Hearing Research, 44 (1990) 99-122

Elsevier

99

HEARES 01325

Encoding of amplitude modulation in the gerbil cochlear nucleus: I. A hierarchy of enhancement

Robert D. Frisina ‘To, Robert L. Smith 3-4 and Steven C. Chamberlain 3.4 ’ Otolatyngology Division of Surgery Department and ’ Physiology Department, Universi@ of Rochester School of Medtcine

and Denttstv, Rochester, New York, U.S.A. and * Institute for Sensory Research

and 4 Department of Bioengineering, Svracuse University, Syracuse, New York, U.S.A.

(Received 1 September 1989; accepted 14 October 1989)

The main goal of the present study was to investigate the encoding of a biologically-relevant acoustic feature-amplitude

modulation (AM)-in single neurons of the auditory nerve and ventral cochlear nucleus (VCN). In the anesthetized gerbil

auditory-nerve fibers and VCN units show strong synchronous responses to low-intensity, low-frequency AM. As frequency increases.

the strength of the synchronous response decreases. In the auditory nerve the strength of the synchronous response is substantially

less at high intensities than at low intensities and does not change significantly with AM frequency at high intensities. In contrast to

the auditory nerve, VCN units show strong responses at high intensities. They have a particular AM frequency to which they are

maximally responsive, and this frequency varies from unit to unit. Therefore, VCN units transform their ascending inputs by

enhancing the synchronous response to AM. A correlation exists between a unit’s ability to encode AM and its responses to simple

sounds. Specifically, onset units show the strongest synchronous responses, followed in order by chopper. primarylike-with-notch and

primarylike units. This enhancement is greatest at high intensities and can occur up to 90 dB above a unit’s threshold. Thus. a

hierarchy of enhancement for AM processing exists in the most peripheral nucleus of the central auditory system.

Cochlear nucleus: Auditory nerve; Amplitude modulation: Neurophysiology: Single neuron: Gerbil

Introduction

It has been known for over two decades that single neurons of the mammalian cochlear nucleus differentially process the inputs they receive from the auditory nerve (Rose et al., 1959; Pfeiffer, 1966). The vast majority of the research performed in this area involved the use of simple auditory signals as stimuli, such as pure tones and clicks. For example, analyses of responses to pure tones in the form of post-stimulus-time histograms (PSTHs) have revealed basic unit categories such as ‘primarylike’, ‘chopper’, ‘onset’, ‘pause? and ‘buildup’. More detailed studies with simple

Correspondence to: R.D. Frisina, Otolaryngology Division, Box

629, University of Rochester Medical Center, 601 Elmwood

Avenue, Rochester, NY, 14642. U.S.A.

sounds have revealed different variations on these basic PSTH response patterns (cat: Godfrey et al., 1975a, b; Bourk, 1976; gerbil: Frisina et al., 1982; rabbit: Hui and Disterhoft, 1980). In some cases, these pure-tone PSTH response categories have been correlated with other responses to simple sounds, such as dynamic range of responses to steady-state changes in sound intensity (Godfrey, 1971; Rhode and Smith, 1986; Rhode and Ket- tner, 1987; Frisina et al., 1990). In other instances, pure-tone response characteristics have been cor- related with single-neuron morphology and loca- tion (Caspary, 1972; Frisina, 1983: Rhode et al., 1983a, b; Rouiller and Ryugo, 1984). Elegant studies of the nature of excitatory and inhibitory response areas of cochlear nucleus units have also been performed using simple acoustic signals (Evans and Nelson, 1973; Young and Brownell, 1976; Voigt and Young, 1980; Ritz and Brownell, 1982).

0378-5955/90/$03.50 Q 1990 Elsevier Science Publishers B.V. (Biomedical Division)

In parallel with these investigations using sim- ple sounds, pioneering single-unit studies of the cochlear nucleus were conducted by Moller using complex sounds. One of his main goals was to

perform a linear systems analysis on single-neuron responses to determine the fidelity with which rapid changes in sound amplitude or amplitude modulation (AM) are encoded (Merller, 1972; 1973; 1974a. b; 1975a, b; 1976a, b, c). He found that, except at very high stimulus modulation depths, most cochlear nucleus units encode AM with little distortion. Units are tuned to different AM fre-

quencies (80-500 Hz) and their tuning properties were relatively insensitive to variations in stimulus parameters such as the depth of modulation, stimulus duration, and whether continuous tones

or repetitive tone bursts were used as stimuli. AM tuning properties of a single unit remained stable for hours and were independent of the method used to measure them. For example, when either tones or noise modulated with sinusoids were used and the depth of modulation in the response was obtained from period histograms phase-locked to the stimulus envelope. In other cases, continuous tones or noise were modulated with pseudoran- dom noise and the stimulus cross-correlated with the spike activity. Fourier analysis of these cross- correlation functions then allowed the computa-

tion of a unit’s AM tuning properties. Moller also found an amplification of the stimulus modulation depth in the responses of some cochlear nucleus units at intensities up to 60 dB above threshold. In contrast, he found that auditory-nerve fibers show this amplification over only a 30 dB range. Lastly, he demonstrated that the dynamic operating range for AM encoding exceeds that of the average rate-intensity function for many cochlear nucleus units.

One of the major questions concerning the role that the cochlear nucleus plays in processing acoustic information under natural listening con- ditions is how the responses of single units to dynamic. biologically-relevant complex sounds are related to what we know about their responses to simple sounds. Primary goals of the present inves- tigation were to further explore encoding of com- plex sounds and possible relationships between units’ responses to classical, simple sounds and their responses to more complex acoustic features

such as AM. We found that for units in the ventral cochlear nucleus (VCN) a hierarchy of enhancement exists for the encoding of AM, with

a unit’s ability to encode AM correlated with the deviation of its pure-tone responses from a primarylike response. Portions of the results of the present study have been reported previously in summary form (Smith et al., 1983; Frisina et al.. 1984; 1985). Possible neural mechanisms by which this hierarchy of enhancement occurs in the VCN are investigated in the companion paper (Frisina et al.. 1990).

Methods

Surgicul preparation

Single-unit, extracellular recordings were ob- tained from 103 ventral cochlear nucleus (VCN) neurons and 37 auditory-nerve fibers from 36 young, adult gerbils ( Meriones unguiculatus. 4-7 months old). Animals were anesthetized with Nembutal for all surgical and recording proce- dures. Initial doses of 50 mg/kg were given with supplemental doses of 25 mg/kg administered as required. Rectal temperature was maintained at 38” C. Surgical approaches to the cochlear nucleus (Frisina et al., 1982) and auditory nerve (Sokolich and Smith, 1973: Chamberlain, 1977) have been described in detail previously and are summarized here. After placing the tracheotomized animal in a headholder and removing the auricle, the skin over the lateral wall of the bulla adjacent to the super- ior-posterior and inferior-posterior mastoid cham- bers was retracted to gain access to the cochlear nucleus (see Lay, 1972, for bullar terminology). The lateral wall of the bulla adjacent to the super- ior-posterior mastoid chamber was removed to expose a region of the temporal bone lying within

the perimeter of the superior semicircular canal. A hole was made in the center of this region to expose the parafloccular lobe of the cerebellum. Electrodes were inserted through this hole and advanced from outside the sound-proofed re- cording booth (IAC) using a piezoelectric micro- drive (Burleigh Inchworm). To gain access to the auditory nerve, a hole was made in the temporal bone within the round window antrum. To record the compound action potential of the auditory nerve, a silver wire electrode was placed near the

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round window. A silver ground wire was placed into the animal’s mouth. Data were collected only from animals with unobstructed outer ears, healthy middle ears, and normal sensitivity of the round-

window compound action potential in response to clicks and tone pips (5-24 kHz).

Stimulus generation and control Tonal stimuli were generated by a beat-

frequency oscillator whose output was gated by an electronic switch with a rise-decay time of 2.5 ms.

The system sync had a period of 390 ms. The signal passed through a digital attenuator which was under computer control (PDP-11/34) and a manual attenuator. Wideband noise stimuli were

produced by a noise generator (GSC 455C) whose output was fed into a parallel circuit identical to the one described for tonal stimuli. Finally, the signal was applied to a : inch condenser micro- phone (B and K) with a 200 V bias. The micro-

phone was coupled to the external auditory meatus with a hollow ear bar.

Sinusoidally amplitude-modulated signals were produced by multiplying the carrier by the sum of

a sinusoidal and DC signal. The modulating sinusoid was generated by a programmable frequency synthesizer (Rockland 5100) under computer control. The timing, amplitude and phase of the modulating sinusoid were under inde- pendent control so that the onset of modulation and percent modulation could be varied indepen- dently of the carrier.

The small size of the gerbil head and external auditory meatus places constraints on the size of an acoustic source and monitor. Consequently, the sound pressure close to the tympanic membrane in the external auditory meatus was measured with an independently placed probe tube and measur- ing microphone. Because of the additional surgery necessary to insert the probe tube, the calibration procedure was performed upon completion of the neurophysiological recording part of an experi- ment. As a control for this procedure, prior to making the additional hole in the ear canal, the cochlear microphonic (CM) was recorded through the round-window electrode for tone bursts of frequencies 0.6-24 kHz. The signal from the round-window electrode was input to a 1000 x amplifier with a bandwidth of 0.08-40 kHz, the

output of which was fed into a lock-in amplifier (Ortholoc-SC 9505). The voltage input to the con- denser microphone required for a criterion re- sponse was measured at each frequency. Next, a small hole was made anteroventral to the natural

opening of the ear canal and a calibrated probe tube (W.G. Sokolich) coupled to a : inch con- denser microphone (B and K) was inserted into it. The probe tube had a flat frequency response up to 2 kHz which then fell off at a slope of 6

dB/octave at higher frequencies. The hole was sealed by placing a porous rubber material soaked in Vaseline around the barrel of the probe tube and up against the surrounding bone. With the probe tube in place the CM measurements de-

scribed above were repeated. Thus, the combined inverse transfer function of the middle ear and cochlea could be compared immediately before and after insertion of the probe tube. Any small changes in sound pressure in the ear canal due to the presence of the probe tube could be corrected for by adjusting the sound pressure for a criterion

CM response. Finally, the sound pressure near the tympanic membrane was measured using the same stimulus as for the CM measurements. The output of the measuring microphone was connected to the same devices used to measure the round- window potentials except that the input to the stimulating microphone was kept at 1 V rms for all frequencies. The output of the lock-in amplifier was converted to sound pressure using the probe- tube calibration data. Individual measurements were made for 15 animals of the present study, and single-unit thresholds in this report have been calculated using the average data from these animals.

Neurophysiological recording and data analyses Recording sites in the VCN were determined

by comparing in vivo electrode orientations with a scale model of the cochlear nucleus and adjacent temporal bone (Frisina et al., 1982) or by making intracellular or extracellular injections of HRP from the recording electrode. Glass micropipettes (Omega-dot borosilicate) pulled on a Brown- Flaming puller were used as recording electrodes. One day prior to a staining experiment. the elec- trode tips were filled with a 4% solution of HRP (Sigma Type VI) in 0.5 M KC1 buffered to pH 7.6

102

with 0.05 M Tris buffer (Light and Durkovic. 1976). They were stored overnight in a cold. humid chamber and backfilled with 0.5 M KC1 in Tris buffer immediately before use. To prevent clogging

of the tip. the micropipettes were beveled using a jet-stream beveler (Ogden et al., 1978). This re- duced the impedance from approximately 300 to 75 MO. For intracellular or quasi-intracellular (McIlwain and Creutzfeldt. 1967) HRP injections. a positive square-wave voltage with a duration of

100 ms, a level of 5-10 nA and a repetition rate of 5 pulses/s was applied to the recording electrode using a constant-current source (WPI 161) for

5-20 min. Extracellular injections were utilized in the following way to localize single-unit recording sites to a subdivision of the VCN. On a single penetration, recordings of several units were often made within a distance of 300 pm or less. After recording from the last unit of the penetration, HRP was injected extracellularly from the record- ing electrode. The polarity and timing of the cur- rent pulses were the same as used intracellularly but the levels were raised to 100 nA. To avoid ambiguities in interpretation, this extracellular staining technique was never performed more than twice in the same animal. Recording micropipettes for auditory-nerve experiments were filled with either 3 M KC1 or 3 M NaCl.

The recording electrodes were coupled to a high-impedance, unity-gain, DC amplifier (Pico- metric 181) via an Ag-AgCl bridge. This amplifier

had a capacitance compensation which was set to optimize the in vivo frequency response for each electrode. The output of this amplifier was analyzed in several ways. To process spike data. the signal was fed to a 1000 x amplifier (Tektronix 122) with a bandwidth of 80-1000 Hz. It was then sent to a direct channel of a 7-track tape recorder (Honeywell 5600) and stored for off-line analysis. To observe generator potentials the signal was input to a 100 x amplifier (Tektronix 122) with a 0.2-1000 Hz bandwidth and was stored on an FM tape channel. To analyze generator and resting potentials the signal was input to a 100 X amplifier with a DC to 3 kHz bandwidth and stored on another FM tape channel. The signal from the round-window electrode was fed into a 1000 X

amplifier (Tektronix 122) with a 80-1000 Hz bandwidth. All channels were displayed on oscil-

loscopes and could be fed to an audio monitor for on-line observation.

Other channels of the tape recorder stored the system sync pulse, the stimulus waveform, the modulating waveform, the experimenter’s voice, and the frequency of modulation and average stimulus intensity as encoded by a microcomputer (Rockwell AIM 65). Further data analyses were

performed on one of two different systems. One system has been previously described in detail by Smith and Brachman (1980a). The other system

utilized a PDP-11/34 minicomputer. In this case, the output of a level discriminator was passed

through a microcomputer interface (Brachman As- soc.) and the time of arrival of each spike was stored on disc with an 8 ps accuracy. PSTHs and Fourier analyses were obtained off-line.

Since micropipettes were used as recording electrodes it was necessary to distinguish primary- like units of the VCN from incoming auditory- nerve fibers (Kiang, 1965). Primarylike units had biphasic spike waveforms and were held for long recording times in contrast to auditory-nerve fibers which had monophasic spike waveforms and were held for shorter periods. All auditory-nerve fibers of the present study were of the low threshold/high spontaneous group (Liberman, 1978) and were recorded in separate experiments from the VCN units using the different surgical approach men- tioned above.

To get a quantitative measure of the AM re- sponses a Fourier analysis was performed on PSTHs during the AM portions of stimulation. This provided the average value and fundamental- frequency component of the responses to AM. As mentioned in the Introduction, cochlear nucleus units encode AM with high fidelity so that the fundamental-frequency component is a good mea- sure of the synchronous response to AM. The ratio of the fundamental-frequency response to the average response gives the percent modulation of the response. In the present report, the strength of the response to AM is given as modulation gain in dB:

Modulation gain

= 20 x log,,, % modulation of the response ! % modulation of the stimulus

103

This particular gain measure was chosen for the

following reasons. First, the percent modulation of the response may reflect a neural signal-to-noise ratio that is important in later stages of the central auditory system. Specifically, the fundamental-

frequency response is a signal which the next stage of the system may be designed to detect against a biologically noisy background. This signal rides on the average response which has a certain noise level associated with it. The higher the average response, the larger its random fluctuations rela- tive to the signal. Thus, the gain will increase with the relative strength of the signal available to the next stage of the system. Second, the gain scale involves normalization for the percent modulation of the stimulus. This allows quantitative compari-

son of the strength of the synchronous response to AM in studies where different depths of modula- tion of the stimulus were used. Third, this gain

scale allows for quantitative comparison of the present results to previous work.

Histology

Upon completion of the neurophysiological portion of an experiment, the cochlear nucleus

was prepared for light microscopy using the fol- lowing procedure. Animals were serially perfused intracardially with a dilute fixative, 1% parafor- maldehyde, 1% glutaraldehyde in 0.1 M Sorensen’s phosphate buffer at pH 7.4; followed by a con- centrated fixative, 2% paraformaldehyde, 2%

glutaraldehyde in the same buffer (J. Robson, personal communication). The right cochlear nucleus was then dissected free and placed in concentrated fixative overnight at 4” C. The tissue was then sectioned at 60 or 100 pm on a vibra- tome with the remaining fixative in the vibratome reservoir. Following a buffer wash, the free-float- ing sections were preincubated for 20 min in 0.033% DAB in 0.1 M Sorensen’s phosphate buffer at pH 7.2. Then they were reacted for 20 min with

H,O, which was added to the preincubation solu- tion to a final concentration of 0.01%. Following a buffer wash, the sections were viewed with a light microscope by temporarily placing them on glass slides in a glycerine/buffer solution. Next the sections were mounted on gelatin-coated slides with an alcohol-gelatin solution and allowed to air dry for 12 h at 37°C. Finally, the sections were

dehydrated through ethanol solutions, cleared in

xylene, rehydrated, stained with cresyl violet, de- hydrated and coverslipped with Permount. Ob- servations and photomicrographs were made with

Nikon Biophot or Optiphot microscopes.

Results

Ventral cochlear nucleus recording sites Responses to AM were studied in 103 single

units localized to intermediate regions of the VCN. Intermediate regions of the VCN include the

posterior AVCN, the interstitial nucleus (IN) and the anterior PVCN as shown by the shaded area of Fig. 1. Our AM studies were initiated here because preliminary recordings indicated that this region contains cells that show enhanced re-

sponses to AM. The rostra1 pole of the AVCN was not included. It contains large spherical/ bushy cells (Osen, 1969; Brawer et al., 1974) which prob- ably relay information to higher centers with a

: DCN

‘\. -*.*

COCHLEAR NUCLEUS

Fig. 1. The shaded area shows the location of the recording sites for the 103 units of this study. The extent of the shaded

area was determined by correlating in viva electrode place-

ments with the scale model of the cochlear nucleus and tem-

poral bone (N = 91) reported in Frisina et al. (1982). or by HRP injections (N = 12) (Frisina. 1983).

104

minimum of processing. The caudal pole of the PVCN, which contains the octopus cell region (Kane, 1973; Brawer et al., 1974) was also not included in the present investigation. The func-

tional implications of these anatomical exclusions are that primarylike units with large prepotentials and onset units with no sustained activity were not included in the present study.

Hierurchical relation between AM encoding and

pure-tone responses-Qualitative analyses

The results presented in this section were ob-

tained using a 100 ms tone burst at a unit’s CF as the stimulus. The amplitude of the stimulus re- mained constant during the first 50 ms and was sinusoidally amplitude-modulated at 150 Hz dur-

ing the last 50 ms. In some cases the modulation interval included a 6 dB increment in intensity to allow comparison of responses to sinusoidal and step modulations. Initial studies utilized modula- tion depths of either 30% or 50%. These values had been shown previously to provide vigorous response modulation in the auditory nerve (Smith and Brachman, 1980a; 1980b; Palmer, 1982) and cochlear nucleus (Moller, 1972; Vater, 1982). The

average intensity of the stimulus was varied for each block of 100 stimulus presentations in 5 or 10 dB steps. Since the stimulus had both constant-in- tensity and AM portions a unit’s pure-tone re- sponse properties could be directly compared to its steady-state responses to AM.

Responses of all types of units in intermediate regions of the VCN were recorded but chopper units were encountered most frequently and studied most extensively. Since the initial dis- covery of chopper units (Pfeiffer. 1966) this cate- gory has been further subdivided into chop-S, chop-T and chop-l categories in the AVCN (Bourk, 1976). Of the 52 chopper units encoun- tered in the present study only 1 was classified as chop-T and 1 as chop-l on the basis of PSTH response patterns. It is possible that a few chop-T units have been misclassified as chop-S units since an additional test (measurement of interspike in- tervals as a function of time of occurrence of spikes, Bourk, 1976) was not used here to dis- tinguish between these two unit types. In any case, to simplify matters, the word ‘chopper’ will be used in the following discussion to refer to all

&

m ‘: . . l6dB :

Fig. 2. PSTHs of the responses of two chopper units to stimuli

containing a constant-intensity and an amplitude-modulated

portion. Both units show significant phase-locking to AM at

low intensity levels and are representative of all chopper units.

AM phase-locking at high intensity levels is strong in some

chopper units, such as unit 74, but weak in others. like unit 80.

The stimuli shown below the PSTHs are actual photographs of

the voltage input to the condenser microphone as displayed by

a storage oscilloscope. The dotted rectangles ouline the AM

intervals. Intensity levels in dB re the unit’s threshold are given

in the upper-right corner of each PSTH. Bin width was 640

psec. The positions of the intensity levels on the input-output

functions for these units are given in Fig. 1 of the companion

paper (Frisina et al.. 1990). Unit numbers, CFs and thresholds

(dB SPL) are: Unit 74, 6.3 kHz, 11 dB: Unit 80. 5.5 kHz,

13 dB.

chopper units of the present study. but it should be remembered that the sample consists primarily of the chop-S category.

The AM responses of two representative chopper units are shown in Fig. 2. The PSTH response patterns for both units show the periodic increases and decreases in firing rate (chopping) that occur transiently following the onset of the pure-tone portion of the stimulus. At low intensity levels, all chopper units show a strong synchro- nous response to AM. At high intensity levels, some chopper units show a strong synchronous response, e.g. unit 74. whereas others show a weak synchronous response, e.g. unit 80. Some chopper

4 . . . . . . . . . .

100

Q 00 dS #NIT 128

0 :

lSO,MSEC

. . . . . . . . . .

Fig. 3. PSTHs of the responses of two on-L units. Both units

show strong phase-locking to AM at low and high intensity

levels and are representative of all on-L units sampled. The

strength of the AM response at high levels was more variable

across units than at low levels. The format of this figure is the

same as that of Fig. 2. Bin width was 600 ps. The positions of

the intensity levels on the input-output functions for these

units are given in Fig. 2 of the companion paper (Frisina, et al.,

1990). Unit numbers, CFs and thresholds (dB SPL) are: Unit 130. 12.0 kHz, 33 dB; Unit 128, 7.5 kHz, -2 dB.

units showed synchronous responses to AM at 90 dB above their threshold.

Onset units are another class of units found in the VCN. Two varieties have been classified in the PVCN (Godfrey et al., 1975a). On-I units respond to pure tones with one spike at stimulus onset with no residual activity during the duration of the tone. On-L units respond with one spike at stimulus onset as well as a few spikes during the duration of the tone. The 11 onset units of this study are of the on-L variety.

The responses of two typical on-L units are shown in Fig. 3. The precise timing of the onset spike may be seen, especially at high intensities, during the pure-tone portion of the response. Dur- ing AM, at low intensities, the synchronous re- sponse is quite strong. At high intensity levels, the synchronous response is also strong, but more variable in strength across units. Some on-L units, such as unit 128, show strong synchronous re-

105

sponses up to 80 dB above threshold. At all inten- sity levels, the synchronous responses appear to be greater, and the widths of each individual AM

response peak narrower, for the on-L units com- pared to chopper units.

A total of 18 primarylike-with-notch (Pri-N) units were encountered in the present investiga- tion. At virtually all intensity levels, p&N units

(Kiang et al., 1973) show a transient decrease in firing rate (notch) just after the initial onset peak. Their PSTH response patterns are otherwise simi-

lar to those of auditory-nerve fibers. Representative responses for pri-N units are

shown in Fig. 4. A l-2 ms notch in the response

pattern may be seen after the onset of the re- sponse to the pure-tone portion of the stimulus.

At low intensity levels, a strong synchronous re- sponse to AM occurs in all p&N units. At high intensity levels, measurable synchronous responses to AM occur in most pri-N units but they are

0 0 .

. 1SOJASEC

.

*

. . . . . . . . . .

0 . :

tS0 MSEC .

Fig. 4. PSTHs of the responses of two pri-N units. The units

are representative of all pri-N units and show a strong

phase-locked response to AM at low intensity levels. The

phase-locked response at high intensity levels is rather weak.

The format of this figure is the same as that of Fig. 2. Bin width was 600 ps. The positions of the intensity levels on the

input-output functions for these units are given in Fig. 3 of the

companion paper (Frisina, et al., 1990). Unit numbers, CFs

and thresholds (dB SPL) are: Unit 122, 14.0 kHz, 25 dB; Unit 159, 15.4 kHz, 15 dB.

106

Fig. 5. PSTHs of the responses of two pri-B units. At low

intensity levels. the phase-locked responses of pri-B units were

generally strong as shown for unit 173. However, a few units

showed somewhat weak phase-locking at low intensity as ex-

emplified by unit 162. At high intensity levels little phase-lock-

ing was apparent. The format of this figure is the same as that

of Fig. 2. Bin width was 600 ps. The positions of the intensity

levels on the input-output functions for these units are given in

Fig. 4 of the companion paper (Frisina et al., 1990). Unit

numbers, CFs and thresholds (dB SPL) are: Unit 173, 7.8 kHz.

- 7 dB; Unit 162.15.2 kHz, 20 dB.

rather weak. At all intensity levels. the synchro- nous responses to AM of pri-N units are less than

those of onset and chopper units. The other major unit type encountered in inter-

mediate regions of the VCN had a primarylike PSTH response pattern. Primarylike units were so named because their PSTH response patterns to pure tones closely resemble those of auditory-nerve fibers (Pfeiffer, 1966). Thirteen of the primarylike units of the present study had biphasic spike waveforms, and as discussed above under Meth- ods, were classified as VCN units (Pri-B).

The responses of two pri-B units are displayed in Fig. 5. The responses to the pure-tone portion of the stimulus resemble those of primary fibers. During the AM portion of the response at low intensities, most pri-B units show strong syn- chrony as seen for unit 173. A few units show weaker synchrony to AM at low intensities as was observed for unit 162. At high intensity levels, very little synchrony to AM was detectable. These

responses to AM were similar to those seen for the auditory-nerve fibers of the present study (not shown). At all intensities, the AM synchronous responses were weaker than those seen for onset and chopper units.

Hierarchical relation between AM encoding and

pure-tone responses-Quantitative unalvses

In the previous section it was shown that the

strength of synchronous responses to AM, particu-

larly at high intensities, varies among VCN units. For example, some chopper units showed strong

synchronous responses to AM at high intensities (Fig. 2a), whereas others showed weaker syn- chrony (Fig. 2b). To obtain a clearer under- standing and quantitative description of this varia-

bility, AM gain at 150 Hz was measured at 50 dB above threshold for chopper units. The results are shown in Fig. 6 in histogram form. The distribu- tion of response gains is unimodal suggesting that chopper units can be viewed as a single class of units with varying abilities to encode AM. In addition, the units vary in terms of the AM frequency producing maximum response gains, as - is presented below.

According to the qualitative findings of the previous section. a relationship exists between a unit’s PSTH response pattern and its ability to

,6- CHOPPERS 50 dB re threshold

- N=4B 14 -

4-

/ -14 -10 -6 -2 +2 +6

MODULATION GAIN (dB)

Fig. 6. Histogram of the number of chopper units with a particular modulation gain at a stimulus intensity level of 50

dB re each unit’s threshold. The AM frequency was 150 Hz

and histogram bin width is 4 dB.

107

TABLE I

MODULATION GAIN FOR 150 Hz AMPLITUDE MODULATION

1 Unit type

On-L

(N=9) Chopper

(N=47) Pri-N

(N=16) Pri-B

(N=13)

2 3 Mean gain SD of gain

(dB)> (dB),

10 dB re 10 dB re threshold threshold

+ 9.0 3.0

+6.1 3.7

+ 7.7 2.6

+5.3 4.1

4 Mean gain

(dB). 50 dB re threshold

+ 2.7

-7.5

- 9.4

- 13.8

5

SD of gain

(dB), 50 dB re

threshold

7.2

7.4

4.9

6.9

6

Change in SD,

low to high

intensity

i4.2

+3.7

+ 2.3

+ 2.8

SD = standard deviation.

encode AM. On-L units showed the strongest re- sponses; chopper responses were not as strong as on-L units but exceeded those of pri-N units; pri-B units showed the weakest responses which are similar to those of auditory-nerve fibers. Thus, the units with the most precisely timed onset responses (on-L and chopper) show the strongest responses to AM. The validity of these observa- tions was tested quantitatively by comparing mod- ulation gains for 150 Hz at low and high intensi- ties for the four types of VCN units. These results are displayed in Table I and it is apparent (col- umns 2 and 4) that the qualitative observations are supported. On-L units show the highest gains, followed by chopper, pri-N and pri-B units, re-

spectively. Standard deviations of the modulation gains

were similar for the VCN unit types (columns 3 and 5). Note however, that an increase in the standard deviations of the gains occurs as the intensity level is raised (column 6). This suggests that some parameter influencing variability is al- tered at high intensity levels, thus increasing the variability of the responses to 150 Hz AM. The increase in variability of the gains at high intensity levels may also be partly a consequence of the nature of the gain scale. The gain scale is logarith- mic, and since the gain is less at high intensity levels, a given amount of noise in the fundamen- tal-frequency response at high intensities causes larger changes in gain than it would at low inten- sity levels.

Transformation of inputs by VCN cells-Enhance- ment of 1.50 Hz AM

A comparison of the AM responses for VCN units with data from the auditory nerve provides information about neural transformations in the VCN. For 150 Hz AM, quantitative analyses are displayed in Table II. The data in columns 2 and 3 indicate that all four VCN unit types amplify the AM information they receive from the auditory nerve. Amplification is defined as the mean gain of a VCN unit type (as in Table I) minus the mean gain for auditory-nerve fibers under comparable stimulus conditions. These auditory-nerve mean data were +2.4 dB at 10 dB re threshold and -16.8 dB at 50 dB re threshold (N = 25). For on-L, chopper and pri-N units the amplification is

TABLE II

AMPLIFICATION OF 150 Hz AMPLITUDE MOD-

ULATION

1 2 3

Unit type Amplification (dB), Amplification (dB),

10 dB re threshold 50 dB re threshold

On-L

(N=9) f6.6 + 19.5

Chopper (N=47) + 3.7 +9.3

Pri-N

(N=16) +5.3 + 7.4

Pri-B

(N=13) + 2.9 + 3.0

108

TABLE III

RESPONSES TO 150 Hz AMPLITUDE MODULATION AT

50 dB re THRESHOLD

Unit type Mean fundamental-

frequency

response (spikes/s)

Mean average

response (spikes/s)

On-L

(N=4) 120 139

Chopper

(N=29) 31 179

Pri-N

(N=15) 17 136

Pri-B

(N=ll) 16 158

8th nerve *

(N=37) 13 217

* Some units are unpublished data courtesy of M.L. Brach-

man. Depth of modulation = 35%.

greater at high intensities than at low intensities. At high intensity levels, the amplification is fairly

large for on-L (19.5 dB), chopper (9.3 dB) and pri-N (7.4 dB) units. Pri-B units show about the

same amount of amplification (3 dB) at low and high intensity levels.

Components of the response gains of the VCN unit types at high intensity levels were investigated

further to determine how the amplification of the auditory-nerve input is achieved. Recall that the fundamental-frequency response was defined as a measure of the synchronous response to the AM frequency. The average response was introduced

above as a measure of the steady-state firing rate of a unit. Increases in fundamental-frequency re- sponse increase response gain as do decreases in average response. The mean fundamental- frequency response (column 2) and mean average response (column 3) during AM are tabulated for the four VCN unit types and for auditory-nerve fibers in Table III. It can be seen that the various VCN unit types each utilize varying strategies for amplifying AM information. On-L units increase the fundamental-frequency response by almost an order of magnitude and have an average response that is reduced by 36%. Chopper units have a fundamental-frequency response that is a little more than twice as large as that of auditory-nerve fibers and an average response that is reduced by

18%. Pri-N units have a fundamental-frequency response that is about the same as the auditory nerve but the average response is reduced by 37%. Pri-B units also show approximately the same fundamental-frequency response as auditory-nerve fibers and a lowering of their average response by 27%. Thus, all the VCN unit types lower their average firing rates during AM relative to the auditory nerve, but only on-L and chopper units

show large increases in the fundamental-frequency

response.

AM tuning at high sound leuels

The data presented above, utilized a single modulation frequency as a basis for comparing different units’ AM encoding abilities. It was found that synchronous responses to 150 Hz AM show a considerable amount of variability at high inten- sity levels. Since it was found previously that some cochlear nucleus units are tuned to different AM frequencies ranging from 50-600 Hz (Msller, 1972; 1974; Vater, 1982), this variability may re- sult from some units being tuned to frequencies other than 150 Hz. This hypothesis was tested for

the four unit types of the present study by measur- ing the synchronous response to AM as the mod- ulation frequency was varied. This allowed de- termination of a unit’s best AM frequency. The stimulus was the same as that used to study 150 Hz AM except that the AM was started at stimu- lus onset and was always at a depth of 35%. Fourier analyses were performed during the last 50 ms of the 100 ms stimulus so that the effects of

rapid and short-term adaptation had subsided. Modulation gain as a function of AM frequency

is plotted in Fig. 7 for three representative audi- tory-nerve fibers. To be consistent with previous research, this representation will be referred to as a gain function (Merller, 1972). The functions tend to have ill-defined peaks that occur at very low gain levels (mostly below - 10 dB) as indicated by the dot-dashed line. Data such as these demon- strate that auditory-nerve fibers are not AM re-

sponsive at high intensities. As above, chopper units were the VCN unit

type affording the most extensive sample. At high intensities (50 dB re threshold) different chopper units were found to be tuned to different AM frequencies. Some representative findings are

109

UDITORY NERVE

- UNIT MB-4 o.....o UNIT MS-9 A---. UNIT M4-2

1

i 8 -10 I .-_-_-_-._._.__-.___.-._._.-._.-.-.-.-,~.-.-.-._._. s

I:~ e : , I I I

10 100 1000

MODULATION FREOUENCY (Hz)

Fig. 7. Gain functions for auditory-nerve fibers at 50 dB re each unit’s threshold. The functions are noisy and do not show

clear maxima, The dot-dashed line shows the level of maxi-

mum responses for most auditory-nerve fibers. Unit numbers,

CFs and thresholds (dB SPL) are: Unit M8-4, 4.7 kHz, 10 dB;

Unit M8-9, 4.8 kHz, 13 dB; Unit M4-2, 15.4 kHz, 14 dB.

shown in Fig. 8. The gain functions show clear peaks at a gain of approximately 0 dB, i.e. where the percent modulation of the response equals that

of the stimulus. In contrast, the dashed line at - 10 dB indicates the maximum gain found for

15 - I I

CHOPPERS

- UNIT 131 ,D- o . . . . . . o UNIT 114

a A---+ UNIT 133

0 5- ,.9

10 100 loo0

MoDuATK)F( FREolmlcY (W

Fig. 8. Gain functions showing modulation gain vs modulation frequency for chopper units at 50 dB re each unit’s threshold. The chopper units are tuned to different modulation frequen-

cies and the maximum gains are at approximately 0 dB, which is 10 dB greater than auditory-nerve fibers under comparable stimulus conditions (dot-dashed line). Note that 0 dB is the gain at which the depth of modulation in the response is equal to that of the stimulus. Unit numbers. CFs and thresholds (dB SPL) are: Unit 131, 9.9 kHz, 9 dB; Unit 114. 11.9 kHz, -2

dB; Unit 133, 12.9 kHz, 9 dB.

I

ON-L

_ UNIT 141 10 - ~.....a UNIT 130

-20 - I I

10 100 1000

MODULATION FREOUENCY 0-k)

Fig. 9. Gain functions for on-L units at 50 dB re each unit’s

threshold. The functions are broadly tuned and much greater

in magnitude than the peak gains of auditory-nerve fibers at

almost all frequencies (dot-dashed line). Unit numbers, CFs

and thresholds (dB SPL) are: Unit 141, 5.0 kHz, 14 dB; Unit 130.12.0 kHz, 33 dB.

auditory-nerve fibers as shown in Fig. 7. Gain functions obtained at 50 dB above

threshold for two on-L units are plotted in Fig. 9. The peak gains clearly exceed those of auditory-nerve fibers, and in comparison to the functions in the previous figure, appear to exceed those of chopper units, which is consistent with the results at 150 Hz. The functions also seem to

be more broadly tuned than those of chopper units, but this conclusion is tentative since only

two complete gain functions for on-L units were obtained in the present study.

Gain functions measured at 50 dB above threshold for several pri-N units are plotted in Fig. 10. The peak gains are less than those seen for on-L and chopper units, and in one case (unit 150) the function has several shallow peaks and no prominent maximum. The results for pri-B units shown in Fig. 11 are similar to the pri-N data. Two of the three functions are noisy and lack clearly-defined maxima. Thus, the primarylike unit types show less AM gain than on-L and chopper units which is consistent with the 150 Hz results.

Transformation of inputs by VCN cells-Enhance- ment at high sound levels

Quantitative analysis of the findings of Figs. 7-11 concerning AM amplification of eighth-nerve

110

15 t PM-N

t

- UNIT150 10 o.....o UNIT 152

ii t--A UNIT 161

L.- ~ ~~~._~ .A.-- .~~ ~~. 1 L- .~I____ -LA 10 100 1000 10 100 1000

MODULATION FREQUENCY (Hz) MODULATION FREWENCY (Hz)

Fig. 10. Gain functions for pri-N units at 50 dB re each unit’s

threshold. The functions have peaks that are less prominent

than those of chopper units and on-L units (Figs. 8-9). The

gains tend to be slightly above those of auditory-nerve fibers

(dot-dashed line). Unit numbers. CFs and thresholds (dB SPL)

are: Unit 150, 2.7 kHz, - 1 dB; Unit 152. 4.5 kHz. 23 dB: Unit

Fig. 11. Gain functions for pri-B units 50 dB re each unit’s

threshold. The gains are similar to those of pri-N umts and

slightly greater than those of auditory-nerve fibers (dot-dashed

line). Unit numbers, CFs and thresholds (dB SPL) are: Unit

165. 4.6 kHz. 18 dB; Unit 146, 1.2 kHz, 8 dB: Unit 171, 14.7

kHz, 29 dB. 161. 15.0 kHz. 10 dB.

inputs is summarized in Table IV. The mean gains at the peak of the gain function for each VCN unit type are presented in column 2. It may be seen that the rank ordering of the four unit types found so far in this report is fairly well preserved here (e.g. compare column 2 with Table I, column

4). On-L units show the highest gains, followed by chopper units, the two kinds of primarylike units, and finally the auditory-nerve fibers. In the latter case. no clear peak was seen on the gain functions,

so the highest gain was taken for the present quantitative computational purposes. The amplifi- cation of the auditory-nerve input is computed in column 4. Again, the gain function results are

similar to the previous findings of this report (e.g. compare column 4 with Table II, column 3).

The standard deviations of the peaks of the gain functions for the VCN units and auditory-nerve fibers are given in Table IV (col- umn 3). They are smaller than for the standard

TABLE IV

MAGNITUDE AND FREQUENCY OF GAIN-FUNCTION PEAKS AT 50 dB re THRESHOLD

1 2

Unit type Mean gain (dB)

On-L

(N=2) + 1.5

Chopper

( N = 20) -0.6

Pri-N

(N=5) -6.5

Pri-B

(N=7) -4.5

8th nerve

(N=26) - 10.6

SD = standard deviation.

3

SD of gain (dB)

_

4.4

3.0

3.2

2.3

4 5

Amplification of Range of peak

8th nerve input frequencies

(dB) (Hz)

+ 18.1 180-240

+ 10.0 80-520

+4.1 120-380

i6.1 80-700

X 80-800

6

Geometric mean of

peak frequencies

(Hz)

209

200

190

253

370

111

deviations of the gains for 150 Hz AM at 50 dB above threshold (Table I, column 5) and are com- parable to those for 150 Hz AM at 10 dB above threshold (Table I, column 3). Hence the frequency variation in gain-function peaks appears to be responsible for some of the large variations in response gain at 150 Hz, 50 dB re threshold as

hypothesized above.

AM tuning properties change with sound level

In the last section the effects of varying AM frequency were investigated by measuring gain functions for each cochlear nucleus unit type at 50

dB above threshold and comparing them to the responses of auditory-nerve fibers. In the present section, this analysis is extended to several differ-

ent intensity levels. Data for two representative chopper units are plotted in Fig. 12. Modulation

gain is plotted versus AM frequency, with average intensity as a parameter. At low intensities the functions mimic those of a lowpass filter. At high intensities the gain functions resemble those of a

bandpass filter. The shape changes because a large drop in gain with intensity level occurs at low modulation frequencies, while the smaller drops occur near the gain-function peaks and at the higher frequencies.

Data for the same two chopper units are plotted in a 3-dimensional format in Fig. 13. The actual data points lie at the intersections of the thick lines on the surface. The thin lines were added to aid in visualizing the height of the surface. A gain function at a given intensity level may be obtained

by making a vertical slice through the surface parallel to the modulation-frequency axis. Con- sistent with the results of the previous section, at high intensity levels the surfaces take on the shape of a bandpass filter. At low intensity levels the surfaces become lowpass in shape. To see how the gain changes with intensity at a single AM frequency, a vertical slice parallel to the intensity- level axis can be made. At low AM frequencies the gain falls rapidly with intensity level. At the peak frequency the drop in gain with intensity level is minimal. At high AM frequencies the decrease in gain with intensity is also small since the gains at low intensities are small. To obtain an iso-re- sponse contour a horizontal slice can be made through the surface. To be consistent with previ-

CHOPPER

10 100 1000

MOLWLATION FREOUENCY (Hz)

-15 3.

t -20 5o I

10 100 1000

MODULATION FREOUENCY (Hz)

Fig. 12. Gain functions at several intensities for two repre-

sentative chopper units. The data are the same as Fig. 13

except that here a two-dimensional format has been used. The

numbers to the left of each function indicate intensity level (dB

re each unit’s threshold). Unit numbers, CFs and thresholds

(dB SPL) are: Unit 131. 9.9 kHz, 9 dB; Unit 134, 12.6 kHz, 19

dB.

ously used terminology, the surface will hence- forth be called a ‘gain surface’.

Comparison of Figs. 12 and 13 shows the rela- tive merits of the 2- and 3-dimensional data pre- sentation formats. The 3-dimensional plot facili- tates comparisons between the four VCN unit types and auditory-nerve fibers as described be- low. This may be due to the fact that the 3-dimen- sional gain surface delineates a volume below it that the viewer tends to perceive as a unit’s overall ability to encode AM. The 2-dimensional format has the advantage that quantitative data are more

Fig. 13. Three-dimensional gain surfaces for chopper units

showing modulation gain as a function of intensity level and

AM frequency. The gain is highest at low intensity levels and

the surface is lowpass in nature. At high intensities the surface

is bandpass in nature with the peak showing a high gain. Upper surface-Unit 131; Lower surface-Unit 134.

easily extracted from it. For example, parts of the gain surface may be hidden from view and the data in these regions are not visible.

Fig. 14 shows group data for chopper units at 10 and 50 dB above threshold. Each gain function is normalized to its peak frequency and peak gain. The plots give an indication of the variability of the shapes of the gain functions in the sample. The main findings of Figs. 12 and 13 can also be seen here. At low intensity levels the functions are lowpass in nature and at high intensity levels the functions take on more of a bandpass shape.

Two gain surfaces were measured for on-L units as displayed In Fig. 15. The responses at all frequencies and intensity levels tend to be greater than those of chopper units but the lowpass shape of the gain surfaces at low intensity levels and the

bandpass shape at high intensity levels are still

present. Data for two representative pri-N units are shown in Fig. 16. The responses of these units

are less than those of on-L and chopper units

especially at high intensity levels. In addition, the shape of the gain surface is somewhat different. The lowpass characteristic at low intensity levels is

present but the bandpass characteristic at high intensity levels tends to be less prominent and responses are more noisy. Data for pri-B units are

r10t 1

CHOPPERS

D 10 dB re threshold

4 +5 r N-1g z

0.1 1.0 10

+10

1 S

50dB ra threshold

z +5

L .___..

0.1 10 10

NORMALIZED MODULATION FREQUENCY

Fig. 14. Normalized gain functions for a group of chopper

units. At 10 dB re threshold the functions are lowpass in

nature. At 50 dB re threshold the bandpass nature of the

functions is evident.

113

Fig. 15. Gain surfaces for on-L units. The gain is high at low

intensity levels and the surface is lowpass in nature. At high

intensities the surface is bandpass in nature and the gains are

high. Upper surface-Unit 130. CF=12.0 kHz, threshold = 33

dB SPL; Lower surface-Unit 141, CF= 5.0 kHz, threshold = 14

dB SPL.

similar to those of pri-N units, as shown in Fig. 17.

The responses of two representative auditory- nerve fibers are shown in Fig. 18. The response gains tend to be less than those of VCN units at all points on the surface. At low intensity levels the now-familiar lowpass characteristic is present. This finding agrees with previous studies in rat (Moller, 1976a) and guinea pig (Palmer, 1982). At high intensity levels the gain is quite low and there does not appear to be a prominent bandpass

characteristic in contrast to most of the VCN units.

Transformation of inputs by VCN cells-Overall enhancement

Gain surfaces for a typical auditory-nerve fiber

(Fig. 18) and each of the four VCN unit types (Figs. 13, 15-17) were overplotted to summarize the transformation of ascending inputs by VCN

cells. The differences between the gain surface of a VCN unit and auditory-nerve fiber can be viewed

as a graphical approximation to the AM transfer

Fig. 16. Gain surfaces for pri-N units. At low intensities the

gains are high and the surface is lowpass in nature. At high

intensities the gains are low and the bandpass characteristic is

not prominent. Upper surface-Unit 160. CF= 17.1 kHz.

threshold =16 dB SPL; Lower surface-Unit 159. CF=15.4

kHz. threshold = 15 dB SPL.

114

Fig. 17. Gain surfaces for pri-B units. At low intensities the

gain> are high and the surface lowpass in nature. At high

intensities the gains are lower and the bandpass characteristic

1s not prominent. Upper surface-Unit 162, CF=15.2 kHz.

threshold = 20 dB SPL: Lower surface-Unit 172. CF=13.1

kHz. threshold = 24 dB SPL.

function for a VCN unit. Gain-surface overplots for an on-L and chopper unit are displayed in Fig. 19. The differences between the surfaces are grea- test at high intensity levels indicating that the most enhancement occurs there. Similar plots for a pri-N and pri-B unit are given in Fig. 20. In general, the differences between their gain surfaces and that of the auditory-nerve fiber are less than for the on-L and chopper units.

Lastly, the data presented in this report indi- cate that one of the main differences in the encod- ing of AM, in auditory-nerve fibers and VCN units, corresponds to the bandpass characteristic

that is prominent at high intensity levels. The lowpass characteristic. dominant at low intensity levels, is similar for all unit types and appears to

drop out at high intensity levels. The relative strength of the bandpass characteristic in each of

the four VCN unit types determines the effective- ness of each unit type in the encoding of AM at

high sound levels.

Addition& anu!vses of‘ chopper AM responses

The natural chopping that occurs at stimulus onset for chopper units is a prominent feature of

Fig. 18. Gain surfaces for audltory-nerve fibers. At low mtensi-

ties the gains are high and the surface lowpasa in nature. At

high intensities the gains are IOU and the surface relatively flat. Upper surface-Unit MR-6. CF= 6.5 kHz. threshold = 2 dB

SPL; Lower surface-Unit M8-2. CF = 6.5 kHz. threshold = 5

dB SPL.

115

CHOPPERA

Fig. 19. Gain surface overplots for a chopper (Unit 131) and

on-L unit (Unit 130). The dotted surface is that of a typical

auditory-nerve fiber (Unit M8-6). The differences between the

auditory nerve and cochlear nucleus surfaces are greatest at

high intensity levels.

their time-domain responses to tone bursts. In PSTHs, the natural chopping bears a strong re- semblence to synchronous responses to AM (e.g. Fig. 2). It is possible that the synaptic or cellular mechanisms responsible for the natural chopping could also be responsible for AM encoding. If this

were true, one would expect the frequency of the gain-function peak to be related to the natural chopping frequency. This was not found to be the case for units of the present study as is shown in Fig. 21. Here the natural chopping frequency at 50 dB above threshold (average of the first 4 peaks) is plotted vs. the peak frequency of the gain function

at 50 dB above threshold. Although the natural chopping frequencies (range: 170-700 Hz) and gain-function peak frequencies (range: 80-520 Hz) have similar ranges, there appears to be only a weak correlation, if any, between the two mea- sures. This lack of correlation may be due to the fact that the AM responses are a steady-state measure whereas the natural chopping is a tran- sient phenomenon. As described in the next sec- tion. striking interactions can occur between the

natural chopping responses and transient re- sponses to AM. Alternatively, the lack of correla-

tion may be due to testing AM responsiveness with only one phase of the AM signal. Varying the

Fig. 20. Gain surface overplots for a pri-N (Unit 160) and a

pri-B (Unit 162). The dotted surface is the same as that of Fig.

19. The differences between the surfaces are not as great as

seen for the chopper and on-L units of the previous figure.

NATURAL CHOPPING FREQUENCY (Hz)

21. Natural chopping frequency vs gain-function peak

frequency at 50 dB re threshold. The natural choppmg

frequency is the average for the first 4 peaks of the chopping

response to pure-tone stimulation. The diagonal line represents

equality between the natural chopping frequency and the best

frequency for AM encoding.

AM phase relative to stimulus onset might alter the responsiveness of a chopper unit to AM. How- ever, note that in Fig. 21 the paucity of data

points above the diagonal suggests that the gain- function peak frequency tends to be less than the natural chopping frequency.

The effects of varying AM frequency on the responses of two representative chopper units are shown in the form of PSTHs in Figs. 22 and 23. In this part of the study the AM was turned on at

stimulus onset, allowing any interactions between the transient response to AM and natural chop- ping responses to be observed. At high intensity levels, regardless of the AM frequency, the natural chopping is relatively unaffected by the AM. At low intensity levels the interactions depend on the frequency and phase of AM relative to the natural chopping frequency. When the AM frequency is less than the natural chopping frequency, natural chopping occurs on each response cycle to the AM. When the AM frequency is near the natural chopping frequency, the natural response is en- hanced. When the AM frequency is greater than the natural chopping frequency, the natural chop- ping occurs as though the stimulus were an un- modulated tone burst. The observed interaction

between the natural and driven chopping re- sponses at low intensity levels may be an im-

portant aspect of the mechanism for the encoding of sounds whose amplitudes are modulated from the outset.

Discussion

AM encoding--Auditor?, nerve The steady-state encoding of AM for low-

threshold. high-spontaneous activity auditory- nerve fibers is shown in Fig. 18. The 3-dimen- sional plot shows how the modulation gain changes for systematic variations in intensity level over a 70 dB range and for variations in AM frequency over a range of 40-800 Hz. If one views the gain surface as a series of isointensity functions, the

functions are lowpass in shape at low intensity levels and are at a low level and fairly flat and noisy at high intensity levels. Viewing the gain

surface as a series of isofrequency functions is also enlightening. At low frequencies the gain drops dramatically with intensity level. The drop in re- sponse at high frequencies is less dramatic since here the gain at low intensities starts off at a low level.

The findings in Fig. 18 are consistent with the limited results of previous studies in other species. Isointensity functions at low intensity levels re- semble those of a lowpass filter in rat (Moller.

1976a) chinchilla (Javel. 1980) guinea pig (Palmer, 1982) and cat (Joris and Yin, 1988). The decrease in the synchronous response as AM frequency increases has been attributed to the movement of the energy of the stimulus sidebands out of the response area of a fiber as the AM frequency is increased. Recall that a sinusoidally amplitude- modulated tone contains energy at three frequen- cies: the carrier. the carrier plus the modulation

frequency, and the carrier minus the modulation frequency. The greater the percent modulation, the greater the amplitude of the two sidebands.

Palmer (1982) also measured AM responses at low intensity levels for frequencies of 800-6400 Hz. Local maxima in the gain functions were sometimes seen at these high AM frequencies. The local maxima were only seen in fibers that had low CFs. It was interpreted that these maxima resulted from the reentering of sideband energy into a

117

CHOPPER

0 150 MSEC

80

150 MSEC 0 150 MSE 0 15OMI

0 0 150 MSEl

80 10 dB I

0 0 150 MSEI

80 1OdB

Fig. 22. PSTHs of a chopper showing interactions of responses to AM and the natural chopping response. At high intensities, the

natural chopping is unaffected by the responses to AM. At low intensities interactions can occur. At low AM frequencies. natural

chopping occurs in response to each cycle of the AM stimulus. At AM frequencies near the natural chopping frequency, the natural

chopping response is amplified for about the first 30 ms. At high AM frequencies, the natural chopping response is unaffected since

there does not appear to be much of an AM response. Bin width was 600 ps.

fiber’s response area due to the stimulus spectral changes that occur when the AM frequency ap-

proaches the carrier frequency. When the gain surfaces of Fig. 18 are sliced

parallel to the intensity axis, the isofrequency functions obtained at low frequencies decrease with intensity level. This drop in response with intensity was observed in auditory-nerve fibers of the rat (Moller, 1976a), gerbil (Brachman, 1980; Smith and Brachman, 1977; 1980a), and guinea pig (Evans and Palmer, 1980; Yates, 1981). The decrease in gain is monotonic, in contrast to the amplitude of the fundamental-frequency response which is a nonmonotonic function (Brachman, 1980; Smith and Brachman. 1977). The gain func- tion declines with increases in intensity starting at threshold because both the average and funda- mental-frequency responses initially increase with

intensity. Qualitatively, the decrease of the funda- mental-frequency response appears to reflect the decrease in slope of the steady-state rate-intensity function with intensity. However, quantitatively the steady-state rate-intensity function is not a good predictor of responses to AM (Smith and Brachman, 1980a). It predicts the peak response at intensity levels that are too low and underesti- mates the response at high intensity levels. The onset rate-intensity function, which is a reflection of the firing rate during the initial 1 ms of the response, is a better quantitative predictor of phase-locking to AM than the steady-state rate-in- tensity function (Brachman, 1980; Smith and Brachman, 1980b, c) presumably because AM re- sponsiveness and the onset function both reflect dynamic, as opposed to static, response properties.

However, this description for the encoding of

70 dB UNIT 105

~__._ _._.. ..-... - _

1 150 MSEt

15dB

CHOPPER 80 70 dB

UNIT 105 . ..________ .___ _ . _ -._

9 h

d 0 150 MBEC

8C 70 dB UNIT 105

15dB

0 150 MSEt

Fig. 23. PSTHs for another chopper showing effects of responses to AM on the natural choppine results. The results are similar to . . - those of Fig. 22. Bin width was 600 us.

AM in the auditory nerve was mainly tested at AM frequencies from 150-300 Hz. To determine the validity of predictions from onset responses for other AM frequencies the rise-decay times and time windows over which the onset rate-intensity functions are measured may have to be matched to the modulation frequency. For example, the onset rate-intensity function for predicting the responses to 500 Hz AM may require applying a tone burst with a 1 ms rise time. To accurately track the peak under these conditions the time- window used to measure the onset response may have to be reduced to less than 1 ms because of saturation of the onset response (Smith et al., 1983).

At high AM frequencies, the isofrequency func- tions of Fig. 18 show less of decline with intensity as compared to lower frequencies. These findings are consistent with previous results in guinea pig

auditory nerve for frequencies between 400 and 800 Hz (Yates, 1981; 1982).

AM encoding- Ventrul cochleur nucleus The steady-state encoding of AM in middle

regions of the VCN is summarized in Figs. 12-17. These representations of the data show that a hierarchy exists for the encoding of AM frequen- cies of 20-1000 Hz. On-L units show the largest response gains, followed by chopper, pri-N and pri-B, in that order. Hence. a functionally relevant response property appears to be strongly corre- lated with the PSTH classification scheme in the cochlear nucleus. Quantitative comparisons of the maximum gains for each unit type with those of auditory-nerve fibers show that each type ampli- fies the ascending inputs by an amount com- mensurate with its rank in the hierarchy. This amplification is greatest at high intensity levels.

119

The forms of the cochlear nucleus gain surfaces are different from those of the auditory nerve in certain regards and similar in others. Isointensity functions at low intensity levels are lowpass in

nature for auditory-nerve fibers and all the cochlear nucleus unit types. As intensity level is increased this lowpass characteristic drops out. At high intensity levels the isointensity functions of

auditory-nerve fibers are at a low level and noisy. In contrast, the isointensity functions of chopper

and on-L units resemble a bandpass characteristic with a prominent peak and high gain. The isoin- tensity functions of pri-N and pri-B units are

intermediate between those of chopper and on-L units, and auditory-nerve fibers. The p&N and pri-B isointensity functions are noisy and shallow but their maxima tend to be more prominent and

occur at lower frequencies than those of the audi- tory nerve. Thus, the major difference between the unit types is the degree to which they have the bandpass characteristic that is prominent at high

intensity levels. The gain surfaces can also be viewed as a set of

isofrequency functions. At low frequencies these functions decrease rapidly with increasing inten- sity for auditory-nerve fibers and for all the cochlear nucleus unit types. At intermediate fre- quencies, near the maxima of the gain functions, the drop in response with increasing intensity is rapid for auditory-nerve fibers but is minimal for

on-L and chopper units. Again, the decrease in response of pri-N and pri-B units is intermediate between that of on-L and chopper units, and auditory-nerve fibers. At high modulation fre- quencies, all of the units show minimal changes in gain with increasing intensity.

Comparison of the amplification of the audi- tory-nerve input at high intensities for the gain function peaks (Table IV, column 4) and at 150 Hz (Table II, column 3) indicates that the amplifi- cation of on-L and chopper units is about the same in these two situations. The amplification of pri-N units at the gain-function peak is actually 2.7 dB less than at 150 Hz. That of pri-B units. in contrast, is 3 dB greater for the gain-function peaks compared to that at 150 Hz. It may seem puzzling that the amplifications of on-L. chopper and pri-N units do not increase as is the case for the pri-B units. After all, the results in Table IV

are for the optimal frequency of AM for each unit whereas the results of Table II are for an arbi- trarily chosen AM frequency. An explanation for these perplexing findings can be found in Table IV (columns 5-6). The peaks of the gain functions for on-L, chopper and pri-N have geometric means within *lo Hz of 200 Hz. The geometric mean

for pri-B units is 253 Hz and the auditory nerve

370 Hz. Thus, on-L, chopper and pri-N units tend to be tuned near 150 Hz whereas pri-B and audi- tory-nerve fibers on the average have maxima in

their gain functions at higher AM frequencies. To summarize this analysis, on-L and chopper

units have gain functions with clear peaks (Figs.

8-9) that tend to be located near 150 Hz *. So on the average, there is only a modest increase in gain as one compares the 150 Hz results to the gain- function peak results * *. Pri-N units have gain functions with peaks that also occur near 150 Hz * but that are less well-defined (Fig. 10). Since the functions are shallower than those of on-L and chopper units, comparing the 150 Hz results to the

gain-function peak results gives less of an increase in gain **. The gain functions of pri-B units are relatively flat (Fig. 11) but their maxima tend to occur further away from 150 Hz *. Thus, compar- ing the 150 Hz findings to the gain-function maxi- mum findings gives a larger increase in gain than that of on-L, chopper and pri-N units * *. Audi- tory-nerve fibers have the flattest gain functions of all (Fig. 7) but their maxima tend to be located the furthest away from 150 Hz *. Comparing the 150 Hz amplification to the gain-function maximum amplification allows for a modest increase in gain similar to that of on-L and chopper units * *.

The word ‘specialized’ is often used in the context of central auditory structures to refer to neurons that respond exclusively to one type of stimulus. For example, some neurons in the bat auditory cortex only respond to certain combina- tions of constant-frequency and frequency-mod- ulated tones that the bat normally hears while

echolocating (Suga, 1984). Use of the word ‘spe- cialized’ in this sense would not be appropriate in the ventral cochlear nucleus since neurons that

* See Table IV, columns 5-6.

* * Compare Table I. column 4. with Table IV, column 2.

120

respond to only one type of acoustic stimulus have never been observed. However, if one were to use the word ‘specialized’ to refer to sensory neurons

that preferentially amplify, encode or extract cer-

tain features of their ascending inputs at the ex- pense of other features, then some units of the present study could be considered specialized. Chopper and on-L units showed high gains and prominent peaks in their gain functions at high intensity levels. Pri-N and pri-B showed lower

gains and shallower maxima in their gain func- tions at high intensity levels. Also, the temporal precision of the onset response peak of on-L and chopper units to pure-tone stimuli is greater than that of pri-N and pri-B units. Thus, this dynamic

response characteristic seems to be correlated with a unit’s ability to encode AM, e.g. the greater the temporal precision of the onset response the

greater a unit’s AM encoding ability. In light of these distinctions, on-L and chopper units could be considered specialized for the encoding of AM at high sound levels. Although the emphasis of this study has been on the encoding of modula- tions in sound amplitude in the ventral cochlear nucleus, it is not justified to conclude that the unit types studied are only encoding AM. Rather, they can, for example, sort and encode several parame- ters of the incoming information and send them

on, simultaneously, to higher auditory centers for further, more specialized processing.

The findings of this report increase our knowl-

edge of the neural correlates of the wide, dynamic operating range of the mammalian auditory sys- tem. Some on-L and chopper units showed strong phase-locking to AM over a 90 dB intensity range. If not for limitations on the maximum intensity allowable for stimulation, this range may have been found to have been even greater. When the 25 dB spread of thresholds for on-L and chopper units (Frisina et al., companion paper) is added to the 90 dB range, a 115 dB operating range can be accounted for. Thus, a group of relatively periph- eral sensory neurons can account for most of the operating range of one aspect of the mammalian auditory system.

Lastly, one of the major findings of the present report is difficult to compare with previous inves- tigations since they have not involved a systematic comparison of a unit’s response to simple sounds

with its ability to encode AM. Where limited comparisons can be made the findings of this report are consistent with prior work. For exam-

ple, Moller (1972; 1974a) and Vater (1982) found that some cochlear nucleus units have high peak gains at different modulation frequencies and that their gain functions resemble those of bandpass

filters. In the present study, this occurred at high intensity levels for on-L and chopper units but not

for pri-N and pri-B units. It has also been found previously that at high intensity levels cochlear nucleus units show stronger responses to AM than auditory-nerve fibers (Moller. 1976a). These re-

sults are consistent with the hierarchy of encoding found for VCN units of the present study. Ad- ditionally, it has been found that the response

gains at frequencies near the peak of the gain function diminish very little as average intensity

level increases (Msller, 1974a; 1975a). This is in agreement with our on-L and chopper findings, but not with the pri-N and pri-B results.

Acknowledgements

We gratefully acknowledge the advice and sup- port of Dr. J.J. Zwislocki in all phases of this research. We thank ST. Frisina and Dr. C. Van Doren for graphic arts, and Drs. L. Westerman and D.G. Pelli for computer expertise. This re- search was sponsored by an NSF Grant to RLS and a Biomedical Engineering Grant from the Whitaker Foundation (Mechanicsburg, PA) to RDF.

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