Speech Communication 41 (2003) 135–149
www.elsevier.com/locate/specom
Temporal coding of the pitch of complex sounds by presumed
multipolar cells in the ventral cochlear nucleus
Ian M. Winter
a
a,*
, Alan R. Palmer
a,b
, Lutz Wiegrebe
a,c
, Roy D. Patterson
a
Department of Physiology, Centre for the Neural Basis of Hearing, Downing Street, Cambridge CB2 3EG, UK
b
MRC Institute of Hearing Research, University Park, Nottingham University, Nottingham NG7 2RD, UK
c
Zoologisches Institut der Universit€at, M€unchen, Luisenstrasse 14, 80333 M€unchen, Germany
Abstract
Extensive studies of the encoding of fundamental frequency (f0 ) in the auditory nerve indicate that f0 can be represented by either the timing of the neuronal discharges or the mean discharge rate as a function of characteristic
frequency. It is therefore of considerable interest to examine what happens to this information at the next level of the
auditory pathway, the cochlear nucleus. Both physiologically and anatomically the cochlear nucleus is considerably
more heterogenous than the auditory nerve. There are two main cell types in the ventral division of the cochlear nucleus; bushy and multipolar. Bushy cells give rise to primary-like responses whereas multipolar cells may be characterised by either onset or chopper type responses. Physiological studies have suggested that onset and chopper units
may be good at representing the f0 of complex sounds in their temporal discharge properties. However, in these studies
the pitch-producing sounds were usually characterised by highly modulated envelopes and it was not possible to tell if
the units were simply responding to the modulation or the temporal fine structure. In this paper we examine the ability
of onset and chopper units to encode the f0 of complex sounds when the modulation cue has been greatly reduced.
These stimuli were steady-state vowels in the presence of background noise, and iterated rippled noise (IRN). The
response of onset units to the vowel f0 in the presence of background noise was varied but many still maintained a
strong response. In contrast, the majority of chopper units showed a greater reduction in their response to vowel f0 in
the presence of background noise. In keeping with the vowel study, the responses of both types of unit to the delay of
the IRN was reduced in comparison with their response to more highly modulated stimuli. Increasing anatomical,
pharmacological and physiological evidence would seem to argue against onset units playing a direct role in pitch
perception. However, some units, identified as sustained choppers, may be able to represent the pitch of complex sounds
in their temporal discharges.
Ó 2002 Elsevier Science B.V. All rights reserved.
Keywords: Fundamental frequency; Autocorrelation; Iterated rippled noise; Onset units; Chopper units
1. Introduction
The fundamental frequency (f0 ) of complex
sounds is closely related to their perceived pitch.
*
Corresponding author.
The f0 may be signaled to the brain (by the auditory nerve) in either a rate-place or temporal-place
code and the responses of cells in the cochlear
nucleus (an obligatory synapse for the auditory
nerve) are of considerable interest in determining
which of these codes is important. The cochlear
nucleus is classically subdivided into three parts;
0167-6393/02/$ - see front matter Ó 2002 Elsevier Science B.V. All rights reserved.
doi:10.1016/S0167-6393(02)00098-5
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I.M. Winter et al. / Speech Communication 41 (2003) 135–149
anteroventral, posteroventral and dorsal. In this
paper we concentrate on the responses of single
units in the antero- and postero-ventral parts, together known as the ventral cochlear nucleus
(VCN). The VCN is characterised by three physiological response types; primary-like (PL), chopper and onset (see Fig. 2 for examples). Each unit
type is assumed to represent a separate, parallel
processing unit, within the VCN. PL units are
named for the similarity of their responses to those
of their primary afferent input from the auditory
nerve. They are recorded from bushy cells, mainly
in the anteroventral part of the nucleus (Rhode
et al., 1983). Both chopper and onset units are
believed to be recorded from multipolar cells distributed throughout the VCN (e.g. Smith and
Rhode, 1989). In keeping with their anatomical
heterogeneity, these cell types give rise to different
physiological responses.
Saturation does not limit the temporal encoding
of pitch at high sound levels in the auditory nerve.
Young and Sachs (1979) showed that the temporal
encoding of speech sounds remained stable well
beyond the sound level where the fiberÕs rate response saturated. The same is true, to some extent,
for the encoding of amplitude modulation in the
auditory nerve (Frisina et al., 1996). For a temporal code based on inter-spike intervals, however,
the monotonically rising rate-level functions of
auditory-nerve fibers represent a further problem.
An increase in discharge rate is accompanied by
shorter inter-spike intervals, thus interfering with
an analysis of these intervals in terms of the periodicity associated with the pitch sensation. One
possible way to overcome this problem is the
processing of higher-order inter-spike intervals;
that is the interval not only between successive
spikes but also non-successive spikes, an operation
equivalent to autocorrelation of the spike train
(Carianni and Delgutte, 1996a,b; Shofner, 1991,
1999). Stimulus periodicity encoded in first-order
inter-spike intervals at low stimulus levels may be
preserved in higher-order inter-spike intervals at
higher sound levels. This was confirmed experimentally by Carianni and Delgutte (1996a,b)
who found a temporal neural correlate of pitch in
the cat auditory nerve; they showed that pitch is
well represented in an all-order inter-spike inter-
val analysis whereas a first-order analysis was
susceptible to changes in sound level. This conclusion cannot readily be extended to the cochlear
nucleus.
In the cochlear nucleus, the neural information
provided by the auditory nerve is subjected to
different types of temporal and spectral processing––the latter through the interaction of units
with different best frequencies (BFs). Onset units
accentuate the degree of amplitude modulation of
an acoustic stimulus (e.g. Kim et al., 1986; Kim
and Leonard, 1988; Rhode and Greenberg, 1994).
Chopper units also accentuate amplitude modulation, but they do so only for a limited range of
modulation frequencies in the vicinity of their
chopping frequency. Thus, chopper units have
modulation transfer functions with a band-pass
characteristic, particularly at high sound levels
(Kim et al., 1990; Frisina et al., 1990). This distinguishes chopper units from PL units or auditory-nerve fibers which typically show modulation
transfer functions with a low-pass characteristic
and a relatively small degree of temporal synchronization to a sinusoidal modulator.
A number of studies suggest that onset units in
the cochlear nucleus are able to represent the pitch
of a wide range of stimuli in their temporal discharge pattern. The onset–chopper (OC, Rhode
and Smith, 1986; Winter and Palmer, 1995) subgroup of onset units is characterised by a dynamic
range much greater than that of individual auditory-nerve fibres; the range can be as much as
80–90 dB. However, OC units typically have a
bandwidth of three octaves and it may even be as
wide as six octaves (Jiang et al., 1996; Palmer et al.,
1996). Thus, although these neurons may be able
to represent pitch over a wide range of levels they
appear not to have sufficient frequency selectivity
to represent the harmonic spectrum.
In this paper we use parametric designs to
measure the response of these putative pitch encoding units in a systematic way. In the first set of
experiments, we examine the ability of chopper
and onset units to encode the f0 of steady-state
vowels in background noise. The noise levels used
do not affect the perception of the vowel pitch or
its identification. We show that while all chopper
units show a reduction in their response to the f0 ,
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
many onset units maintain a good representation
of f0 even in the presence of background noise.
In the second set of experiments we examine
the ability of onset and chopper units to represent the delay of iterated rippled noise (IRN). For
most pitch-producing sounds, such as steady-state
vowels, there is a strong correlation between the
presence of harmonically spaced peaks in the internal tonotopic representation of the sound, and
the presence of peaks in the interval histogram or
autocorrelogram at the period of the sound. For
such sounds it is difficult to say whether a spectral
or temporal auditory mechanism is more likely to
be the basis of the pitch. IRN enables the decoupling of pitch from the peaks in the internal tonotopic representation; when highpass filtered, to
remove resolved harmonics, the IRN produces a
tonotopic rate representation very similar to that
of the original noise even though it produces a
pitch (Patterson et al., 1996). It has been argued
that the pitch arises from the fine-grain temporal
regularity which is well represented in the autocorrelogram. Consequently, this stimulus has
been used in both perceptual and physiological
experiments to study the processing of temporal fine structure in the auditory system (e.g.
Shofner, 1991, 1999; Wiegrebe and Patterson,
1999; Yost, 1996a,b; Yost et al., 1996; Krumbholz
et al., 2001).
Rippled noise (RN) is produced from white
noise (WN) by delaying a copy of the noise by d
ms and adding the delayed noise back to the
original. IRN is produced by repeating the delay
and add process n times, and it is referred to as
IRN(d; n). The delay-and-add process introduces
temporal regularity into the fine structure of the
noise (Fig. 1A) which is revealed by peaks in the
autocorrelation function of the waveform (Fig.
1C). It also introduces a ÔrippleÕ into the long-term
power spectrum of the waveform (Fig. 1B). Note,
however, that the resolution of the spectral analysis performed in the cochlea is inversely related to
frequency and so high frequency peaks merge in
the internal tonotopic representation. Simulations
of the processing of IRN (Griffiths et al., 1998) do
not show resolved peaks above about the sixth
harmonic and it has been argued (Yost et al., 1996)
that the pitch of IRN is best represented by the
137
Fig. 1. An illustration of IRN. (A) The IRN waveform when
the delay is 8 ms, the gain is unity and the number of iterations
is 16. The resulting magnitude spectrum (B) shows peaks at
integer multiples of 125 Hz which is the reciprocal of the 8 ms
delay used to generate the IRN. Note that the complete stimulus is not shown. The normalized autocorrelation function (C)
shows peaks at integer multiples of the 8 ms correlation lag. The
position and height of the first peak (apart from the peak at the
zero lag) in the autocorrelation function, h1 , has been used to
model the pitch and pitch strength of IRN. Note that the height
of h1 is slightly less than unity reflecting the quasi-periodicity of
IRN stimuli.
position of the first peak in the autocorrelation of
the waveform (h1 , Fig. 1C).
Analyses of the first-order inter-spike interval
histograms (ISIHs) revealed that units often showed
a maximal response to a specific IRN delay (best
period), but also responded well for a limited range
of delays (or pitches) around this best period.
We refer to this preference in first-order interval
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I.M. Winter et al. / Speech Communication 41 (2003) 135–149
statistics as Ôperiodicity tuningÕ. The range of best
periods varied from 3.75 to 13 ms (between 77 and
267 Hz) for OC units and from 2.25 to 10.8 ms
(between 93 and 444 Hz) for sustained chopper
(CS) units. The range of best periods for transient
chopper (CT) units was 1.4–8.8 ms (113–714 Hz).
However, increasing anatomical, physiological and
pharmacological evidence suggests that if multipolar cells are to directly contribute to the encoding
of the pitch of complex sounds then those units
classified as CSs are the most promising candidates.
2. Methods
A detailed description of the stimulus presentation and response acquisition procedures for the
vowel study can be found in (Winter and Palmer,
1995) and for the IRN study in (Wiegrebe and
Winter, 2001) and so we shall only describe them
in brief here. All experiments were carried out
using anaesthetised, pigmented, post-weaned, guinea pigs. The procedures used in this paper were
approved by the United Kingdom Home Office
Act (1986) by the issue of a project and a personal
license to the first and second authors.
chronization index (SI) was then obtained by
dividing the magnitude of the f0 component of
the Fourier transform (100 Hz) of these histograms by the magnitude at 0 Hz.
IRN was generated by delaying and adding
WN. In the majority of cases we used the ‘‘add
same’’ configuration as defined in (Yost, 1996a,b)
with a gain of 1 and 16 iterations. For convenience, we use f0 to designate the reciprocal of the
delay of an IRN, although the waveform is not
periodic. The f0 of the IRN ranged from 31.25 to
1000 Hz in half-octave steps. Stimuli were generated digitally using the Tucker–Davis System II
DSP Board at a sampling rate of 20 kHz. The
stimulus duration was 409.6 ms including 10 ms
cos2 ramps. Each stimulus was presented 25 times
at a rate of one per second. Unless otherwise stated, the stimuli were refreshed for every presentation. Despite the stochastic nature of IRN,
different stimulus waveforms share the same form
of temporal regularity. The stimulus energy was
kept constant irrespective of f0 . As a control we
also collected responses to WN at the same sampling rate and energy level.
2.2. Analyses
2.1. Complex stimuli
The vowel sound /a/ was produced using the
Klatt software cascade synthesizer (Klatt, 1980).
Details of formant frequencies and bandwidths are
shown in Table 1. The stimuli were presented in
pairs; each pair consisted of a vowel alone (120 ms
duration), a silent interval of 240 ms and then the
vowel in WN (3 or 10 dB s/n, 120 ms duration).
These vowel pairs were presented at a rate of one
per 740 ms at approximately 80 dB SPL. To
quantify the responses to f0 , we first constructed
period histograms from the spike times. The syn-
Recordings from single units were made using
tungsten-in-glass microelectrodes. Wideband noise
was used to search for single units. Upon isolation
of a single unit, estimates of BF and threshold
were obtained using audio–visual criteria. The
spontaneous discharge was measured over a 10-s
period. Single units were classified by their discharge regularity (Young et al., 1985), and by the
shape of their temporal discharge pattern (see Fig.
1) as revealed by their peri-stimulus time histogram (PSTH) in response to suprathreshold BF
tone bursts. To identify a unit as an onset unit, we
Table 1
Fundamental frequency (Hz) and frequency (Freq.) and bandwidth (BW) in Hz of formants (F1–F3) of the synthetic vowel /a/
Vowel
/a/
f0
F1
Freq.
Freq.
BW
Freq.
F2
BW
Freq.
F3
BW
100
730
90
1090
110
2440
170
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
used the classification scheme of Winter and Palmer (1995).
PSTHs were generated using the responses to
250 pure tone bursts; the signal duration was 50
ms and the frequency was the unitÕs BF. The rise–
fall time was 1 ms (cos2 gate) and the repetition
rate was 4 s1 . The starting phase of each tone
burst was varied randomly to reduce the influence
of phase-locked discharges on the shape of the
PSTH for units with low BFs. Spikes were timed
with 1 ls resolution with a Tucker–Davis Technologies event timer (ET1). Typically, two PSTHs
were collected at sound levels of 20 dB and either
40 or 50 dB suprathreshold. All single tone PSTHs
shown in this paper include a 20 ms delay before
the onset of the stimulus.
We have analysed the responses of single units
in terms of their first-order and all-order interval
statistics. The all-order interval statistic is analogous to the autocorrelation of the spike train. In
the IRN study, for the majority of cases, we also
presented WN to the unit at the same sampling
rate and sound level. A similar discharge rate was
elicited for both WN and IRN stimuli except
where the BF of the unit was in a spectral dip
between low-frequency spectral peaks in the IRN
spectrum. The strength of the pitch associated with
IRN increases monotonically with the number of
iterations (see Fig. 6 of this study and Yost,
1996a).
In order to quantify the relationship between
the first-order ISI response to WN and the firstorder ISI response to IRN (see Fig. 8), we fitted a
gamma distribution (Eq. (1)) to the first-order ISI
distribution of the WN (e.g. Fig. 7A)
gðtÞ ¼ atn1 e2pbt
ð1Þ
The best-fitting gamma distribution was then
subtracted from the first-order ISI distribution in
response to the IRN. For each IRN delay the
difference between the number of intervals at the
IRN delay in the two distributions was termed
the interval enhancement. The interval enhancement distribution was then itself fitted with a
gamma function (see Fig. 7B). The interval enhancement measure emphasises the fact that our
reference condition (WN) does not produce a pitch
139
sensation and that any changes in the ISI statistics
are due to the quasi-periodicity present in the IRN
stimuli.
3. Results
Single units were classified by the shape of their
PSTH and their discharge regularity (Bourk, 1976;
Young et al., 1985; Blackburn and Sachs, 1989;
Rhode and Smith, 1986; Winter and Palmer,
1990). For comparison purposes, in Fig. 2 we show
the responses of five unit types commonly recorded from the VCN. Four of these are thought
to be recorded from multipolar cells while the fifth,
PL is thought to be recorded from bushy cells. The
PL unit has a high probability of discharge just
following the stimulus onset followed by an exponential decline to a steady-state rate. The ISIH
also has an exponential decline and is multipeaked
which is indicative of the unitÕs ability to phase
lock well to low-frequency sounds (Bourk, 1976;
Rhode and Smith, 1986; Blackburn and Sachs,
1989; Winter and Palmer, 1990). The regularity
analysis reveals that the unit is characterised by
irregular firing (coefficient of variation; CV > 0:5).
In contrast the CS unit is characterised by a sequence of regularly spaced peaks in the PSTH that
are unrelated to stimulus frequency. The ISIH has
a narrow peak at the chopping period and the
regularity analysis confirms the regularity of the
sustained discharge (the mean and standard deviation remain constant over the analysis period).
The constant regularity, with a CV less than 0.35,
identifies this unit as a CS (Young et al., 1985).
When the PSTH is characterised by regular peaks
but the CV is greater than 0.35 the unit is classified
as a CT as illustrated in the bottom row of Fig.
2The figure also shows the responses of two onset
units to a 50 dB suprathreshold tone burst at the
unitÕs BF (OC and OL). Onset units are characterised by a very high probability of discharge at
stimulus onset, often followed by a pause and then
a low level of discharge. The OC unit had a reasonably high rate of steady-state discharge which
enabled the calculation of the unitÕs discharge
regularity. The CV was 0.32 which placed it in
between the regular dischargers and the irregular
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I.M. Winter et al. / Speech Communication 41 (2003) 135–149
Fig. 2. Examples of the unit types found in the VCN (see text). All temporal discharge patterns were obtained in response to 50 ms
suprathreshold BF tone bursts, 20 dB above threshold at the unitÕs BF. The solid line beneath the top-left panel indicates the temporal
position of the tone burst. The second column shows the first-order ISIHs. The third column shows a measure of a unitÕs discharge
regularity, with the solid lines representing the mean interval and dotted lines the standard deviation of the intervals. Note that a low
coefficient of variation (CV < 0:5) indicates a unit with a regular discharge pattern. The PSTHs for the OC and OL units were obtained
in response to a 50 dB suprathreshold tone burst.
dischargers (cf. Young et al., 1985; Winter and
Palmer, 1995). The narrow peaks in the temporal
adaptation pattern and also in the first-order ISIH
pattern identify this unit as an OC. The OL unit is
similar in many of its response properties to the
OC unit but is characterised by only one peak at
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
response onset (e.g. Rhode and Smith, 1986;
Winter and Palmer, 1995).
3.1. Response of multipolar cells to vowels in quiet
and in noise
Both onset and chopper responses appear to
be characteristic of multipolar cells in the anteroventral and posteroventral cochlear nucleus.
However, consistent with their very different responses to pure tones, these response types respond quite differently to vowels and vowels in
noise. Fig. 3 shows period histograms (over two
periods of the f0 ) of the responses of an OC unit
(left column) and a CS unit (right column) to the
vowel /a/. The BFs are different which probably
contributes to the different details of the responses.
The response of the OC unit (Fig. 3A) is well
locked to the f0 in quiet and its locking to f0 is
141
little diminished by the addition of background
noise, be it 10 dB s/n (Fig. 3C) or 3 dB s/n (Fig.
3E). In contrast, while the response of the CS unit
in quiet is well locked to the f0 (Fig. 3B), it is severely degraded even by the addition of the weaker
noise. Further increasing the noise level did not
further degrade the locking of the CS unit to the
f0 . Note that the BF of the CS unit shown in this
figure is 3.57 kHz which is well away from the
nearest formant of /a/ and in the region where
auditory-nerve fibres show good modulation to the
f0 . The OC unit has a BF of 1.31 kHz, which is
close to the first formant (F1) of /a/, where auditory-nerve fibre responses would usually be
strongly locked to F1 and hence the response to f0
would be relatively weak.
Fig. 4 shows the responses of populations of
onset and chopper units to the vowels in quiet and
in noise. No attempt has been made to subdivide
Fig. 3. Responses from an onset (BF ¼ 1:31 kHz) and chopper unit (BF ¼ 3:57 kHz) to the steady-state vowel /a/ in quiet and two
levels of background noise. Signal-to-noise ratios are indicated on the right-hand side of the figure. Two consecutive periods of the f0
are shown in the histogram. Even when the s/n ratio is 3 dB, the onset unit still provides a good representation of the f0 in terms of its
synchronized discharges.
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I.M. Winter et al. / Speech Communication 41 (2003) 135–149
Fig. 4. Degree of modulation of period histograms at f0 as a function of unit BF, as determined by the SI, for the steady-state vowel /a/.
The bottom row shows the responses from a population of onset units in quiet; the s/n was 10 dB. The top row is in the same format for a
population of chopper units. Note that the SI for chopper units at 10 dB s/n dropped below 0.5 whereas many onset units had SIs above
this value at the same s/n ratio.
the populations of onset and chopper units. As
in the auditory nerve (Miller and Sachs, 1984;
Palmer, 1990), the response to a vowel in quiet, in
terms of locking to f0 , tends to occur in the frequency regions between formants. The addition of
10 dB s/n noise reduces the locking to the f0 of
virtually all of the units in our chopper population
(as it does in the auditory nerve: Miller and Sachs,
1984), but the locking still remains significant in
most cases. For the onset population several features are noteworthy. First, the locking of the
onset units is generally stronger (higher SI values
reaching close to 1.0) than in the chopper population (or in the nerve fibre population; Miller and
Sachs, 1984; Palmer, 1990). Second, the spread of
locking in the onset population seems to be more
extensive than in the auditory nerve (i.e. not so
much restricted by the regions of good response
between the formants). Third, the background
noise at 10 dB s/n, while reducing the locking to f0 ,
still leaves the vast majority of onset units significantly locked to the f0 (Fig. 4C and D). Note that
in background noise, the SI to f0 is always below
0.5 for chopper units, whereas for the onset population, the SI of many units remains above 0.5. It
is clear that despite the relatively high levels of
background noise both types of multipolar cell can
still signal the f0 in the timing of their spikes.
3.2. Responses of multipolar cells to iterated rippled
noise
The responses of an OC unit to IRN as a
function of the number of iterations are shown
in Fig. 5. The responses are plotted as first- and
all-order ISIHs, in the left and right columns, re-
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
143
Fig. 5. The effect of increasing number of iterations at a delay near the unitÕs best periodicity. The unit was an OC. The left-hand
column shows the first-order ISIH in response to an IRN with a gain of 1, delay of 11.2 ms. The top row shows the response to equal
energy WN. The right column shows the all-order ISIH in response to the same stimuli.
spectively. The top row shows the response to
equal energy WN. The delay of the IRN was 11.2
ms and, as the number of iterations was increased,
a clear peak emerged in both the first- and allorder ISI at 11.2 ms. We describe this increase as
Ôinterval enhancementÕ as there is an increase in the
number of intervals at the delay in comparison
with the response to the WN stimulus. Thus, the
IRN delay (and hence the pitch) is well represented
in the temporal discharges of this unit. It should be
noted that this type of response was delay dependent, with the unit showing a preference for some
delays over others; in this respect the unit could be
said to be tuned to the delay of IRN. We refer to
the delay at the peak of this tuning as a unitÕs best
periodicity (see Fig. 7 for a further example of this
delay tuning).
It has been shown psychophysically (Yost,
1996b) that the pitch strength of IRN grows
monotonically with the number of iterations and
that the pitch strength grows as a function of 10h1 .
In Fig. 6 we show the growth of the height of h1 as
well as the growth of 10h1 . Also shown in Fig. 6 is
the growth in the number of intervals at the delay
of IRN (11.2 ms) as a function of the number of
iterations for both the first- and all-order analyses.
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I.M. Winter et al. / Speech Communication 41 (2003) 135–149
Fig. 6. A comparison of the responses of the OC unit shown in
Fig. 5 with the growth of h1 (j) and 10h1 . It is claimed that the
pitch strength of IRN follows this latter function (d). The
number of intervals at the delay (11.2 ms) is plotted as a
function of number of iterations for both the first-order ( ) and
the all-order (N) ISIs. The ordinate represents the magnitude of
h1 or 10h1 measured from the autocorrelation of the stimulus for
the lower two plots while for the upper plots the ordinate
represents the number of intervals per presentation.
Fig. 7. Estimation of the peak in the first-order ISIH for WN
and the peak in the interval enhancement. (A) An example of a
WN first-order ISIH and the fitted gamma function for an OC
unit. The BF was 3.1 kHz. The interval enhancement is shown
in (B) by the solid line and asterisks. The best-fitting gamma
function for the interval enhancement is shown by the line. The
peaks, as estimated from the maximum height in the gamma
functions are shown on the figures.
Consistent with the psychophysics, we also observe monotonic growth in the number of intervals
at the IRN delay.
3.3. Comparison of the responses to broadband noise
and IRN
To examine the relationship between the response to WN and the response to IRN we have
chosen to fit the first-order ISIH in response to
WN with a gamma function and then compare this
fit with a gamma function fitted to the interval
enhancement plot (see Section 2). An example of
the results of the fitting procedure is shown in Fig.
7 for a unit classified as OC. The positions of the
peak fitted to the noise ISIH distribution and the
peak fitted to the IRN interval enhancement plot
are, in this example, similar. Fig. 8 shows the relationship between the peak of the gamma fit to
the IRN and the peak of the gamma fit to the WN
for a population of units believed to be multipolar
cells. Units classified as onset exhibit peaks between 3 and 13 ms. Of these 23 onset units, 16 were
Fig. 8. Relationship between the peak of first-order ISIH to
WN and the peak of the interval enhancement plot for single
units. The peak of the first-order ISIH in response to WN is
plotted on the abscissa. The peak was estimated from a gamma
fit to the ISIH. The peak of the gamma fit to the interval enhancement plot in response to IRN is plotted on the ordinate.
The dotted line indicates equality for the two values. The correlation between the two measures is greatest for OC and CS
units (see Table 2).
classified as OC. Units classified as CS show
preferences for delays between 3 and 10.8 ms.
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
Table 2
Mean and standard deviation of the peak in the first-order ISIH
to WN and the peak in the interval enhancement plot
White noise (ms)
Interval enhancement (ms)
Correlation
CT
CS
Onset
2.42 1.08
3.53 2.02
4.45 1.83
4.88 2.1
6.55 2.36
7.05 2.61
0.44
0.72
0.81
*
Significant difference between peak in interval enhancement
and peak in WN (one-tailed studentÕs t-test) at p < 0:05.
Units classified as CT show, on average, interval
enhancement at shorter delays than CS units. It
should be noted (Table 2) that there was a significant difference between the peak in response to
WN and the peak in response to IRN for CT units.
There was a tendency for the points to lie above
the line of unity slope indicating that the maximum enhancement to the IRN stimulus is at lower
frequencies (longer delays) than the peak in the
first-order ISIH. There was no significant difference between the peak in the response to WN and
the peak in response to IRN for the CS and OC
unit types. The correlation between the WN and
IRN peak responses for the three unit types is
shown in Table 2. There is a weak correlation for
CT units and there are strong correlations for the
CS and OC unit types.
4. Discussion
In this study we have shown that units in the
VCN, presumed to be multipolar cells, respond in
several ways that are consistent with a role in the
representation of the pitch of complex sounds.
Onset-responding multipolar cells appear to signal
the f0 of vowel sounds better than choppers, and
can do so even in moderate levels of background
noise. Such levels of background noise do not affect the identification or the timbre of the vowel
sounds. However, it should also be noted that the
best responses to the f0 were obtained from units
with BFs above the third formant frequency, a
frequency where the harmonics would be unresolved. It is unlikely that this frequency region is
crucial in conveying the pitch of steady-state
vowels (Houtsma and Smurzynski, 1990). Both
145
types of multipolar cell can enhance the representation of the delay of iterated ripple noise in their
ISIHs; the enhancement was dependent on the
magnitude of the delay. Transient chopper units
seemed to enhance the short delays more; sustained and onset choppers seemed to enhance the
longer delays more. The implications of these
findings for the neural encoding of the pitch of
complex sounds are discussed below.
4.1. Onset units and pitch
Onset units have been subdivided into at least
three physiological response types. However, we
have only been able to record from two of these in
this study. The discussion that follows relates primarily to OC units but might also apply to OL
units. The third type, onset-I (OI) have also been
implicated in the coding of pitch (see below for a
brief discussion). OC units encode the pitch of
voiced speech sounds with remarkable fidelity and
may respond to the ambiguous pitches of inharmonic complexes (Kim et al., 1986; Palmer and
Winter, 1992, 1993; Rhode, 1994, 1995). They also
respond to amplitude modulated noise in a manner that is similar to their response to 200% amplitude modulated tones (Rhode, 1994). As we
have shown here, their responses to f0 survive
moderate levels of background noise. In order to
explain the remarkable precision of spike timing in
these units several authors have speculated that a
form of across-frequency coincidence detection
must be employed by these units (Rhode and
Smith, 1986; Kim et al., 1986; Palmer and Winter,
1996). The wide bandwidth of OC units is certainly
beneficial for the encoding of envelope periodicity
(e.g. steady-state vowels; Kim et al., 1986).
The responses of two onset units to IRN were
shown by Shofner (1999). These units responded
with discharges locked to the f0 of sine or cosine
phase harmonic (CPH) complexes but responded
very poorly to random phase harmonic (RPH)
complexes and IRN with identical f0 Õs and sound
level. We have not observed such an extreme difference in response to these three stimuli when
recording from OC units. Nevertheless, we have
observed that the response to the f0 of IRN is
much weaker than that observed to RPH or CPH
146
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
complexes (e.g. Figs. 4 and 5 in Winter et al., 2001)
The complete absence of a response to IRN or
RPH stimuli, as observed by Shofner (1999), may
be due to either stimulus presentation level or type
of onset unit. Interestingly, Evans and Zhao (1998)
have shown that units classified as OI respond
poorly to RPH complexes.
OC units have been recorded from large multipolar cells within the VCN (Smith and Rhode,
1989). These are probably the same type of cell
that Doucet and Ryugo (1997) have observed to
contact cells in the fusiform layer of the dorsal
cochlear nucleus. The connection of these cells in
the cochlear nucleus is likely to be inhibitory, as
their terminals stain positively for glycine and are
characterised by pleomorphic vesicles in their
synaptic endings (Smith and Rhode, 1989). In
further studies, Doucet et al. (1999) have shown
that the same large multipolar cells project to the
contralateral cochlear nucleus. Therefore, despite
their ability to precisely encode the f0 of many
complex sounds, the current anatomical information about OC units would seem to argue against
them playing a role in the encoding of the pitch of
complex sounds and suggests that other unit types
(e.g. PL and choppers) may play a more pivotal
role.
4.2. Chopper units and pitch
Chopper units can enhance the representation
of sinusoidal amplitude modulated (SAM tones in
comparison to their auditory-nerve fibre input. At
moderate to high sound levels, some chopper units
show a band-pass modulation transfer function
(MTF: Frisina et al., 1990; Kim et al., 1990; Rhode
and Greenberg, 1994). The units most likely to
show a band-pass MTF were identified as CSs.
This observation was used by Hewitt and Meddis
(1994) to model the transformation from temporal
MTFs to rate based MTFs in single units in the
IC. It has since been proposed (Wiegrebe and
Winter, 2001) that the regular discharge patterns
seen in the responses of CS units may serve as a
stage of temporal processing that converts the allorder ISI representation of the pitch at the level of
the auditory nerve into a first-order ISI code and
hence may also be useful for encoding the pitch of
complex sounds. This hypothesis requires an array
of chopper units with a range of best periodicities
in iso-frequency laminae of the cochlear nucleus.
The range of intrinsic oscillation frequencies seen
in the unanaesthetised cat is very similar to the
range seen in the anaesthetised guinea pig. However, while the range of best periodicities may, in
part, be attributable to differences in stimulus
presentation level or output discharge rate of a
unit, in neither animal is this range sufficient to
encompass the range of pitch perception in humans (see Krumbholz et al., 2000). The lack of a
range of best periodicities to encompass the entire
range of pitch perception appears to argue against
chopper units playing a role in pitch perception.
However, if the bandwidths of the periodicity
tuning were sufficiently broad then perhaps the f0
could be represented by far fewer periodicity filters, perhaps analogous to the situation in colour
vision.
A further problem for the above hypothesis is
the response of chopper units to IRN. Shofner
(1999) has presented evidence that multipolar cells,
specifically chopper units, were not well suited to
encode the pitch of IRN. This conclusion was
based on the responses to IRN stimuli with negative gain. These stimuli elicit ambiguous pitches
that were only signalled in the temporal discharge
patterns of PL units (and hence bushy cells). The
responses of non-PL units (mainly choppers) largely reflected the stimulus envelope and not the
fine timing in the waveform structure. This result
appears to argue against chopper units playing a
role in the encoding of the pitch of complex sounds
in their first-order ISIHs. However, the examples
given in (Shofner, 1999) come from units with
relatively high BFs and a CT response pattern (see
Fig. 2); it is possible that low BF units, in particular those classified as CS, may show responses in
their temporal discharges related to the shift in
time intervals associated with the pitch of IRN
with negative gain. Until we have more data on
this issue the role of CS units in encoding the pitch
of complex sounds remains unresolved.
Interestingly, Shofner (1999) also found that the
majority of units with features related to the delay
of the RN were characterised by low BFs, where
phase locking would be strong. While we also
I.M. Winter et al. / Speech Communication 41 (2003) 135–149
observe the strongest temporal responses in units
with low BFs (unpublished observations) we also
observed that some units, with BFs well removed
from the phase-locking region, and at relatively
high stimulus presentation levels, could encode the
delay of IRN in terms of their first-order interval
statistics (Winter et al., 2001). This result is in
agreement with the vowel study presented here (see
Fig. 3), where both onset and chopper units
showed a strong response to the f0 , despite their
BFs being above the phase-locking cut-off in the
guinea pig (3.5 kHz, Palmer and Russell, 1986).
Stimulus presentation level may well explain the
different frequency ranges over which stimulus
related features were observed between the two
studies. It should, however, be made clear that the
significance of high BF units responding well to
the f0 of complex sounds is, at best, uncertain.
If the regular discharge pattern observed in
chopper units is responsible for the interval enhancement seen in this paper, and the best modulation frequency observed in other studies, then
one might find a close correlation between intrinsic
chopping frequency and interval enhancement. In
the (Frisina et al., 1990) study there was little
correlation between intrinsic chopping frequency
and best periodicity (their best modulation frequency). However, in the (Kim et al., 1990) study a
much closer relationship was found between a
unitÕs intrinsic oscillation and its best modulation
frequency. Kim et al. (1990) attributed this to their
method of estimating a unitÕs intrinsic oscillation
and/or a difference in unit type. The best correlation in the Kim study was found in CS units. If
the response to WN is also a good measure of a
unitÕs intrinsic oscillation then the results in the
present study (see Fig. 8 and Table 2) support the
findings of Kim et al. (1990).
In a small number of units, Wiegrebe and
Winter (2001) have shown that low BF units
identified as CS may respond in a relatively levelindependent manner. Whether this is a common
feature in CS units is not known. The importance of level independence, at such a low level
of auditory processing is, however, unclear. For
instance the majority of units in the inferior colliculus (the ultimate termination site for outputs
from the cochlear nucleus and superior olivary
147
complex) respond in a highly non-monotonic
fashion, suggesting that any level-independent response in the cochlear nucleus is recoded, in some
as yet unspecified manner.
5. Summary and conclusions
Our results show that units classified as onset
show a more robust response to f0 in the presence
of background noise than with chopper units.
Both onset and chopper units are able to encode
the delay of IRN in their first-order ISIHs but no
single unit type is able to represent the entire range
of delays over which a pitch is perceived. Although
OC units often show a strong response to the f0 of
complex sounds, increasing circumstantial evidence would appear to make their role in the
encoding of pitch uncertain. For instance, anatomical and pharmacological studies suggest
that they are probably wideband inhibitory interneurons within the cochlear nucleus. They may
also project to the contralateral cochlear nucleus.
Based on their responses to sinusoidal amplitude
modulation (Frisina et al., 1990; Kim et al., 1990)
and to IRN (Shofner, 1999; Winter et al., 2001) it
would appear that CT units are ill-suited to encode
the f0 of complex sounds. In contrast the responses
of CS units to SAM and IRN suggest that they
may have a role to play. However, it will be important to demonstrate that CS units can also
show a strong response to f0 at relatively low
sound levels and can represent the pitch of IRN
with negative gain. Until we have answers to such
questions, the role of these multipolar cells in the
encoding of pitch will remain unresolved.
Acknowledgements
Supported by the United Kingdom MRC
(G9900369). We thank Brian Moore and Keith
Kluender for helpful reviews of the manuscript.
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