Parmly Hearing Institute, Loyola University Chicago, Chicago, Illinois 60626
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ABSTRACT |
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Shofner, William P..
Responses of cochlear nucleus units in the chinchilla to
iterated rippled noises: analysis of neural autocorrelograms.
Temporal encoding of stimulus features related to the pitch of iterated rippled noises was studied for single units in the chinchilla cochlear
nucleus. Unlike other periodic complex sounds that produce pitch,
iterated rippled noises have neither periodic waveforms nor highly
modulated envelopes. Infinitely iterated rippled noise (IIRN) is
generated when wideband noise (WBN) is delayed (), attenuated, and
then added to (+) or subtracted from (
) the undelayed WBN through
positive feedback. The pitch of IIRN[+,
,
1 dB] is at 1/
,
whereas the pitch of IIRN[
,
,
1 dB] is at 1/2
. Temporal
responses of cochlear nucleus units were measured using neural
autocorrelograms. Synchronous responses as shown by peaks in neural
autocorrelograms that occur at time lags corresponding to the IIRN
can be observed for both primarylike and chopper unit types. Comparison
of the neural autocorrelograms in response to IIRN[+,
,
1 dB]
and IIRN[
,
,
1 dB] indicates that the temporal discharge of
primarylike units reflects the stimulus waveform fine structure,
whereas the temporal discharge patterns of chopper units reflect the
stimulus envelope. The pitch of IIRN[±,
,
1 dB] can be
accounted for by the temporal discharge patterns of primarylike units
but not by the temporal discharge of chopper units. To quantify the
temporal responses, the height of the peak in the neural
autocorrelogram at a given time lag was measured as normalized rate.
Although it is well documented that chopper units give larger
synchronous responses than primarylike units to the fundamental
frequency of periodic complex stimuli, the largest normalized rates in
response to IIRN[+,
,
1 dB] were obtained for primarylike units,
not chopper units. The results suggest that if temporal encoding is
important in pitch processing, then primarylike units are likely to be
an important cochlear nucleus subsystem that carries the pitch-related
information to higher auditory centers.
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INTRODUCTION |
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A variety of complex sounds produce the perception of pitch in
human subjects (Fastl and Stoll 1979), and it is likely
that the neural mechanisms underlying the perception of pitch are
similar among the various types of complex sounds. Licklider
(1951)
proposed that the nervous system extracts the pitch of a
complex stimulus by performing an autocorrelation analysis of the
information encoded in the auditory nerve. Similar conclusions
concerning complex pitch and autocorrelation have been made based on
computational models of the auditory periphery (Meddis and
Hewitt 1991
; Meddis and O'Mard 1997
). Using a
wide variety of periodic complex sounds, Cariani and Delgutte
(1996a
,b
) have shown that autocorrelation analysis of auditory
nerve spike trains provides a robust representation of pitch-related information.
Many of the neurophysiological investigations that have studied the
temporal representation of fundamental frequency in the auditory nerve
and cochlear nucleus have used periodic stimuli having highly modulated
stimulus envelopes. These stimuli include sinusoidally amplitude
modulated tones (Frisina et al. 1990; Javel 1980
; Joris and Yin 1992
; Khanna and
Teich 1989
; Kim et al. 1990
; Rhode
1995
; Rhode and Greenberg 1994
; Zhao and
Liang 1995
), complex tones (Greenberg and Rhode
1987
; Palmer and Winter 1992
; Rhode 1994
), and synthetic vowels (Keilson et al.
1997
; Kim and Leonard 1988
; Kim et al.
1986
; Palmer 1992
; Palmer and Winter
1992
; Rhode 1998
; Wang and Sachs 1993
,
1994
). One common observation from several of these studies is
that the synchronization to the fundamental frequency measured for
chopper and onset units in the cochlear nucleus is larger than that
observed for auditory nerve fibers or primarylike units unit types in
the cochlear nucleus (Frisina et al. 1990
;
Keilson et al. 1997
; Rhode 1998
;
Rhode and Greenberg 1994
; Wang and Sachs
1994
). Although not explicitly stated, the hierarchy of
synchrony described in many of the above studies implies that
primarylike units may play only a minor role in the temporal encoding
of pitch-related information in the cochlear nucleus. One proposed
neuronal circuit model of periodicity pitch involves components from
onset units, chopper units, and pauser units but does not include any
input from primarylike units (Langer 1988
). However, the
enhanced synchronization of chopper and onset units may only reflect
strong temporal responses to highly modulated stimulus envelopes, while
having lesser importance for pitch per se.
In contrast to the complex sounds mentioned above, rippled noises
generate the perception of pitch, but do not have highly modulated
stimulus envelopes. There is a temporal regularity in the waveform of
rippled noise, but this regularity is not repeated in a periodic
manner. Rippled noise of one iteration is generated when a wideband
noise (WBN) is delayed () and the delayed repetition of the WBN is
added to the original WBN; this type of rippled noise has been referred
to as cosine noise (Bilsen et al. 1975
). This
delay-and-add network can be repeated N times to generate rippled noises of N iterations (see Yost et al.
1996
). Figure 1 shows the circuit
used for generating a rippled noise of infinite iterations, i.e.,
infinitely iterated rippled noise (IIRN). WBN is delayed and
attenuated, and the delayed repetition of the WBN is added to the
original WBN through positive feedback. This type of rippled noise has
a spectrum with sharp peaks at integer multiples of 1/
(see Fig. 1)
and has been referred to as comb-filtered noise (e.g., Raatgever
and Bilsen 1992
). If the delayed repetition is inverted before
it is added (i.e., subtracted), then the spectral valleys occur at
integer multiples of 1/
, and the spectral peaks occur at odd integer
multiples of 1/2
. For simplicity throughout this paper, IIRN stimuli
will be referred to as IIRN[±,
, att], where ± indicates
whether the delayed noise was added (+) or subtracted (
),
is the
delay in milliseconds, and att is the attenuation of the delayed noise
in decibels. Thus an IIRN that was generated by adding the delayed
noise to the undelayed noise with a
of 4 ms and a delayed noise
attenuation of
1 dB will be referred to as IIRN[+, 4 ms,
1 dB].
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Figure 2 shows examples of the
autocorrelation functions of the waveforms for WBN and IIRN. The
waveform autocorrelation function of WBN is flat (Fig. 2A),
whereas there are positive correlations in the autocorrelation
functions of IIRN[+, 4 ms, 1 dB] at time lags of 4 ms and integer
multiples of 4 ms (Fig. 2B). The perceived pitch of the
IIRN[+, 4 ms,
1 dB] is at 1/
or 250 Hz (Fastl
1988
; Raatgever and Bilsen 1992
; Yost
1996a
), and if the pitch strength of a tone complex is 100%,
then the estimated pitch strength for the IIRN[+, 4 ms,
1 dB] is
~50-60% (see Yost 1996b
). For IIRN[
, 4 ms,
1
dB], there are negative correlations in the waveform autocorrelation
function at time lags of 4 ms and at odd multiples of 4 ms but positive
correlations at even multiples of 4 ms (Fig. 2C). That is,
these negative and positive correlations alternate throughout the
waveform autocorrelation function. Perceptually, the perceived pitch of
IIRN[
, 4 ms,
1 dB] is at 1/2
, or 125 Hz, i.e., one octave
lower than the pitch of IIRN[+, 4 ms,
1 dB] (Fastl
1988
; Raatgever and Bilsen 1992
; Yost
1996a
).
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Figure 2 also shows examples of the autocorrelation functions for the
envelopes obtained from a Hilbert transform of the waveform for WBN and
IIRN. The envelope autocorrelation function for WBN is flat (Fig.
2D), whereas there are positive correlations at and
integer multiples of
for both IIRN[+, 4 ms,
1 dB]
and IIRN[
, 4 ms,
1 dB] (Fig. 2, E and F).
The alternation of negative and positive correlations observed in the
waveform autocorrelation function is not observed in the envelope
autocorrelation function of IIRN [
, 4 ms,
1 dB].
Recent psychophysical studies have shown that the pitch and pitch
strength of iterated rippled noises as well as discrimination data can
be accounted for using temporal processing models based on
autocorrelation (Patterson et al. 1996; Yost
1996a
,b
, 1997
; Yost et al. 1996
). We have shown
previously that chinchillas can discriminate behaviorally IIRN[+,
,
att] from WBN and have argued that the underlying neural mechanisms
are common between chinchillas and human subjects (Shofner and
Yost 1995
, 1997
). Neurophysiological studies in the auditory
nerve and cochlear nucleus using rippled noise of one iteration have
shown that a temporal representation related to pitch can be found in
the discharge patterns of low-frequency auditory nerve fibers and
primarylike units (Shofner 1991
; ten Kate and van
Bekkum 1988
). The present study examined the representation of
in the temporal discharge patterns of cochlear nucleus units in the
chinchilla in response to IIRN stimuli. In this paper, the responses of
primarylike and chopper units are compared. If the hierarchy of
synchrony previously discussed reflects the relative importance of
units in the temporal encoding of pitch-related information, then
primarylike units should give the smallest synchronous responses to
rippled noise stimuli compared with other unit types.
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METHODS |
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The procedures have been reviewed and approved by the
Institutional Animal Care and Use Committee of Loyola University
Chicago. Twenty-three adult chinchillas weighing between 500 and
800 g were anesthetized with intraperitoneal injections of
pentobarbital sodium (70 mg/kg); supplemental injections were given to
maintain areflexia. Body temperature was maintained around 37°C with
a DC heating pad. Animals were tracheotomized, and the external auditory canals were exposed and transected. Animals were placed in a
modified headholder (Kopf Model 900), and the left bulla was exposed
and opened. The cerebellum was exposed by an opening in the temporal
bone in a manner similar to that described for gerbils by
Frisina et al. (1982). Animals were placed in a
double-walled sound-attenuating chamber (Tracoustics) during
neurophysiological recording of unit responses.
Indium-filled micropipettes (Dowben and Rose 1953) or
tungsten microelectrodes (Microprobe) were used to record single-unit activity. Neural spikes were amplified and filtered using standard electrophysiological procedures. Electrodes were advanced through the
cerebellum into the cochlear nucleus using an hydraulic microdrive system (Kopf 650). Using this approach, it was not uncommon to hold an
isolated single unit for 1-2 h. However, the use of metal microelectrodes often made the isolation of clear single units difficult, because multiple-unit activity or large neurophonic evoked
potentials were recorded frequently. Data regarding spike times were
obtained from neural spike trains that clearly were evoked from a
single unit and were not obtained by attempting to isolate single unit
activity from multiunit clusters of spike trains.
Data acquisition and stimulus presentation were under the control of
either a MassComp computer system or, in later experiments, a
Gateway2000 Pentium computer system with Tucker-Davis Technologies (TDT) modules. The sampling and conversion rates were set at 50 kHz for
the A/D and D/A devices. The times of occurrences of spikes were
determined on-line relative to the onset of the stimulus; the amplified
neural spikes were digitized and averaged on-line to examine the
averaged spike waveform for the presence of prepotentials (Pfeiffer 1966). Acoustic stimuli were presented to the
left ear through a Sennheiser HD 414 SL earphone that was enclosed in a brass housing; the housing also held a calibration microphone (Bruel
and Kjaer 4134). Acoustic search stimuli consisted of 100-ms bursts of
either wideband noise or tones at the best frequency (BF) of the
background neural activity.
When a unit was isolated, its BF first was determined using audiovisual
cues, and data were collected to classify the unit physiologically.
Classification of unit types was based on poststimulus time (PST)
histograms, interspike interval (ISI) histograms, and regularity
analysis (Bourk 1976; Young et al. 1988
)
as well as the presence or absence of a prepotential. BF tones were
generated by the computer and presented through a 16-bit D/A converter
(MassComp DA04H or TDT DA3-2 module). Rate-level functions were
generated over a 100-dB range in 1-dB steps for either 200- or 400-ms
BF tone bursts with rise/fall times of 10 ms presented once per second. One tone burst was presented at each level, and the rate-level function
was smoothed using a 5-bin triangular moving window average. Threshold
was defined as the level that first evoked an increase in discharge
rate >2 SDs above the estimated spontaneous discharge rate, provided
that the next three levels also evoked firing rates >2 SDs above
spontaneous rate. PST histograms were typically generated at 20-40 dB
above threshold for 250 presentations of a 50-ms BF tone with 2-ms
rise/fall times presented once every 250 ms. If the characteristic
discharge pattern was obscured in the PST histogram due to strong
phase-locking, then additional PST histograms were generated in which
each of the 250 presentations of the BF tone had a random starting
phase. The use of random starting phases sometimes allowed the
characteristic discharge pattern to become apparent.
After the data were collected for unit classification, the responses to
WBN and IIRN were studied. A set of WBN and IIRN stimuli were generated
using the same equipment and parameter settings that were used
previously to measure discrimination thresholds in chinchillas
(Shofner and Yost 1995). For WBN and each IIRN, 5 s
of the waveform was sampled; the waveform amplitudes were adjusted so
that all WBN and IIRN stimuli had equal root-mean-square (rms)
amplitudes. The 5-s samples of each noise then were stored on disk as
stimulus files. Rate-level functions first were generated over a 100-dB
range in 1-dB steps for 500-ms WBN bursts with rise/fall times of 10 ms
presented once per second, and threshold was estimated as defined above
for BF tone rate-level functions. The responses of the isolated unit
then were studied for WBN and IIRN stimuli at a fixed overall level,
generally at 20 dB above threshold as determined from the WBN
rate-level function. A total of 100 separate samples of WBN or IIRN
were presented. Consequently, the waveform of the noise was not the
same for each presentation. Each sample had a duration of 500 ms with
10-ms rise/fall times and were presented once every second; these are
the same parameters used in the previous behavioral study
(Shofner and Yost 1995
). Typically, the value of
was
first chosen to be 4 ms, followed by
s of 2 and 8 ms. These values
of
were chosen, because these were the
s at which psychometric
functions were obtained for chinchillas (Shofner and Yost
1995
). The delayed noise attenuation was fixed at
1 dB; an
attenuation of
1 dB generated an IIRN having the greatest pitch
strength without causing the positive feedback circuit (see Fig. 1) to oscillate.
The spike trains obtained in response to WBN and IIRN were analyzed as
PST histograms, spike count distributions, ISI histograms, and neural
autocorrelograms (i.e., all-order ISI histograms). The ordinates of the
autocorrelograms are scaled in terms of firing rate as described by
Abeles (1982), and each autocorrelogram displays three
horizontal reference lines. The middle horizontal line shows the
average firing rate obtained from the spike count distributions; the
upper and lower horizontal lines show the average rate ±2 SDs. These
horizontal lines only serve as visual aids and are not meant to imply
statistical significance. For comparison, temporal discharge properties
were occasionally obtained in response to harmonic tone complexes
consisting of the fundamental frequency and all harmonic frequencies
10 kHz. This produced tone complexes having bandwidths similar to the
bandwidths of the IIRNs. Tone complexes were synthesized by adding
individual components in cosine phase, sine phase, or random phase. The
rms amplitude of each tone complex was adjusted to equal the
rms amplitudes of the WBN and IIRN stimuli.
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RESULTS |
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Classification of unit types
The responses to IIRN stimuli were studied in a total of 86 single
units. A total of 26 units were grouped broadly as primarylike; this
sample includes both primarylike (n = 20) and
primarylike with notch (n = 6) subcategories of units.
Of these units, a total of 10 units were observed to have a
prepotential in the averaged spike waveform. A total of 35 units were
grouped broadly as chopper units.1 Although
a distinction among the various subcategories of chopper units was
made, all chopper units were grouped together for the present analysis.
A total of nine units were grouped broadly as onset units. Onset units
in this sample typically showed some low rate of discharge during the
duration of the tone stimulus and showed PST histograms similar in
shape to on-A or on-P units described by Bourk (1976).
Units were grouped as onset if the firing rate between 20 and 50 ms was
<100 spike/s (i.e., mean interspike interval was >10 ms) similar to
the scheme described by Blackburn and Sachs (1989)
. An
additional nine units having BFs <450 Hz were grouped as phase-locked;
these units showed strong BF phase-locking, and a characteristic
discharge pattern could not clearly be observed when BF tones were
presented with random starting phases. Finally, a total of seven
additional units could not be classified easily into any of the
preceding groups and are grouped as unusual. Prepotentials were not
observed in the spike waveform for any nonprimarylike unit.
Temporal responses to IIRN stimuli
The effect of on the temporal discharge pattern of a
primarylike unit (Fig. 3) in response to
IIRN[+,
,
1 dB] is illustrated in Fig.
4, A-C. There are peaks in
the neural autocorrelograms that occur at time lags of
and integer
multiples of
for each of the IIRN[+,
,
1 dB] conditions. In
response to IIRN[+, 2 ms,
1 dB], there are peaks in the
autocorrelogram at time lags of 2 ms and at integer multiples of 2 ms
(Fig. 4A); in response to IIRN[+, 4 ms,
1 dB], there are
peaks in the autocorrelogram at time lags of 4 ms and at integer
multiples of 4 ms (Fig. 4B); in response to IIRN[+, 8 ms,
1 dB], there are peaks in the autocorrelogram at time lags of 8 ms
and at integer multiples of 8 ms (Fig. 4C). Note that these
peaks are narrow and that there are oscillations in firing rate that
occur around
and each integer multiple of
.
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Figure 4, D-F, shows the autocorrelograms of the
primarylike unit obtained in response to IIRN[,
,
1 dB] with
delays of 2, 4, and 8 ms. In contrast to the autocorrelograms obtained
for IIRN[+,
,
1 dB], there are nulls in the IIRN[
,
,
1
dB] autocorreolograms at time lags corresponding to
and at
odd-integer multiples of
. For example, when
is 4 ms, there is a
null in the autocorrelogram at a time lag of 4 ms (Fig. 4E).
Note that there is also a pair of positive peaks at time lags of ~3.5
and 4.5 ms that flank these nulls. The pair of peaks around the null at
reflect the tuning properties of the unit and are not directly
related to the pitch of the stimulus. The peaks are further apart for
low BF units and are closer together for high BF units. In addition to
this pair of peaks, there is also a peak in the autocorrelogram at a
time lag of 8 ms (i.e., at 2
). Consequently, there are nulls at time
lags of
and odd-integer multiples of
but peaks at time lags of
even-integer multiples of
. Similar results are observed in the
autocorrelograms in response to IIRN[
, 2 ms,
1 dB] (Fig.
4D) and IIRN[
, 8 ms,
1 dB] (Fig. 4F).
Comparison of these neural autocorrelograms to the stimulus
autocorrelograms (Fig. 2) suggests that the temporal discharge
properties of the primarylike unit are driven by the waveform fine structure.
The effect of on the temporal discharge pattern of a high BF
primarylike unit in response to WBN and IIRN[±,
,
1 dB] is illustrated in Fig. 5. Note that this
unit has a prepotential in its spike waveform (Fig. 5A,
inset). Similar to the preceding primarylike unit, the
autocorrelograms of this high BF primarylike unit show peaks at
and
integer multiples of
in response to IIRN[+,
,
1 dB] (Fig. 5,
C and D). However, in contrast to the previous
primarylike unit, the autocorrelograms in response to IIRN[
,
,
1 dB] also show peaks at
and integer multiples of
(Fig. 5,
E and F). That is, nulls at time lags of
and
odd-integer multiples of
are not observed for the high BF
primarylike unit. Comparison of these neural autocorrelograms with
stimulus autocorrelograms (Fig. 2) suggests that the temporal discharge
properties of this primarylike unit are driven by the stimulus
envelope.
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The effect of on the temporal discharge pattern of a
transient-chopper unit (Fig. 6) in
response to IIRN[+,
,
1 dB] is illustrated in Fig.
7, A and B. The
temporal discharge pattern of the chopper unit is similar to that
described above for the primarylike unit in that there are peaks at
and integer multiples of
in response to IIRN[+,
,
1 dB].
When
is 4 ms, there are peaks in the autocorrelogram at time lags
of 4 ms and at integer multiples of 4 ms (Fig. 7A); when
is 8 ms, there are peaks in the autocorrelogram at time lags of 8 ms
and at integer multiples of 8 ms (Fig. 7B). The temporal
discharge of the chopper unit in response to IIRN[
,
,
1 dB] is
shown in Fig. 7, C and D. The autocorrelograms in
response to IIRN [
,
,
1 dB] are similar to those obtained for
IIRN [+,
,
1 dB] when
is 4 and 8 ms. In particular, in
response to IIRN [
, 4 ms,
1 dB], there are no nulls observed at a
time lag of 4 ms, but rather there are peaks at a time lag of 4 ms and
integer multiples of 4 ms (Fig. 7C). Similar peaks at time
lags of 8 ms and integer multiples of 8 ms also are observed in the
autocorrelograms in response to IIRN[
, 8 ms,
1 dB] (Fig.
7D). Example autocorrelograms in response to IIRN[+,
,
att] and IIRN[
,
, att] stimuli obtained from 1 of the 15 units
classified as a chopper1 based on its ISI histogram but
having a PST histogram more similar to a primarylike pattern (Fig.
8) are shown in Fig.
9. Again there are peaks in the
autocorrelograms at time lags of 8 ms and at integer multiples of 8 ms
in response to both IIRN[+, 8 ms,
1 dB] and IIRN[
, 8 ms,
1
dB] (Fig. 9, A and C); there are peaks in the
autocorrelogram at time lags of 4 ms and at integer multiples of 4 ms
in response to both IIRN[+, 4 ms,
1 dB] and IIRN[
, 4 ms,
1
dB] (Fig. 9, B and D). Comparison of these
neural autocorrelograms with stimulus autocorrelograms (Fig. 2)
suggests that the temporal discharge properties of the chopper units
are driven by the stimulus envelope.
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The temporal responses to IIRN[+, 4 ms, 1 dB] and to harmonic
tone complexes having a fundamental frequency of 250 Hz (i.e., period
of 4 ms) for an onset unit are shown in Fig.
10. It can be observed clearly that
neither IIRN[+, 4 ms,
1 dB] (Fig. 10A) nor the random
phase harmonic tone complex (Fig. 10B) evoked an excitatory
response from the unit. In contrast, a large excitatory response can be
observed to both the harmonic tone complex added in cosine and sine
phase (Fig. 10, C and D). Although 4-ms ISIs were
not obtained, the autocorrelograms (Fig. 10, E and
F) show that the temporal discharge pattern is related to
the periodicity of the tone complex. Figure
11 shows the autocorrelograms of
another onset unit in response to WBN, IIRN[+, 4 ms,
1 dB] and
harmonic tone complexes. Although this unit gave an excitatory
response, the autocorrelograms show no temporal features at a time lag
of 4 ms in response to either IIRN[+, 4 ms,
1 dB] (Fig.
11C) or a cosine phase harmonic tone complex with a period
of 4 ms (Fig. 11D). In response to a random phase harmonic
tone complex with a period of 20 ms, there is a weak peak at a time lag
of 20 ms in the autocorrelogram (Fig. 11E). Note the general
similarity in the shape among the autocorrelograms for WBN, IIRN[+, 4 ms,
1 dB] and these two harmonic tone complexes. In contrast, the autocorrelogram shows that there is strong phase-locking to the period
of 20 ms obtained in response to a cosine phase harmonic tone
complex with a period of 20 ms (Fig. 11F). Thus a strong
synchronous response from this unit is driven by a stimulus having
a highly modulated envelope but a low fundamental frequency.
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Quantitative analysis of temporal responses to IIRN[+, 4 ms,
1 db]: peak height
The temporal properties of IIRN stimuli can be quantified by
measuring the heights of the peaks at a time lag of in the stimulus
autocorrelation functions. The temporal discharge patterns of units
displayed in neural autocorrelograms can be quantified in an analogous
manner by estimating the heights of the peaks at a time lag
corresponding to
. Note that in all of the neural autocorrelograms,
the peak heights are expressed in units of firing rate; consequently,
the firing rates at a particular time lag in the autocorrelogram will
be referred to as instantaneous firing rates. The instantaneous firing
rate at
is defined as the maximum firing rate in the
autocorrelogram in a 1-ms window centered at a time lag of
. To
compare across units having different average firing rates, the
instantaneous firing rates at a time lag of
were measured in terms
of normalized rate at a particular time lag as given by
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(1) |
Figure 12 compares the normalized rates
at a time lag of 4 ms for WBN and IIRN[+, 4 ms, 1 dB] for the
primarylike and chopper units sampled in this study. The normalized
rates for WBN also were measured as the maximum firing rate in a 1-ms
window centered around the time lag of 4 ms and are shown for
comparison. Note that for primarylike units (Fig. 12A) the
normalized rates obtained in response to IIRN[+, 4 ms,
1 dB] are
generally larger than the normalized rates for WBN, whereas this does
not appear to be the case for chopper units (Fig. 12B).
Although there is scatter in the data, it can be observed that for the
primarylike/phase-locked units, there are no normalized rates measured
at a 4-ms lag having negative values for IIRN[+, 4 ms,
1 dB],
whereas there are normalized rates having negative values for the
chopper units (see Fig. 12B,
). In response to IIRN[+, 4 ms,
1 dB], there were 0/51 (0%) negative normalized rates observed
for primarylike/phase-locked group (Fig. 12A), there were
14/55 (25.4%) negative normalized rates observed for chopper group
(Fig. 12B), there were 7/15 (46.7%) negative normalized
rates observed for onset group, and there were 6/10 (60%) negative
normalized rates observed for unusual group.
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The normalized rates obtained in response to IIRN[+, 4 ms, 1 dB]
for a sample of 15 autocorrelograms from 11/20 primarylike units and 12 autocorrelograms from 5/6 primarylike with notch units were ranked.
These primarylike and primarylike with notch units had a similar range
of BFs between 0.85 and 5.44 kHz. Based on a Mann-Whitney U
test, the normalized rates for the primarylike and primarylike notch
units were the same. Therefore the data for primarylike and primarylike
with notch units were pooled. Figure 13
shows the average normalized rates obtained for both WBN and IIRN[+, 4 ms,
1 dB] for primarylike and chopper units having BFs between 0.64 and 1.6 kHz (left) and BFs >1.6 kHz (right). A
single-factor ANOVA showed that there was a significant difference across the eight groups of WBN and IIRN conditions for primarylike and
chopper units [F(7,166)=15.86; P < 0.0005]. Onset and unusual units were not included in the analysis
because there were relatively few responses in each of the above
groups. Paired comparisons were subsequently made using the Tukey's
HSD test and are summarized in Table 1.
For the IIRN[+, 4 ms,
1 dB] conditions, there is a significant
difference between the mean of the primarylike and the mean of the
chopper units at
= 0.01 for units with BFs between 0.64 and 1.6 kHz
as well as for units with BFs >1.6 kHz. Paired comparisons between the
responses to WBN and IIRN[+, 4 ms,
1 dB] within a given unit type
show that there is a significant difference at
= 0.01 between the
means for WBN and IIRN[+, 4 ms,
1 dB] for primarylike units with
BFs between 0.64 and 1.6 kHz and for primarylike units with BFs >1.6
kHz.
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Quantitative analysis of temporal responses to IIRN[±, ,
1 dB]: peak location
As previously described, there appears to be a tendency that the
autocorrelograms of low BF primarylike units show a peak at a time lag
of in response to IIRN[+,
,
1 dB] but show a peak at 2
in
response to IIRN[
,
,
1 dB], whereas the autocorrelograms of
chopper units and high BF primarylike units appear to show a peak at a
time lag of
in response to both IIRN[+,
,
1 dB] and
IIRN[
,
,
1 dB]. To quantify this, it was determined whether the time lag of the first or largest peak in the neural autocorrelogram occurred at
or 2
for each response to IIRN stimuli, provided that there was a clear temporal response to the IIRN and that data were
obtained for both IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB]
for the same unit.
Figure 14 shows the number of responses
occurring at a time lag of either or 2
for primarylike and
chopper units. For primarylike units, 28/29 (96.6%) of the peaks were
at a time lag of
in response to IIRN[+,
,
1 dB]. Only one
response was observed at a time lag of 2
; no peak at
was
observed in this autocorrelogram. In response to IIRN[
,
,
1
dB], 8/29 (27.6%) of the peaks were located at a time lag of
; the
ISI histograms of these primarylike units did not show any evidence of
phase-locking to BF tones. In contrast, 20/29 (70%) were observed at
2
in response to IIRN[
,
,
1 dB]; the ISI histograms of
these primarylike units showed phase-locking to BF tones. One response
was observed at 4
; this was the same unit that showed a peak at 2
for IIRN[+,
,
1 dB] described above. For chopper units, 12/16
(75%) of the peaks were located at a time lag of
, whereas 4/16
(25%) were located at 2
in response to IIRN[+,
,
1 dB]. In
response to IIRN[
,
,
1 dB], 11/16 (68.8%) were located at
time lags of
and 5/16 (31.2%) were at time lags of 2
. To
determine whether there was a significant difference in the location of
the peaks for primarylike and chopper units, contingency tables were
generated and a
2 analysis was carried out. The location
of the peak in the neural autocorrelogram is not the same in response
to IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB] for primarylike
units (
2 = 29.3; P < 0.001). In
contrast, the location of the peak in the autocorrelogram is the same
in response to IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB] for
chopper units (
2 = 0; not significant at
= 0.05).
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DISCUSSION |
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The responses of primarylike and chopper units in the chinchilla
cochlear nucleus were measured to the same IIRN stimuli that have been
studied previously in psychophysical experiments using chinchillas
(Shofner and Yost 1995) and human listeners
(Fastl 1988
; Raatgever and Bilsen 1992
).
Temporal responses of single units were studied using autocorrelograms
or all-order ISI histograms. Neural autocorrelograms show the
probability of discharge after a given spike; that is, they show the
average firing pattern of a unit after a spike. Autocorrelation
analysis provides a robust representation of the pitch related
information encoded in the spike trains of auditory nerve fibers
(Cariani and Delgutte 1996a
,b
; Palmer
1992
). The present results show that a temporal representation of
can be obtained in neural autocorrelograms in response to IIRN[±,
,
1 dB] from both primarylike and chopper units. To gain some insight into the relative importance of primarylike and
chopper units, it is informative to make comparisons between the
neurophysiological data and behavioral results with respect to IIRN
pitch and coloration discrimination.
IIRN pitch
The perceived pitch of IIRN[+, 4 ms, 1 dB] corresponds to
1/
or 250 Hz, whereas the pitch of IIRN[
, 4 ms,
1 dB]
corresponds to 1/2
or 125 Hz (Fastl 1988
;
Raatgever and Bilsen 1992
). In other words, human
listeners can discriminate IIRN[+, 4 ms,
1 dB] from IIRN[
, 4 ms,
1 dB] based on pitch. Autocorrelograms of some primarylike units
show peaks at time lags of
and integer multiples of
in the
neural autocorrelograms in response to IIRN[+,
,
1 dB], but
nulls at times lags of
followed by a peak at 2
in the
autocorrelograms in response to IIRN[
,
,
1 dB]. These primarylike units typically show phase-locking to BF tones. Thus the
temporal discharge patterns of this phase-locked group of primarylike
units are similar to the stimulus waveform autocorrelation functions.
Autocorrelograms of some chopper units, as well as nonphase-locked
primarylike units show peaks at time lags of
and integer multiples
of
in response to both IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB]. That is, the temporal discharge patterns of these units are
more similar to the stimulus envelope autocorrelation function than the
waveform autocorrelation function.
2 analysis of the location of the first or largest peak
in the autocorrelogram shows that for primarylike units, there is a
difference in the responses to IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB], but the difference does not exist for chopper units. Thus a discrimination between IIRN[+,
,
1 dB] and IIRN[
,
,
1 dB] can be made based on temporal discharge patterns of
primarylike units, whereas a discrimination between IIRN[+,
,
1
dB] and IIRN[
,
,
1 dB] cannot be made on the basis of the
temporal discharge properties of chopper units. Current models that
account for the pitch and pitch strength of iterated rippled noises are based on temporal processing of the waveform fine structure
(Patterson et al. 1996
; Yost 1996a
,b
,
1997
; Yost et al. 1996
), and the present study
shows that the temporal discharge patterns of primarylike units are
driven by the waveform fine structure. More recent psychophysical data
argue that the pitch perception of iterated rippled noises cannot be
based on stimulus envelope (Yost et al. 1998
), and the present results show that the temporal discharge patterns of chopper units are driven by the stimulus envelope of IIRN. This finding is
consistent with the idea that chopper units are principal subsystems that encode stimulus envelope in their temporal discharge (see Greenberg and Rhode 1987
).
Coloration discrimination
At the present time, it is not known whether chinchillas can
discriminate IIRN[+, ,
1 dB] from IIRN[
,
,
1 dB].
Behavioral studies using chinchillas (Shofner and Yost 1995
,
1997
) have been based on coloration discrimination paradigms
(see Bilsen and Ritsma 1970
). In the coloration
discrimination experiment, the listener discriminates IIRN from WBN,
and chinchillas can easily discriminate IIRN[+, 4 ms,
1 dB] from
WBN (Shofner and Yost 1995
, 1997
). In the present study,
the magnitudes of the temporal responses were compared between IIRN[+,
4 ms,
1 dB] and WBN. The response to WBN provides insights into the
temporal response to a noise that does not generate a pitch and then
can be compared with the temporal response to a noise that does
generate a relatively salient pitch. For human listeners, the pitch
strength of IIRN[+, 4 ms,
1 dB] is ~50-60% of the pitch
strength of a harmonic tone complex (see Yost 1996b
).
The magnitude of the neural response was estimated as the normalized
rate at milliseconds from the neural autocorrelograms. The peak at
is generally the largest
-related peak in the autocorrelogram. Yost (1996b)
has shown that the pitch strength of
IIRN[+,
, att] can be accounted for using a model based on the
height of the first peak in the autocorrelation function. The average
normalized rate at a time lag of 4 ms in response to IIRN[+, 4 ms,
1
dB] is larger for the sample of primarylike units than that of the chopper units, whereas the average normalized rate at a time lag of 4 ms is the same for primarylike and chopper units in response to WBN.
Moreover, the average normalized rates at 4 ms are larger for
primarylike units in response to IIRN[+, 4 ms,
1 dB] than in
response to WBN, whereas the average normalized rates at 4 ms for
chopper units in response to IIRN[+, 4 ms,
1 dB] are not different
from those obtained in response to WBN. However, for some units the
largest peak in the neural autocorrelogram is observed at a time lag of
2
rather than at
(e.g., see Fig. 9, B and D). Peaks at 2
also should convey information about pitch
strength. A single-factor ANOVA and subsequent paired comparisons based on either the normalized rates at 2
or an average of the normalized rates at
and 2
also showed that the responses of primarylike units are larger than chopper units. Moreover including the data at
2
does not make the difference between IIRN and WBN statistically significant for chopper units. Thus the largest
-related temporal responses for IIRN are those associated with primarylike units not
chopper units. Chopper units do show an enhancement of synchronization compared with primarylike units in response to the fundamental frequency of SAM tones, complex tones and synthetic vowels
(Frisina et al. 1990
; Keilson et al.
1997
; Rhode 1998
; Rhode and Greenberg 1994
; Wang and Sachs 1994
). Although the
periodic stimuli that have been used in the preceding studies do
generate the perception of pitch in human listeners, these stimuli also
possess highly modulated stimulus envelopes. The enhanced
synchronization to the fundamental frequency observed for chopper units
in response to periodic complex sounds having highly modulated
envelopes is not found for their temporal responses to IIRN stimuli.
Conclusion
The results of the present study show that primarylike units give
larger temporal responses than chopper units to IIRN, and the temporal
responses of primarylike units can account for the differences in pitch
between IIRN[+, ,
1 dB] and IIRN[
,
,
1 dB], whereas
those of chopper units cannot. However, it cannot yet be concluded that
primarylike units are the principal cochlear nucleus subsystem that
encodes the pitch related information in their temporal discharge. The
present study did not sample onset-type-I (on-I) and onset-chopper
units, which have been suggested to be important cochlear nucleus
subsystems that encode pitch-related information in their temporal
discharge patterns (Greenberg and Rhode 1987
; Kim
and Leonard 1988
; Kim et al. 1986
). Recent
studies have shown that on-I units can show strong synchronization to the fundamental frequency of a tone complex in which components were
added in cosine phase but weak or no synchronization to random phase
tone complexes (Evans and Zhao 1998
), suggesting that
on-I units may not give strong temporal responses to IIRN stimuli. Nevertheless, the results of the present study suggest that the contribution of primarylike units in the temporal encoding of pitch-related information is not insignificant. Although primarylike units may not be the principal subsystem, they are likely to be an
important cochlear nucleus subsystem underlying the perception of pitch.
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ACKNOWLEDGMENTS |
---|
The author thanks R. Patka for assistance in the data collection of some of these experiments and Drs. W. A. Yost and R. H. Dye, Jr., and two anonymous reviewers for comments on the manuscript.
This research was supported by National Institute of Deafness and Other Communications Disorders Program Project Grant (P01 DC-00293).
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FOOTNOTES |
---|
Address for reprint requests: Parmly Hearing Institute, Loyola University Chicago, 6525 N. Sheridan Rd., Chicago, IL 60626.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1
Of these 35 chopper units, 20 units were classified
initially as chopper and 15 were classified initially as on-G (i.e.,
onset-gradual). The PST histograms of these on-G units did not show
clear multiple peaks characteristic of chopping, but rather were more
similar in shape to PST histograms of primarylike or onset-enhanced
primarylike units (Palmer et al. 1986). However, the
interspike interval (ISI) histograms of these on-G units were more
similar to ISI histograms of chopper units (see Fig. 8,
C and D). A single-factor ANOVA showed
that there was a significant difference across the mean coefficients of
variation (CV) of the ISI histograms for primarylike, chopper
(n = 20), and on-G (n = 15)
units; the mean CVs were 0.66, 0.42, and 0.41, respectively. Paired
comparisons subsequently were made using the Tukey's HSD test. At the
= 0.01 level, there was a significant difference in the means
between primarylike versus chopper units and a significant difference
in the means between primarylike and on-G units. There was no
significant difference in the means between chopper and on-G units.
Therefore, it was concluded that the on-G units were not a separate
group of units but should be classified as chopper units.
Received 1 September 1998; accepted in final form 9 February 1999.
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REFERENCES |
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