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The Journal of Neuroscience, May 15, 1998, 18(10):3955-3966
Response Classes in the Dorsal Cochlear Nucleus and Its Output
Tract in the Chloralose-Anesthetized Cat
Philip X.
Joris
Department of Neurophysiology, University of Wisconsin-Madison,
Madison, Wisconsin 53706, and Coleman and Epstein Laboratories,
Department of Otolaryngology, University of California at San
Francisco, San Francisco, California 94143-0526
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ABSTRACT |
Neurons in the dorsal cochlear nucleus (DCN) can be classified into
three major physiological classes on the basis of responses to pure
tone and broadband noise stimuli. A circuit diagram that associates
these classes with different cell types has been proposed. According to
this proposal, type II cells are inhibitory interneurons that respond
well to tones and poorly to broadband noise, type IV cells are
projection neurons with the opposite behavior, and type III cells are
an inhomogeneous class with intermediate properties. To test the
associations proposed, I compared the response type distribution in the
DCN with its output tract, the dorsal acoustic stria (DAS), in
chloralose-anesthetized cats.
Axonal recordings in the DAS showed type III and IV responses as in
DCN, but no type II responses. Compared with reports in decerebrate
animals, fewer type IV neurons were encountered having sustained
inhibition that generated strongly nonmonotonic responses to tones in
both DCN and DAS. The presence of type II responses in the nucleus, but
not in the output tract, offers strong support for the proposed
association with DCN interneurons. On the other hand, the distinction
between type III and IV responses needs refinement because the
differences are only graded and because both types of responses occur
in DAS, which shows that they are both associated with projection
neurons.
Key words:
audition; dorsal cochlear nucleus; dorsal
acoustic stria; chloralose; response type; cat
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INTRODUCTION |
All auditory information reaching
the CNS is channeled through the cochlear nuclear (CN) complex. The
dorsal cochlear nucleus (DCN) is the most complex subnucleus, and
despite a considerable body of knowledge regarding its physiology and
anatomy, its function remains unknown. In an elegant series of studies,
Young and his colleagues (Young and Brownell, 1976 ; Young, 1980; Voigt
and Young, 1980, 1988, 1990; Young and Voigt, 1982; Shofner and Young,
1985; Spirou and Young, 1991) constructed a classification scheme of DCN response patterns based on an earlier scheme of Evans and Nelson
(1973), and they proposed a correspondence with morphological cell
types in a circuit that explains observed response patterns at a
qualitative level. Two issues related to this scheme were examined in
the current experiments. First, I wished to characterize the DCN input
to the midbrain by recording directly from its output tract to
differentiate responses of DCN interneurons and projection neurons. The
evidence for associations between certain response types and
interneurons or projection neurons is incomplete, but few attempts at
direct recordings from dorsal acoustic stria (DAS) have been made
(Kiang et al., 1973; Adams, 1976), despite the fact that such
recordings provide a straightforward means to assess some of the
proposed associations. A second issue concerns anesthesia. Progress in
understanding of the DCN has been hampered by its susceptibility to
anesthesia, which has been demonstrated indirectly by comparison of
population statistics for anesthetized and unanesthetized preparations
(Evans and Nelson, 1973; Mast, 1973; Kaltenbach and Saunders, 1987;
Rhode and Kettner, 1987; Gdowski and Voigt, 1997) and directly for a
few individual cells before and after administration of a barbiturate
(Young and Brownell, 1976). Many investigators have resorted to a
decerebrate preparation, which has other drawbacks. Previous reports
(Evans and Nelson, 1973; Young and Brownell, 1976; Kaltenbach and
Saunders, 1987; Evans and Zhao, 1993) suggested that anesthesia with
 -chloralose seemed to affect the inhibition in DCN responses least,
but limited data are available in these early studies to assess the
generality of this claim.
In this report I compare responses from projection neurons, recorded in
the DAS, with responses from DCN (note that the term "projection
neuron" does not preclude that these cells functionally have an
"interneuronal" role by virtue of collaterals within the cochlear
nucleus). To enable comparison with the decerebrate preparation, I used
the classification scheme constructed by Young and coworkers (Young and
Brownell, 1976; Young, 1980; Voigt and Young, 1980, 1988, 1990; Young
and Voigt, 1982; Shofner and Young, 1985; Spirou and Young, 1991),
which is based on response maps obtained by graphing average response
rates over a range of stimulus frequencies and intensities, as well as
on the response to broadband noise. Comparisons will be made largely
with published data for the cat, because there are indications for
species differences in the proportions of response types (Davis et al.,
1996; Stabler et al., 1996; Gdowski and Voigt, 1997). The conclusions
drawn therefore may need modification as applied to other species.
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MATERIALS AND METHODS |
Animal preparation. Young adult cats were induced
with an intramuscular injection of a mixture of ketamine (20 mg/kg) and acepromazine (0.4 ml). In some animals mucous secretions were reduced
with a subcutaneous injection of atropine sulfate or atropine methyl
nitrate (0.1 mg/kg). A cannula was placed in the cephalic vein with a
slow drip of Ringer's solution; 60 mg of -chloralose was dissolved
in a warm 1:3 mixture of propylene glycol and saline. While the heart
rate was monitored, this solution was slowly injected intravenously
until no limb withdrawal reflexes could be provoked, and the procedure
was repeated when these reflexes returned. In about half the animals,
chloralose was supplemented with a slow intravenous injection of
diazepam to obtain more complete flaccidity of the limbs. Body
temperature was maintained at 37°C by a feedback-controlled heating
pad. After a tracheotomy was performed, the nuccal ridge and external
ear canal(s) were exposed. The ear canal was cut, and the pinna and
temporalis muscle were retracted or removed. A craniotomy was performed
as laterally as possible without intruding on the squamous portion of
the temporal bone. Parts of the lateral cerebellum were aspirated until
the DCN was visualized. The electrodes were positioned on the DCN under
visual control.
Exposure of the DAS followed the same general approach, but the
craniotomy was centered over the midline to allow exposure of both
sides. Cerebellum was aspirated, starting at the midline, until the
lateral recess and most dorsal portion of the DCN were visualized on
left and right side. Fascicles from the DCN can be seen as they cross
the inferior cerebellar peduncle and then run medial to descend along
the surface of the fourth ventricle (Adams, 1976). The electrode was
aimed just medial to the most dorsal point of this crossing. The
absence of strong field potentials makes single-unit isolation easier
in the DAS than in the fusiform cell layer of the DCN, but a drawback
is the difficulty in obtaining stable recordings. After the electrode
was positioned, warm 2% agarose was poured in the posterior fossa to
stabilize the brain.
Data collection and analysis. Search stimuli were low-level
tones, at the best frequency of the background activity, alternating with broadband noise. Single units were recorded with glass-insulated tungsten electrodes of ~3-4 M (MicroProbe, Clarksburg, MD) or sometimes glass micropipettes (3 M KCl, ~10 M),
mounted in a hydraulic microdrive controlled from outside the
sound-shielded room (IAC). The amplified and filtered neural signal was
fed to an audio amplifier, oscilloscope, and window discriminator,
which converted action potentials to standard pulses timed by the
computer.
Two different setups were used for stimulus generation and data
acquisition. Both were custom-made 16-bit digital stimulus systems
described previously [Schreiner and Sutter (19920 for the University
of California at San Francisco system; Rhode (1976) and Olson et al.
(1985) for the University of Wisconsin-Madison, system]. In the first
13 (University of California at San Francisco) experiments, stimuli
were delivered monaurally with an electrostatic driver (STAX 54)
connected to a plastic earbar via a shielded, metal container modeled
after Sokolich (1977). In later (University of Wisconsin-Madison)
experiments, monaural and binaural stimuli were delivered with dynamic
phones (Chan et al., 1993). In some of these experiments the frequency
response of the phones was compensated by a digital filter
("prewhitened") to flatten the spectrum at the output of the sound
system (see Results).
All driven and well isolated units were studied. After isolation of a
single unit, the approximate characteristic frequency [(CF) the
frequency with the lowest excitatory threshold], response to broadband
noise, and presence of inhibitory sidebands (if spontaneous activity
was present) were noted. Response maps, rate-level functions, and
poststimulus time histograms (PSTHs) were then collected and displayed
on line. Spontaneous rate (SR), CF, and a general overview of the
response of the cell to a range of frequency-sound pressure level
(SPL) combinations were obtained from a response map or tuning curve.
The response map program presented tone bursts in pseudorandom order of
frequency and intensity. Most often, a grid of 45 frequencies over
three octaves and in 4 dB steps was used; tone duration was usually 200 msec. In some of the later experiments, a coarser grid of combinations
was often used, and each combination was presented multiple times and
in nonrandom order. The tuning curve program tracked the excitatory
threshold (as described in Geisler and Sinex, 1982) and was used mainly
in the DAS recordings to speed data collection.
Rate-level functions were obtained for long duration tone bursts at CF
and for broadband noise bursts, with the following parameters: duration
100 or 200 msec with a 1:5 duty cycle, rise-fall times of 10 msec,
usually 40 repetitions in 5 or 10 dB increments. If time permitted, a
rate-level function to short tone bursts at CF (25 msec every 100 msec,
rise-fall times of 1.6 msec, at least 200 repetitions) was obtained.
Spikes were counted over the stimulus duration. To facilitate graphing
on a single abscissa, stimulus levels in figures are specified in dB
SPL (re 20 µPa) for tones and with an arbitrary reference (attenuator
setting) for broadband stimuli. Noise levels re 20 µPa, computed by
integrating the stimulus energy over a one-third octave band centered
on CF, were close to the attenuator dB values stated in the figure
labels and are specified separately in the figure legends only for
those cases in which the difference exceeded 10 dB.
Response classification. Physiological studies of DCN
circuit properties have for the most part used a classification scheme in the frequency-intensity domain (the response map scheme), whereas structure-function studies have relied mainly on the time domain (the
PSTH scheme) (for review, see Young, 1984; Rhode, 1990). In the
classification used by Young and colleagues, three major response
categories are distinguished. Quantitative criteria are stated in
Results; here a general description is given. Type IV units show high
SR, which is inhibited by pure tones over a broad range of frequencies
and SPLs. There is typically a small excitatory area of frequency-SPL
combinations around the CF, so that rate-level functions obtained at CF
are nonmonotonic. Despite the predominance of inhibitory responses to
pure tones, broadband noise stimuli are excitatory at all stimulus
levels (Young and Brownell, 1976). Type II units, on the other hand,
have low SR, respond weakly or not at all to broadband noise, and have
an excitatory response to pure tones (Young and Voigt, 1982). Type III
responses show spontaneous activity, an excitatory response to CF tones
and broadband noise at all SPLs, and response maps with inhibitory
sidebands. They are the least distinctive response type and are found
throughout the CN (Shofner and Young, 1985). "Type III+IV" refers
to the type III and IV classes combined, not to a new response
type.
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RESULTS |
Before comparing DAS and DCN responses I shall examine how
classification of responses in DCN of the chloralose-anesthetized animal compares with that in the decerebrate preparation. To enable comparison with the diverse classifications used in previous studies, responses are here sorted first on the basis of SR and response to CF
tones, then by the shape of the rate-level functions to broadband noise
and CF tones, and finally by the shape of the PSTH pattern over a range
of SPLs at CF.
Responses in DCN
Classification by responses to CF tones and spontaneous rate
DCN responses encountered under chloralose anesthesia resembled
those reported in decerebrate animals. Representative examples of
response maps are shown in Figure 1 as
iso-level contours (top row) and in a three-dimensional
(3-D) format (bottom row) for three cells with similar CF.
The response map of the type II cell in Figure 1A is
characterized by an absence of spontaneous activity and by orderly rate
changes with SPL and frequency. Above the threshold near 40 dB, the
firing rate increases steeply with SPL to a maximum rate of 180 spikes/sec and then decreases somewhat to ~150 spikes/sec at 80 dB.
The type III response (Fig. 1B) has a similar
excitatory central portion in the response map showing a monotonic rate
increase with SPL, but the cell displays spontaneous activity
(arrow on ordinate of top panels) revealing inhibitory sidebands flanking the central area, most strongly on the
high-frequency side. The type IV response (Fig. 1C) is
typified by a complex response map with wide areas of frequency-SPL
combinations over which spontaneous activity is inhibited. The response
to CF tones has a threshold near 0 dB SPL and is very nonmonotonic:
there is a net increase in the average firing rate over only a
restricted range of low SPLs. The central inhibitory area is flanked by
excitatory regions.
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Figure 1.
Examples of the three main DCN response types.
Data are plotted as response maps (top panels) and in a
3-D format (bottom panels). The type III and type IV
units were obtained in the same animal. Horizontal
arrows on ordinate of top panels show
spontaneous rate (SR). Symbols (inset on
right) for different sound pressure levels
(SPLs) apply to all top panels. Stimulus
parameters (number of presentations × stimulus
duration/repetition interval): 10 × 100/500 msec. The
characteristic frequency (CF) was 7.5 kHz for A and
B and 7 kHz for C.
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Table 1 shows the distribution of
response types based on SR and rate-level functions to pure tones, to
permit comparison with studies in which the response to noise was
either not determined (Evans and Nelson, 1973; Rhode and Smith, 1986b;
Rhode and Kettner, 1987) or was not the primary criterion used for cell
classification (Young et al., 1976, 1982). Cells were assigned to one
of three categories, defined by two criteria: nonmonotonicity and SR.
If the response was nonmonotonic at CF, the cell was classified as type
IV; otherwise it was classified as type II/III. The criterion was that
of Shofner and Young (1985). If the driven rate (measured rate  SR) at 35 dB above rate threshold was less than half the peak rate at
lower SPLs, the response was nonmonotonic. With this criterion,
nonmonotonic cells include those that are profoundly inhibited by CF
tones as well as the so-called type IV N-T cells (Shofner and
Young, 1985), in which average rate is not suppressed much below SR.
Type II/III cells were subdivided further according to an SR criterion:
type II cells have SR < 2.5 spikes/sec, and type III cells have
SR  2.5 spikes/sec. This criterion was first used by Young and
Brownell (1976) and later was shown by Young and Voigt (1982) to
segregate cells along other response properties as well.
For the responses recorded in the DCN under chloralose anesthesia
(n = 166; obtained from 23 animals), types III
(n = 71; 43%) and IV (n = 68; 41%)
neurons were represented equally, with type II cells constituting the
remaining 16% of the sample (n = 27). The mean SR
(Table 1, numbers in parentheses) of type III cells lay between that of
types II and IV. Early in this experimental series, one animal was
studied under barbiturate anesthesia; here type III responses
dominated, with type IV cells constituting only 10% of the sample, and
average SR was lower.
Comparison with previous studies is difficult for various reasons (see
Discussion). Nevertheless, there is sufficient consistency to discern
the following trends (Table 1). In decerebrate animals, ~50% of the
cells sampled are type IV, 25% are type II, and 25% are type III. It
appears that under chloralose, responses in the type III category
increased at the expense of type IV cells, a shift that is even more
dramatic under barbiturate anesthesia. The increase in type II
responses under barbiturate, relative to chloralose, is possibly
explained by a general decrease in SR. Similar effects of barbiturate
anesthesia on response type distribution and average SR, relative to
the awake (Rhode and Kettner, 1987) or decerebrate state, are present
in the data of Rhode and Smith (1986b) (Table 1). The distribution
obtained under chloralose anesthesia thus is intermediate between those seen in decerebrate preparations and those from
barbiturate-anesthetized animals.
Classification by responses to tones and broadband noise
Young and Voigt (1982) pointed out that monotonic (types II and
III) cells that differ in SR also differ in their responses to
broadband noise: cells with low SR respond poorly to noise, whereas
those with high SR show generally higher response rates. Accordingly,
type II and III classes were redefined on the basis of a relative noise
ratio  (Young and Voigt, 1982; Shofner and Young, 1985; Davis et
al., 1996), which is defined as [maximum driven rate to broadband
noise]/[maximum driven rate to a CF tone]. Monotonic units with a
poor response to noise, resulting in < 0.3, were classified as
type II; if was > 0.3 they were classified as type III. For
units with a nonmonotonic response to tones, the maximum rate used to
calculate was taken at the first local maximum above threshold.
Examples of rate-level functions to CF tones and broadband noise for
the three responses types are shown in Figure
2. The rate-level curve to 100 msec CF
tones (Fig. 2A, ×) of the type II cell rises steeply
to a maximum, then declines. There is no response to broadband noise
(Fig. 2A,  ). The relationship between the
responses to CF tones and broadband noise is reversed in the type IV
unit (Fig. 2C), where there is a high response rate to noise
but little response to tones, except at low SPLs. Finally, CF tones and
broadband noise cause similar maximal firing rates in the type III cell
(Fig. 2B). The values for the cells in Figure 2
were near 0 for the type II cell and near 1 for the type III and type
IV cell.
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Figure 2.
Representative rate-level functions for types II,
III, IV. Relative noise ratios (, defined in Results) were 0.002, 1.03, and 0.99, respectively. Stimulus parameters: 40 × 100/500
msec for noise (), 50 × 100/500 msec for long tone bursts
(×), 200 × 25/100 msec for short tone bursts (+). Tone bursts
were at the CF (in kilohertz) of each cell; A, 9.5;
B, 15.3; C, 11.6.
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Qualitatively, the shape of the tonal rate-level functions usually was
affected minimally by the stimulus parameters, although these
parameters could affect the response quantitatively. In 19 cells,
rate-level functions were obtained to both short and long tone
durations over a wide range of SPLs. Five cells with a monotonic
response to 100 msec tones had a nonmonotonic response to 25 msec
tones. There were no cells with a change in the opposite direction. The
remaining cells were consistently monotonic (n = 6) or
nonmonotonic (n = 8) for either stimulus regimen.
Particularly for type III and IV cells, the strength of the tonal
response and the degree of nonmonotonicity often depended on the
stimulus duration and repetition parameters. The cell in Figure
2B was monotonic to 100 msec tone bursts but
nonmonotonic to short (25 msec) tone bursts (for another example, see
Fig. 4D). The cell in Figure 2C was
nonmonotonic with both stimulus durations, but with short duration
tones was much larger (3.5 for 25 msec tones, 0.99 with 100 msec
tones), and the response to tones was suppressed below SR. For type II
cells, the shape of the rate-level functions and the relative response
strengths to tones and noise did not depend on stimulus duration; short and long tone burst rate-level functions superimposed (Fig.
2A), or more commonly, the latter were simply scaled
down with respect to the former, having no effect on unit
classification (see Fig. 4B).
Figure 3 shows the categorization of 141 units for which quantitative data for both noise and CF tones were
available, a subset of the 166 units of Table 1. To reduce subjectivity
the categorization is performed with binary decisions based on the two
quantitative criteria used previously by Young and coworkers (Young and
Brownell, 1976; Young, 1980; Voigt and Young, 1980, 1988, 1990; Young
and Voigt, 1982; Shofner and Young, 1985; Spirou and Young, 1991). Note, however, that these authors defined response classes on the basis
of a cluster of properties, which included these criteria but did not
follow a strict hierarchical classification tree.
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Figure 3.
Decision tree for classification of cells on the
basis of response to tones and broadband noise. The two main branch
points correspond to the two main criteria used: nonmonotonicity and
relative response to noise. Number and percentage of cells in each
branch are indicated. Dashed lines and criterion on the
right indicate inhomogeneities in the resulting classes
revealed by SR.
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Of the 141 cells, two showed exclusively inhibitory responses to either
tones or noise (type V) and are not considered further. The
nonmonotonicity criterion separated type IV from type II and III cells,
and the latter two types were distinguished on the basis of . The
response to long tone bursts was used to assess nonmonotonicity, except
for a minority of cells (~20%) for which only the short (25 msec)
tone burst response was available. Parcellation of 139 units into these
three response categories yielded 30 (22%) type II cells, 56 (40%)
type III cells, and 53 (38%) type IV cells. In a recent sample of
similar size in the decerebrate cat and using the same classification
criteria (although not a binary decision tree), Nelken and Young (1994)
obtained 18% type II cells, 33% type III cells, and 52% type IV
cells. Thus, as was the case with the distribution obtained with the SR
criterion (Table 1), the present data show a preponderance of type III
over type IV responses in comparison with decerebrate animals. The
proportion of type II responses to the total is similar in both
preparations.
In terms of signal processing abilities, differences in response to
narrow versus broadband stimuli are presumably more important than SR,
and is therefore intrinsically a more satisfactory criterion with
which to separate types II and III than is a distinction that relies
merely on the basis of SR (Table 1). Nevertheless, the subpopulations
resulting from strict application of the quantitative classification
criteria (Fig. 3) are inhomogeneous and unsatisfactory in several
respects. First, a number of type II cells appeared to be
miscategorized as type IV because of a strongly nonmonotonic rate-level
function. Application of the SR criterion (Fig. 3, dashed
lines) to the type IV category reveals seven cells with SR < 2.5 spikes/sec (of which six had SR = 0 spikes/sec). Two examples
are shown in Figure
4A,B; it is clear that
these cells fit into the type II category (compare Fig.
2A) better than into the type IV category, both
because of their poor response to noise and because of the shape of the
rate-level function to tones. Many type II cells in the decerebrate
animal are also nonmonotonic (Young and Voigt, 1982), but the
nonmonotonicity is a sloping decrease in rate with respect to SPL
rather than the sharp drop in firing rate at low SPLs seen in type IV
cells (compare Fig. 2A,C). Moreover, the response of
type II cells is typically incompletely suppressed at high SPLs.
Although it is not entirely clear whether the seven cells with low SR
are type II cells with a marked degree of nonmonotonicity or type IV
cells with low SR and a poor response to noise, these seven cells will
be classified as type II in the remainder of the analysis.
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Figure 4.
Examples of responses inconsistent with general
properties of their class. A, B, Two cells that were
classified as type IV based on their nonmonotonic response to long (100 msec) CF tones (×), but that are more consistent with type II because
of the absence of SR and the nearly absent response to noise ( indicates that noise stimulus was prewhitened). C, D,
Two cells classified as type II based on their monotonic response to
long duration tones and low relative noise response (RNR). Note
nonmonotonicity of response in D to short (25 msec, +)
CF tones. CFs (kilohertz) were A, 4.75;
B, 38.3; C, 13; D, 33. Stimulus parameters are as in Figure 2. For B, an
attenuator setting of 100 dB corresponds to a noise level of 81 dB.
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Conversely, 10 cells classified as type II cells stood out from the
rest of that population (Fig. 3) by virtue of their high SRs (>2.5
spikes/sec; mean = 26.4 spikes/sec). Two examples are shown in
Figure 4C,D. The high SR and other considerations suggest that these cells should be classified with type III or IV cells. They
showed PSTH patterns most commonly associated with type III+IV cells
(six Pauser-Buildup, one ON-OFF, one Negative responder, one Unusual;
see below for explanation of PSTH patterns). Moreover, cells with poor
noise responses were also recorded in DAS (see below), and there are
other indications in the literature (Young and Brownell, 1976; Kim et
al., 1990; Nelken and Young, 1994; Davis et al., 1996) and in the
present sample that some type III+IV cells have a low response to
broadband noise. To distinguish cells with high SR and poor response to
noise from cells with low SR and no response to noise, can simply
be redefined as the ratio of absolute rather than
driven rates, i.e., without subtracting the SR. This ratio
is indeed >0.3 for 8 of the 10 "problematic" type II cells
with high SR.
In addition to the 10 miscategorized type II cells just mentioned,
there were an equal number of type III+IV cells for which SR was high
(mean = 44 spikes/sec) and the response to noise inhibitory at one
or more SPLs (seven type IV cells, three type III cells). There is thus
a sizeable proportion of high-SR cells (20 of 104) that responded
poorly to noise but in other respects fit the traditional description
of type III or IV categories.
If SR and the modified are used to regroup the cells of Figure 3,
the resulting numbers and percentages are 29 (21%) type II, 64 (46%)
type III, and 46 (33%) type IV. The composition of these groups is
more homogeneous and presumably closer to that in the studies of Young
and colleagues (Young and Brownell, 1976; Young, 1980; Voigt and Young,
1980, 1988, 1990; Young and Voigt, 1982; Shofner and Young, 1985;
Spirou and Young, 1991; Nelken and Young, 1994), and in the remainder
of this paper cells will be analyzed according to this last assignment.
In conclusion, responses recorded in this study were similar enough to
those in the decerebrate animal to be sorted into the three basic
response classes established for that preparation. Nevertheless, there are also some differences, most notably the less frequent appearance of
strong and sustained inhibition typical of type IV responses in the
decerebrate cat.
Classification by PSTH
The time dimension, lost in the calculation of average firing
rates, is important to consider. A first indication hereof are the
sometimes pronounced differences in firing rate for tones of different
stimulus durations and repetition rates (Figs. 2C, 4D). Second, the temporal response pattern, obtained
as the PSTH to short tone bursts at CF, provides an alternative
classifier that has been used extensively in the CN, particularly in
intracellular labeling studies. The correspondence between the two
classification schemes has been studied in the decerebrate cat by
Shofner and Young (1985). To enable a comparison, we will use the main
PSTH categories used in that study.
PTSHs were obtained for 23 type II cells, usually over a wide range
(>50 dB) of SPLs. As in the decerebrate animal (Shofner and Young,
1985), PSTHs of type II cells proved to be diverse and could be
assigned to the four categories (Fig. 5):
Onset-slow (Os, n = 9),
Pauser-Buildup (n = 4), Chopper (n = 4), and Unusual (n = 4). Clearly, these assignments are
approximate, because responses often displayed features of several of
these qualitative categories, sometimes to different degrees at
different SPLs. For example, the PSTH in Fig. 5B was
categorized as Os because response probability tended to be
higher around stimulus onset, particularly at lower SPLs, but there
clearly is a chopping component in the response.
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Figure 5.
PSTHs of type II cells to 25 msec tone bursts at
CF (100 msec interstimulus interval). CFs and SPLs were
(A) 38.3 kHz, 65 dB, (B)
4.5 kHz, 75 dB, (C) 9.5 kHz, 80 dB,
(D) 9.5 kHz, 45 dB, (E) 8.6 kHz, 80 dB, and (F) 8.5 kHz, 75 dB. The number of
repetitions was 300 (B, F) or 200 (A,
C-E); number of bins = 200.
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Type III and IV cells showed various PSTH patterns similar to data
published for other preparations (Godfrey et al., 1975b; Shofner and
Young, 1985; Rhode and Smith, 1986b; Rhode and Kettner, 1987). The same
caveats apply as for the type II cells: PSTH patterns vary with SPL and
can show various components at a single SPL. It is shown below (see
Fig. 7) that it is particularly the change in PSTH with SPL
that sets type III and IV responses apart from other responses. Here,
the PSTH category of a cell is defined by the pattern that reveals the
most inhibition and that dominates the response over several SPLs;
e.g., if a Pauser-Buildup pattern is present at low SPLs and an
ON-OFF pattern at higher SPLs, the cell is classified as ON-OFF.
PSTHs obtained in 33 type III cells were predominantly Pauser-Buildup
(n = 15) and Chopper (n = 14), with
only three ON-OFF or ON-I, one Unusual, and one Negative responder
(for examples see below). This distribution is similar to that in the
decerebrate cat, in which Shofner and Young (1985) also found a nearly
equal number of Pauser-Buildup and Chopper patterns. Type IV cells
(n = 21) were predominantly Pauser-Buildup (n = 12) or ON-OFF or ON-I (n = 6),
with one Chopper, one Unusual, and one Negative responder. In contrast,
Type IV responses in the decerebrate animal are characterized by low or
no sustained rate, and give almost exclusively transient responses
(ON-OFF or ON-I). This difference is the time-domain equivalent of
the difference in rate-level functions pointed out earlier: there is
less sound-driven tonic inhibition under chloralose anesthesia than in
the decerebrate animal, consequently less nonmonotonicity in responses
to tones, and therefore a shift from type IV to type III responses.
Responses in the DAS
The response variety in the DAS partially overlapped with that
encountered in DCN. Comparison of the two sets of data are complicated
by the spatial contiguity of the DAS to the intermediate acoustic stria
(IAS), which contains axons from the posteroventral CN (PVCN), and by
the presence of descending fibers (Fernandez and Karapas, 1967; Warr,
1969; Adams, 1976; Adams and Warr, 1976; Smith and Rhode, 1989). The
following analysis is therefore guided by results from intra-axonal
labeling experiments, performed in parallel, and using the same
exposure and recording strategy (Joris et al., 1992; Joris and Smith,
1995) (P. Smith and P. Joris, unpublished observations). These
experiments confirm and extend observations in earlier physiological
and anatomical work (Godfrey et al., 1975a,b; Rhode et al., 1983a,b;
Smith and Rhode, 1989). Of relevance here, first, is a clear
association between certain onset PSTH patterns and cell types:
exquisitely timed pure onset responses (Oi) are
derived from octopus cells in the PVCN, and onset-chopper (Oc) responses are derived from large multipolar
cells in the ventral CN and deep DCN. Second, these experiments show
that the latter multipolar cells can have an extensive axonal
arborization within the ipsilateral DCN and give centrally projecting
axons that run contiguous to fusiform cell axons in the DAS. These
cells thus should be considered in DCN circuitry schemes and are
included in the following analysis. Indeed, these cells have recently
gained attention as the possible source of wideband inhibition to type IV cells (Nelken and Young, 1994; Winter and Palmer, 1995).
From a total sample of 122 units (obtained from eight animals, two of
which also supplied DCN data), the following were excluded: cells with
an Oi response, cells excited by the contralateral ear, and
cells for which the recording time was too brief to obtain the response
to broadband noise. From the 55 remaining DAS units, three were not
considered further because their only response to noise and tones
consisted of inhibition or because their response to tones was very low
and sluggish.
Oc responses are characterized not only by the chopping
onset pattern in their PSTHs but also by a wide dynamic range of
responses to short CF tone bursts (Rhode and Smith, 1986a). Of the 55 units, 10 showed these characteristics, as illustrated by the three
examples in Figure 6. The tonal
rate-level functions in particular are distinctively expansive, rather
than compressive, with increasing SPL. A wide dynamic range is often
also present in the responses to noise; however, these functions level
off at high SPLs in about half of the cells, perhaps because of the
very high discharge rates attained. Although PSTHs (Fig. 6, right
panels) may resemble those of type III and IV cells, especially
when considered at only a few SPLs, the absence of any nonmonotonicity
in the rate-level function and associated pauses in the PSTH make the
distinction between Oc and type III+IV cells clear-cut.
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Figure 6.
Examples of rate-level functions to tones and
noise for three Oc units recorded in the DAS. PSTHs for 25 msec tone bursts are shown in the right column at two SPLs
(arrows). The PSTHs in each panel have the same ordinate
scale and number of bins (200). CFs were (A) 4.8 kHz, (B) 23.8 kHz, and (C)
16 kHz.
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Oc responses have been observed mainly in PVCN recordings
[On-type L units in Godfrey et al. (1975a); Rhode and Smith (1986a); Smith and Rhode (1989); Winter and Palmer (1995)], but they also occur
in deep DCN near the PVCN border (Godfrey et al., 1975b; Joris et al.,
1992). Reexamination of the DCN sample revealed only four cells,
categorized as type III (Fig. 3), with expansive rate-level functions.
The PSTH to short tone bursts was available only for one of these cells
and showed the Oc pattern.
Using the nonmonotonicity and noise response criteria defined earlier
( calculated with absolute rather than driven firing rates), I
classified the remaining 42 units as 3 type II, 21 type III, and 18 type IV. The data for the three units shown in Figure 7 were obtained in the same animal. The
responses in Figure 7A,B were classified as type IV
(nonmonotonicity criterion was barely reached by responses in
B), and those in of Figure 7C were classified as
type III. The graded differences between the tonal rate curves in the
three panels are representative of the range of behaviors seen across
units and illustrate the arbitrariness of the nonmonotonicity criterion. The extent of the inhibitory trough on the SPL axis (Fig.
7A-C, left panels) corresponds in the time
domain (Fig. 7, right panels) to the degree to which the
inhibition is sustained throughout the stimulus duration. Although the
PSTHs show various shapes, the progression of PSTH shapes is similar
across type III and IV units: sustained (Primary-like or with slow
chopping) at low SPLs, with a pause of variable duration at mid-SPLs
(giving Pauser-Buildup, ON-OFF, or ON-I pattern), and usually
sustained again at the highest SPLs (Pauser or Chopper). Responses
having a sustained and profound inhibition over most of the SPL range (Fig. 7A) predominate in type IV units reported for the
decerebrate cat (e.g., Shofner and Young, 1985) but were encountered
infrequently here.
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Figure 7.
Rate-level functions to tones and noise of three
units, recorded in the DAS of one animal, which illustrate similarities
between type III (C) and type IV (A,
B) responses. Format as in Figure 6. PSTHs in the right
column are for the firing rate maxima obtained at a low SPL and
at the highest SPL, and for the trough in between
(arrows). CFs were (A) 22.8 kHz,
(B) 14.7 kHz, and (C) 4.3 kHz.
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The nearly equal number of type III (n = 21) and IV
(n = 18) responses recorded in the DAS matches well the
distribution in the DCN recordings (Fig. 3), consistent with the
proposal that type III and IV responses are derived from projection
cells of the DCN (Young, 1980). The finding of three type II cells in
the DAS, however, seems inconsistent with the presumed association of
these responses with DCN interneurons. Rate-level functions and PSTHs
of these three units are shown in Figure
8. Only one of these units had SR < 2.5 spikes/sec, and all showed a rate curve with the inflection at
mid-SPLs characteristically found in type III and type IV cells.
Comparison with the functions of Figures 2 and 7 shows that these three
units are more plausibly classified as type III cells or as type IV
cells that had a poor response to noise rather than as type II cells
(as was the case for responses of Figure 4C,D). Note that
short and long tone bursts yielded generally similar rate-level
function shapes despite sometimes large differences in absolute firing
rate (Figs. 6-8; also see Fig. 10).
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Figure 8.
Rate-level functions to tones and noise of three
unusual units recorded in the DAS (see Results). Format as in Figure 6.
CFs were (A) 1.1 kHz, (B)
1.45 kHz, and (C) 9.6 kHz.
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The scatter plots in Figure 9 provide a
summary of the relative responses to CF tones and noise of all DCN and
DAS units. For each unit the maximal firing rate in response to either
short (25 msec) or long (100 msec) tone bursts is plotted against the maximal firing rate for broadband noise of the same unit. If rates for
both short and long tone bursts were available, both are plotted and
joined by a dotted line. Several population trends can be seen. First,
Oc units (Fig. 9A) stand out by virtue of their
large maximal firing rates. Moreover, most Oc data points
are above the diagonal of equality (Fig. 9 A, dashed line),
indicating a higher response to noise. This is in contrast to type II
cells, which are all below the solid line indicating the criterion (0.3) used to define this response type. In fact, the opposite behavior
of type II and Oc units is more dramatic than is
illustrated by this figure. Over most of the dynamic range of
Oc units, the asymmetry between firing rates to tones and
noise is even stronger than implied by the maximum firing rates shown
here. This is so because rate-level functions of Oc units
to tones are expansive, whereas those in response to noise can be
compressive (Fig. 6). Second, as a population, for both tones and
broadband noise, maximum rates of type III cells in DAS and DCN are
indistinguishable (Fig. 9B), and the same holds true for
type IV cells (Fig. 9C) (Mann-Whitney U test).
Third, there is a wide range of maximal response rates in both type III
cells (Fig. 9B) and type IV cells (Fig. 9C). The
noise response ranges overlap with Oc responses at the high end and with type II responses at the low end. Interestingly, data
points for type IV responses are preponderantly above the diagonal of
equality (63% of 73 data points), whereas type III cells predominate
under the diagonal (68% of 127 data points). This is attributable to a
larger response to broadband noise in type IV than in type III cells
(Mann-Whitney U; p < 0.001), whereas the
maximal response to tones is similar in the two populations (Mann-Whitney U; NS). Thus, cells that are more strongly
inhibited by tones, and therefore classified as type IV, tend to be
more strongly excited by broadband noise than cells with little
inhibition to tones, classified as type III. Indeed, there is a weak
correlation (data not shown; r = 0.49; 64 measurements
in 41 cells) between the driven response to noise and the degree of
inhibition to tones, measured as the decrease in firing rate between
initial maximum and the minimum at an intensity above this maximum in
the rate-level function (e.g., difference in rate at two leftmost
arrows in Fig. 7). This is surprising because it is not a
simple consequence of the criteria that define these two types (Fig.
3): there is no a priori reason to expect different levels of noise
response in type III and IV cells. In fact, the use of the noise
criterion to distinguish type II and III (with type III cells having
the stronger response to noise), combined with the strong
nonmonotonicity and presumably stronger inhibition to tones in type IV
cells, points to the opposite prediction.
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Figure 9.
Relationship of maximal response (raw firing rate)
to broadband noise and CF tones. Dashed line indicates
equality of response; solid line indicates criterion
of 0.3. Dotted lines join data points for short and long
tone bursts if both were available for the same cell. Total number of
cells = 189. A, Oc
(n = 11 cells) and type II cells
(n = 29). B, Type III cells (64 in
DCN, 23 in DAS). Average rates (spikes per second): tones 144 (n = 127), broadband noise 126 (n = 104). C, Type IV cells (43 in
DCN, 19 in DAS). Average rates: tones 126 (n = 73),
broadband noise 177 (n = 62).
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Review of the results presented so far suggests that the majority of
DCN/DAS responses in the cat can be assigned satisfactorily to one of
three classes according to a parsimonious scheme that is an amalgam of
the two most frequently used classification systems. The three groups
are type II, Oc, and III+IV, and are based on the
shape of the PSTH and rate-level functions to short CF tones (expansive
for Oc, nonmonotonic with single maximum for type
II, variable for III+IV but usually with two maxima) and the response to noise (small or nonexistent for type II, very high for
Oc, variable in type III+IV). In the cases examined,
the rate-level function to short (25 msec) and long (100 or 200 msec)
CF tones generally were similar in shape, but large differences in
firing rate occurred (Figs. 2C, 4D,
8C). Presumably because of the lack of sustained inhibition,
the short tone rate-level functions usually better revealed
nonmonotonic behavior, and they have the added benefit of providing
PSTHs at many SPLs (rather than a single PSTH at a fixed suprathreshold
SPL).
Responses to notched noise
The pure tone and noise responses described so far show that some
cells in DCN of the chloralose-anesthetized cat have type IV responses
similar to those in the decerebrate animal but that there is a tendency
at the population level for less nonmonotonic behavior in response to
tones. An additional property of type IV cells in the decerebrate cat
(Spirou and Young, 1991; Nelken and Young, 1994) is an exquisite
sensitivity to spectral features of broadband stimuli. As a further
test of response similarity in the two preparations, I occasionally
tested type III and IV cells for this sensitivity. A series of
band-reject noise stimuli were constructed with a stopband of
increasing width, always arithmetically centered on the CF. Responses
to a complete series of notch widths were obtained in six cells. The
type IV unit illustrated in Figure 10A showed the
largest effect seen. Similar to the data of Nelken and Young (1994),
the cell was inhibited by a CF tone, excited by broadband noise, and
progressively less driven as the stopband in the noise widened.
However, in contrast to the data reported by Nelken and Young (1994),
none of the notched-noise stimuli resulted in the profound inhibition
seen with tone bursts. The cell in Figure 10B was
robustly driven by all wideband stimuli, even at high notch widths. The
responses of four other cells recorded in DCN (two type III and two
type IV) were intermediate between those shown in Figure 10.
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Figure 10.
Responses of type IV cells, recorded in DAS of
one animal, to CF tones and broadband and notched noise. Noise
bandwidth was 40 kHz, and notch bandwidth was varied as indicated by
the symbol caption, with a nominal depth of 100 dB and
slopes of several thousand dB/octave. CFs were 29 kHz
(A) and 9 kHz (B). For
A, an attenuator setting of 100 dB corresponds to a
noise level of 87 dB.
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DISCUSSION |
The only previous reports of DAS physiology were of a preliminary
nature (Kiang et al., 1973; Adams, 1976) and established that PSTH
patterns were predominantly of the Pauser, Buildup, and Chopper
variety. Young (1980) stimulated the DAS electrically and found that
antidromically activated DCN cells gave predominantly type IV
responses. On the basis of this evidence, it was proposed that these
responses are associated with DCN projection neurons, whereas type II
responses are derived from interneurons such as tuberculoventral cells
(Wickesberg and Oertel, 1988). Consistent with that proposal, the
present results show that DAS responses are predominantly type III+IV
and Oc, to the exclusion of type II.
Neither the response map scheme nor the PSTH classification scheme is
strictly quantitative. Both rely on prototypical response features and
are fuzzy at the response class borders (see Figs. 4, 5). Studies of
the relationship between the two schemes (Shofner and Young, 1985;
Stabler et al., 1996; Gdowski and Voigt, 1997) emphasized their
incompatibility, and often the two response measures (PSTH patterns and
average rate) are treated as being independent. PSTH patterns can
change with frequency, SPL, and other stimulus parameters (Godfrey et
al., 1975b; Shofner and Young, 1985; Rhode and Smith, 1986b; Stabler et
al., 1996), and, equivalently, response maps constructed over small
consecutive integration windows vary over time (Kaltenbach et al.,
1989). However, these dependencies show that the two schemes are
mutually constraining rather than incompatible. For example, at the
risk of stating the obvious, PSTHs obtained at frequency-SPL
combinations in an inhibitory area of the response map must also be
dominated by inhibition.
The aim of classification in the present experiments was to
derive the minimal number of DCN-DAS classes that plausibly correspond to cell types differing in morphological and projectional features and
was guided by the following assessment of the relevant literature. First, difficulties in classification promote the tendency to elaborate
the number of (sub)types (seven response map classes in Davis et al.,
1996; 17 PSTH classes in Gdowski and Voigt, 1997), although only a
small number of functional elements are needed to account for DCN
responses in models (Arle and Kim, 1991; Nelken and Young, 1994; Reed
and Blum, 1995; Davis et al., 1996). Consequently, response classes do
not carry equal weight: some classes are devices to accommodate
classification difficulties (e.g., types I/III, IV-T in the response
map scheme). Second, recent studies have based classification on
rate-level functions for CF tones and broadband noise rather than on
the complete response map (Nelken and Young, 1994; Stabler et al.,
1996). Third, there is substantial evidence for structure-function
associations from in vivo intracellular labeling studies in
DCN and DAS (Rhode et al., 1983a,b; Smith and Rhode, 1989; Joris et
al., 1992; Joris and Smith, 1995), albeit that this evidence is
incomplete in different ways for different cell types (classification,
anesthesia, number of cells), which clouds the relationship with the
associations proposed on the basis of decerebrate studies.
On the basis of the preceding observations and the present results, a
plausible and parsimonious classification scheme can be derived that
uses features of both schemes to a varying degree for different cell
types. For a first class of responses, type II, the cardinal features
are a poor response to broadband noise and a robust response to tones:
the PSTH is highly variable and is not a reliable classifier (Fig. 5).
These cells have low SRs and the rate-level function to tones usually
has an accelerating negative slope at high SPLs. With the exception of
lower maximal rates to tones (compare Fig. 9A with Fig.
6A in Young and Voigt, 1982), these features are
consistent with those recognized by Young and coworkers (Young and
Brownell, 1976; Young, 1980; Young and Voigt, 1982; Shofner and Young,
1985).
The cardinal features of a second class of responses are almost
opposite: a very high response to noise and a response to tones that
shows an accelerating positive slope at high SPLs (Fig. 6). This class
was first recognized on the basis of the PSTH pattern (On-type L or
Oc) and is associated with multipolar cells in the nerve root region and deep DCN (Rhode and Smith, 1986a; Smith and
Rhode, 1989; Godfrey et al., 1975a,b; Joris et al., 1992; Palmer et
al., 1996). The response map classification of these cells is
indistinct (type III or I/III, i.e., excited by tones and broadband
noise and lacking sufficient SR to test for inhibitory sidebands), but
these cells do not constitute a high proportion of DCN recordings
because of their anatomical location.
Regarding the final group, types III and IV, the present results
suggest an interpretation that diverges from previous studies in the
decerebrate cat. Definition of the type III class is too general to
warrant homogeneity. It does not discriminate among several CN cell
types, the distinctive PSTH patterns and morphologies of which have
been well documented (e.g., multipolar cells, stellate cells, globular
bushy cells, and some fusiform cells, can all be type III or I/III). On
the other hand, the type III and IV cells described in this study were
found in approximately equal proportions in DCN (III, 58%; IV, 42%;
n = 110) and DAS (III, 54%; IV, 46%;
n = 39), and with few exceptions they had PSTHs along
the spectrum Pauser-Buildup/ON-I. This suggests that despite the
nonspecific definition of the type III response, type III+IV responses
in DCN and DAS are derived predominantly from projection neurons and
not from DCN interneurons. Second, the responses are not suggestive of
a type III-type IV dichotomy. Rather, these two classes appear to be
the opposite poles of a continuum. To tones, there is a continuum of
degrees of inhibition and PSTH shapes, but with a stereotyped
dependency on SPL (Fig. 7). Not the shape of a single PSTH at a fixed
suprathreshold level, but the dynamics of the PSTH changes with
level, and its reflection in the rate-level function,
distinguishes these cells from type II or Oc cells. To
broadband noise, there is a sizeable fraction of type III+IV cells
(~8-19% depending on criteria) that had a low or even inhibitory
response to broadband noise. Such responses are also apparent in
initial studies of the decerebrate cat as well as in more recent
publications in cat and other species (Young and Brownell, 1976; Kim et
al., 1990; Nelken and Young, 1994; Davis et al., 1996; Gdowski and
Voigt, 1997). Thus from the present results it appears that projection
cells are more varied in their responses to tones and noise than is
implied by the prototypical description for the decerebrate cat, and
that there is little rationale for maintaining the type III-type IV
distinction rather than using a single class III+IV. This is congruent
with data from other anesthetized and even unanesthetized preparations
(Rhode and Smith, 1986b; Rhode and Kettner, 1987; Stabler et al.,
1996).
It is not entirely clear how appropriate this characterization may be
for the decerebrate animal. The type III-type IV dichotomy in that
preparation is based largely on co-segregation of response properties
and does not clearly map onto an interneuron-projection neuron
dichotomy. Antidromic stimulation of the DAS (Young, 1980) indicates
that at least some type III cells project out of the DCN, but the exact
proportion is difficult to estimate because that study predates the
more recent type II-type III subdivision. On the one hand, there have
been no labeling studies in the decerebrate animal to refute the claim
that a significant portion of DCN projection neurons have responses
other than type IV. On the other hand, there is undeniably a difference
in response class distribution between decerebrate and anesthetized
preparations, as also observed in this study, although it is not
obvious which of those preparations is the better model for the awake
state. Thus, it is possible that the continuity of the type III-type
IV properties as emphasized here is an anesthesia artifact. A
straightforward means to resolve this issue, short of intracellular
labeling studies in decerebrate animals, is to record from DAS in the
decerebrate animal.
An intriguing result is the stronger response to noise in cells
strongly inhibited by tones (Fig. 9C) compared with cells only weakly inhibited by tones (Fig. 9B). According to
Nelken and Young (1994), type IV responses to tones and noise reflect different processes: the nonmonotonic response to tones is derived from
inhibition by type II interneurons, whereas the response to broadband
noise is limited by wideband inhibitors, presumably Ocs.
Generalizing to the III+IV class, their model predicts that cells with
poor tonal responses receive weak Oc inputs but strong type
II inputs, and the reverse for cells with strong tonal responses, perhaps as a consequence of the position of the fusiform cell relative
to the axonal arbors of type II cells below the fusiform cell layer and
the more deeply located Oc cells. Interestingly, in line
with this possibility is the observation by Rhode and Smith (1986b)
that cells with Pauser PSTH are generally located deeper than cells
with Buildup PSTH, which are more poorly driven by tones.
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FOOTNOTES |
Received Jan. 15, 1998; revised March 3, 1998; accepted March 4, 1998.
This work was supported by grants from National Institutes of Health
(NS-10414), Fulbright, NATO, National Institutes of Health Fogarty
International Center, and the Coleman Fund (at the University of
California at San Francisco), and by the National Institute on Deafness
and Other Communication Disorders Grant DC-00116 and National Science
Foundation Grant BNS-8901993 (at the University of Wisconsin-Madison).
I thank M. M. Merzenich, C. E. Schreiner, P. H. Smith,
R. L. Snyder, and T. C. T. Yin for their encouragement and support; C. E. Schreiner and R. L. Snyder for
participation in initial experiments; and I. Nelken and P. H. Smith for criticisms on this manuscript. I am grateful for the
technical support of R. Kochhar (software) and G. Meulemans
(photography).
Correspondence should be addressed to Philip X. Joris, Division of
Neurophysiology, K. U. Leuven, Campus Gasthuisberg, B-3000 Leuven,
Belgium.
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Abstract
Introduction
