling why several unit studies of the spatiotemporal
dynamics of multivibrissa stimulation report a predominance
of suppressive interactions even with short (0- to 5-ms) in-
tervibrissa delays (Mirabella et al. 2001; Simons 1985; Simons
and Carvell 1989). As noted by Simons and coworkers (Si-
mons 1985), one explanation may be that the failure to find
supralinear responses to simultaneous vibrissa deflections re-
flects a ceiling effect produced by occlusion of multiple inputs
to maximally activated neural pools. In studies where multi-
vibrissa stimulation at short intervals do not produce supralin-
ear responses, there is usually a dramatic recovery from sub-
linearity with decreasing delay, approaching a linear or barely
sublinear response with simultaneous stimuli (Mirabella et al.
2001; Simons 1985; Simons and Carvell 1989). This finding is
consistent with increased excitation or less inhibition resulting
from closely timed stimuli, even if the net effect is not a
supralinear response.
We also reported a ceiling effect arising from maximum
depolarization in field potential measurements of excitability
cycles in the PMBSF (Barth and Di 1991). This may explain
why the supralinear responses of the present data are almost
exclusively recorded from electrodes surrounding the principal
www.jn.org
1988 K. M. RODGERS, A. M. BENISON, AND D. S. BARTH
vibrissa barrels for a given stimulation condition (i.e., 0°; Fig.
2A). Responses from sites corresponding to the principal
vibrissa barrels typically sum linearly (except, note Fig. 2C;
0°). Similar results, obtained from mapping studies of spatially
distributed unit responses in the PMBSF, indicate supralinear
summation only in the far surround of a neuron’s receptive
field and rarely in the center (Ghazanfar and Nicolelis 1997).
The largest supralinear responses are usually observed in cells
that respond weakly or not at all to individual vibrissae but are
robustly driven by combined stimulation, suggesting minimum
single-vibrissa response levels are most effective for revealing
supralinear multivibrissa effects (Ego-Stengel et al. 2005;
Ghazanfar and Nicolelis 1997; Shimegi et al. 1999, 2000).
Interestingly, recent examination of intervibrissa interactions
using voltage-sensitive dyes failed to find supralinear re-
sponses in the PMBSF to simultaneous vibrissa deflection,
except rarely and in the extreme periphery of the principal
barrels (Civillico and Contreras 2006). One possible explana-
tion for this difference with the present data is that these
investigators used paired vibrissa stimulation as opposed to
five-vibrissa stimulation of the present study. Facilitative in-
teractions between multiple barrels may be better suited to
production of reliable supralinear responses.
Fast oscillations versus slow waves in coincidence detection
Although the brief window of responsiveness in our results
is probably shaped in large part by fast inhibition, the angular
tuning of FO is significantly narrower than the slow wave,
suggesting involvement of an additional mechanism. Unlike
the slow wave, angular sensitivity of FOs reveals a periodicity
that corresponds to the average frequency of 345 Hz in these
animals, suggesting submillisecond phase sensitivity in addi-
tion to the inhibitory damping evident for both FO and the slow
wave. Because FOs represent the earliest and the most pre-
cisely tuned response to simultaneous or near-simultaneous
vibrissa displacement, they may serve a primary role in coin-
cidence detection in the PMBSF. The angular tuning of slow
waves is roughly threefold wider than that of FO, suggesting a
heightened sensitivity to coincident stimuli, yet one that is not
further narrowed by the phase sensitivity apparent in FO. It is
notable that only the N1 and P2 produce supralinear responses
to coincident stimuli; the P1 is typically linear or sublinear,
suggesting different functional roles for these temporal com-
ponents. Laminar field potential studies have demonstrated that
the P1 reflects depolarization of the proximal apical dendrites
of supragranular (Di et al. 1990) and, to a lesser extent,
infragranular (Staba et al. 2004) pyramidal cells in the PMBSF.
Although not registering supralinear responses to simultaneous
stimuli, the P1 may reflect establishment of an essential back-
ground of common excitation among subgroups of activated
barrels, bringing select populations of cells near threshold and
facilitating phase-sensitive interbarrel interactions of concur-
rently recorded FOs. Recent computational models suggest
that, under conditions of near-threshold depolarization, even
weakly correlated synaptic inputs can dramatically increase
discharge probability (Salinas and Sejnowski 2000), possibly
improving coincidence detection between pyramidal cells of
mutually depolarized barrels. Laminar recording of the subse-
quent N1 in PMBSF indicates depolarization of distal apical
dendrites of both supra- and infragranular pyramidal cells (Di
J Neurophysiol • VOL
et al. 1990). Supralinear responses recorded for the N1 and P2
during closely timed stimuli suggest a late phase of coinci-
dence detection distinct from FOs. It cannot be determined
from our data whether this is conducted independently of FO or
is in fact boosted by preceding discharge of FO-generating
neurons. However, the long poststimulus latency and wider
spatial distribution of these late components suggest the in-
volvement of multisynaptic pathways for their generation,
perhaps serving to distribute the results of coincidence detec-
tion performed locally in the principal barrels to wider areas of
the PMBSF.
Homogeneity of multivibrissa integration: two-dimensional
processing in the barrel field
Anatomical studies show a bias toward interconnectivity
between barrels within rows versus arcs in the PMBSF (Ber-
nardo et al. 1990; Hoeflinger et al. 1995) that may be reflected
in elongation of vibrissa-evoked activity patterns along the
Downloaded from jn.physiology.org on January 24, 2007
rows (Armstrong-James and Fox 1987; Kleinfeld and Delaney
1996; Simons 1978). Perhaps for this reason, a number of
studies concerned with multivibrissa stimulation have exam-
ined integration within barrel rows as opposed to arcs (Gold-
reich et al. 1998; Kleinfeld and Delaney 1996; Simons 1985).
Investigations that have compared multivibrissa stimulation
within an arc versus row at short interstimulus intervals vari-
ously suggest a tendency toward supra- versus sublinear re-
sponses in arcs and rows, respectively (Ego-Stengel et al. 2005;
Ghazanfar and Nicolelis 1997), or sublinear responses in both
(Mirabella et al. 2001).
A surprising finding of the present experiment is that there is
little difference in the spatiotemporal pattern of sub- or supra-
linear responsiveness in the rows versus arcs, and neither
differs from the diagonal group of vibrissa. To our knowledge
intradiagonal integration within the PMBSF has not been
previously examined. For all three conditions (arc, diagonal,
and row), course range (⫾45°) stimulation yields half-ampli-
tude angular windows averaging 5.3° for FO and 15.9° for the
slow wave. Closer examination, with a finer range of stimula-
tion angles (⫾6°), yields half-amplitude angular windows
averaging 2.7 and 6.3° for FO and slow wave, respectively.
Whereas the angular windows in both frequency bands are
significantly smaller in the rows (FO ⫽ 2.1°, slow wave ⫽
5.1°) than in the arcs (FO ⫽ 2.8°, slow wave ⫽ 6.5°),
suggesting a slight improvement of angular tuning in the rows
(neither significantly differing from the diagonal), this differ-
ence is quite small. Indeed, the most striking result is the
similarity in all response characteristics between stimulus con-
ditions. These characteristics include the spatial distribution of
responses (relative to the principal barrels), sublinear and
supralinear responsiveness with large and small stimulus an-
gles, respectively (intervibrissa delay), and correlated changes
in both FO and slow-wave power, suggesting an appreciable
absence of direction specificity within the PMBSF. Further-
more, in all experimental conditions, the decline of both FO
and slow-wave power with stimulus angle is nearly symmet-
rical about 0°, indicating that intervibrissa interactions are
insensitive to the order in which the vibrissae are stimulated.
Field potential mapping was used in the present study to
examine the central tendency of population interactions in the
entire PMBSF. This central tendency suggests a predominant
96 • OCTOBER 2006 • www.jn.org
 COINCIDENCE DETECTION IN THE BARREL FIELD
spatial and temporal homogeneity underlying multivibrissa
integration. However, unlike unit recording, field potential
recordings may be relatively insensitive to selective activation
of subpopulations of cells within or between barrels. Thus our
results ignore the potential contributions to spatiotemporal
integration of somatotopically organized motion direction
maps, recently demonstrated in single- and multiple-unit re-
cordings (Andermann and Moore 2006). Proper examination of
possible contributions from directionally tuned subpopulations
at the subcolumnar level to the present field potential records
would require multivibrissae stimulation at a variety of orien-
tations instead of the consistently orthogonal orientation used
here.
Coincidence detection and spatial feature analysis
The present experiments were performed in anesthetized rats
with passive stimulation. As such, they may be assumed to
provide a simplified view of mechanisms underlying spatial
feature analysis in the awake behaving animal, where atten-
tional states, whisking strategies, head position, and accompa-
nying interactions between motor and somatosensory cortex all
must come into play. However, the sharp angular tuning of
population responses recorded here suggests that simultaneous
or near-simultaneous displacement of multiple vibrissae may
constitute a preferred stimulus in the PMBSF. Responses to
asynchronous vibrissa contact, with delays more than a couple
of milliseconds, are considerably suppressed. Inhibition has
long been thought to enhance both spatial contrast (Laaris et al.
2000; London et al. 1989; Mountcastle and Powell 1959;
Petersen et al. 2001; Simons 1995; Simons and Carvell 1989)
and temporal contrast (Gabernet et al. 2005; Gardner and
Costanzo 1980; Pinto et al. 2000, 2003) in somatosensory
cortex. Temporal contrast enhancement could serve to improve
resolution of asynchronous input by briefly suppressing re-
sponses to an initial stimulus in preparation for response to a
subsequent one (Gardner and Costanzo 1980). In the PMBSF,
this would result in an improved resolution of sequentially
activated vibrissae within a row when brought in contact with
an object during forward extension (Simons 1985).
However, our results support an alternative role for temporal
contrast enhancement, one in which asynchronous vibrissa
contact outside a short time window of several milliseconds is
powerfully suppressed in favor of simultaneous or nearly
simultaneous contact, producing sharply tuned supralinear re-
sponses particularly notable in high-frequency oscillations aris-
ing from additional phase sensitivity. In this way, intra- and
interbarrel circuitry may serve the function of coincidence
detection (Berger and Luscher 2003; Gabernet et al. 2005;
Ghazanfar and Nicolelis 1997; Pinto et al. 2000, 2003; Roy and
Alloway 2001; Schaefer et al. 2003; Shimegi et al. 1999, 2000;
Stuart and Hausser 2001; Swadlow 2003), favoring inputs with
low temporal contrast, and identifying common object features
on the basis of simultaneous contact with subgroups of vibris-
sae (Pinto et al. 2000, 2003; Shimegi et al. 2000). The equiv-
alence of function apparent during arc, diagonal, and row
stimulation suggests that the PMBSF may be capable of work-
ing as a two-dimensional integrative array, processing spatial
features according to common mechanisms despite the direc-
tion with which the vibrissae pass across an object. Spatial
features, extracted from coincident contacts within two-dimen-
J Neurophysiol • VOL
1989
sional vibrissa space, include orientation of straight edges or
planes (Shimegi et al. 2000), with a potential resolution of 1°
as suggested here. However, the same mechanism of coinci-
dence detection should also provide information about object
curvature or shape (Benison et al. 2006) indicated by behav-
ioral studies of object discrimination in rats (Harvey et al.
2001; Polley et al. 2005).
ACKNOWLEDGMENTS
We thank Dr. Eva Fifkova for the careful review of this manuscript and
helpful comments.
GRANTS
This research was supported by National Institute of Neurological Disorders
and Stroke Grant 1 R01 NS-36981, the Marion Downs Center, and the
University of Colorado Undergraduate Research Opportunity Program.
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