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Auditory neurophonic responses to amplitude-modulated tones: Transfer functions and forward masking
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neurophonic responses to amplitude-modulated Transfer functions and forward masking
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transfer functions or CTF) for carrter frequencies
and response anlplitud~
from 6 to 30 kHz.
Frequency
to: R.L. Snyder, Coleman
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When sustained low-frequency stimuli are presented to the auditory system. sustained ensemble neural responses can be recorded both intracranially from several auditory nuclei as well as extracraniaiiy from the scalp. The term neurophonic has been applied to these responses in order to emphasize both their neural origins and their similarity to the cochlear microphonic (CM) (Weinberger et al.. 1969; Snyder and Schreiner. 1984, 1985). However, these neurophonic responses have longer latencies compared to the CM, more spectrally complex waveforms and display pronounced adaptation.
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Introduction
tories. X71 blSE. University
ib dependent
by forward
functions were saturating
and MTFs
following
functions.
as a function
with similar data for single units and compound
neurophonic:
of this depression
masking
frequencwa varied hctwcen
re\ponae waveforms
rates of recovery
an unmodulated
which have restricted characteristic
( I/O)
responses. Thr AM
and similar
neurophomcs,
and duration
of stimulus level
were‘ alw measured. It was found that the 1/O
Auditory
rates of adaptation,
and one from the
~tin~ulati~~n of the cat cochlea with ~implitud~-rn~)~i-
neurophonic
of the depression is demonstrated
responses arise from fiber populations
compared
with pure-tone
responses. As with the pure-tone
depresston of the probe response. The amount
Response amplitude
following
tones. The carrier frequencies varied between 2 and 30 kHz. The modulation
400 and 3000 Hz. The AM responaea were compared to have d similar
followin, 0 response or t-I;Ri
from the scalp (frequency
- were obtained
tones:
CA
modulation:
Forward
masking
The stimuli usually employed to evoke neurophonic responses consist of low-frequency pure tones (between 100 Hz and 2 kHz) at levels below 90 dB SPL. However, one study has used amplitude modulation of low-frequency tones to evoke a very low-frequency neurophonic (Rees et al.. 1986). The most intensively studied ~leuroph~?ili~ in animals and humans is the one recorded from the scalp - the frequency following response or FFR (Moushegian et al., 197X; Worden and Marsh, 1978; Gardi and Merzenich, 1979: Rees et al., 1986; Greenberg et al.. 1987). In cats the auditory nerve neurophonic (ANN) and FFR have been demonstrated to be neural responses arising primarily from phase-locked activity in the ensemble of auditory nerve fibers (Snyder and Schreiner. 1984, 1985). Forward masking studies have demonstrated that the distribution of fibers which contribute to
” 1987 Elsevier Science Puhlishors H.V. (Biomedical
Division)
80
the pure-tone ANNs and FFRs are spatially highly restricted and that these fibers innervate sectors of the cochlea which are appropriate for the evoking frequencies (Snyder and Schreiner, 1985). The fibers in the most strongly contributing population have characteristic frequencies (CFs) ranging from the stimulus frequency up to approximately one octave above the stimulus frequency. The CF distribution of the fibers which are constructively contributing to the neurophonic depends upon the signal level having a bandwidth of l/3 octave or less at 10 dB above threshold (Snyder and Schreiner, 1985). Thus the neurophonic responses to low-frequency tones reflect the functional properties of auditory nerve fibers which innervate restricted sectors of the apical cochlea and consequently allow examination of their functional integrity. This is in marked distinction to the click and tone evoked action potentials (APs) and auditory brainstem responses (ABRs) which reflect primarily the activity in fibers innervating the cochlear base (Antoli-Candela and Kiang, 1974). In this study we have examined the ANNs and FFRs evoked by ~gh-frequency (> 4 kHzf tones sinusoidally amplitude modulated at frequencies between 200 Hz and 4 kHz. We have found that such amplitude modulated signals produce neurophonic responses which have many properties in common with those produced by low-frequency pure tones: the major frequency components of amplitude-modulated (AM) ANNs and FFRs match harmonics of the modulation or envelope frequency; they have relatively long latencies; and they display adaptation. Using forward masking techniques these AM neurophonics have been shown to arise from fibers whose characteristic frequencies approximate the carrier frequency. Therefore, AM-ANNs and AM-FFRs are presumed to arise as a consequence of a spatial summation of activity in auditory nerve fibers which innervate the cochlear base, which are most sensitive to the carrier frequency, and which phase-lock to the envelope of the stimulus. Thus despite their similarity to low-frequency, pure-tone evoked neurophonics, these AM responses arise from entirely different fiber populations.
Materials
and Methods
Animal surgery~ Experiments were conducted using JO adult cats obtained from a closed breeding colony at the University of California at Davis. The cats were given an otologic examination to ensure healthy external and middle ears. Each animal was initially anesthetized with an intramuscular injection of ketamine (10 mg/kg) and acepromazine (1 mg/kg). A catheter was inserted into the cephalic vein and lactated Ringer’s solution was continuously infused through the catheter. Supplementary doses of sodium pentobarbital were administered via this catheter in order to induce and maintain a surgical level of anesthesia. The scalp was incised and reflected to expose the posterolateral surface of the skull. The external ear canal was incised and a rigid hollow ear bar inserted and sealed. The auditory nerve was exposed via a burr hole made in the occipital bone and aspiration of the lateral cerebellum. Platinum-iridium ball electrodes were placed on either side of the auditory nerve as it exits the internal auditory meatus. Three silver wire electrodes were placed in the skin: one just below the pinna of the stimulated ear. one at the vertex. and one at the nape of the neck. Recording The ANN was recorded differentially using the two platinum-iridium ball electrodes on either side of the auditory nerve as it exits the internal meatus. The FFR was recorded using silver wires; the vertex electrode as the active and an electrode below the stimulated ear as the reference. An electrode through the skin at the nape of the neck served as the ground electrode for both recordings. The responses were initially amplified using a Princeton Applied Electronics battery powered amplifier (Model 113) and led through a second stage amplifier consisting of a 3A9 plug-in amplifier for a Tektronix 565 oscilloscope. The bandpass of the amplifiers was set to 30 Hz-30 kHz. The total gain varied depending upon the signal that was being recorded. The usual amplifications were 20000 X for the ANN and 100~ X for the FFR. The amplified signal was digitized using a 12 bit analogue-to-digital converter operating at a 20 kHz sampling rate and averaged using a
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PDP11/23 computer. The averaged responses were obtained for a variable number of stimulus presentations, usually 100 for the ANN and 500 for the FFR. Stimulus generation Stimuli were generated by a Texas Instruments TMS 32010 ~crocomputer, which synthesized and shaped the signal digitally and transmitted the signal to a 16 bit deglitched DAC. The output rate of the stimulus generation system was varied between 60 and 120 kHz depending upon the carrier frequency of the stimulus and always exceeded the frequency of the upper side band by at least a factor of four. The output of the stimulus generation system was low-pass filtered at 15 or 35 kHz, fed through an attenuator and delivered via an equalizer/amplifier system to a STAX 54 electret headphone encased within an electrically shielded container. The output of this system is flat within it 6 dB variation at the tympanic membrane over the range of 100 Hz-15 kHz. Above 15 kHz the output rolled off at a rate of 10 dB/octave. All stimuli were gated on and off with 5 ms ramps and all stimulus levels are expressed in dB SPL (sound pressure level re: 20 FPa). Results Response
war!efarms Neurophonic responses elicited by pure tones and those elicited by AM tones have a number of features in common. Some of these features can be seen simply by examining the response waveforms. Fig. 1A and B illustrates the response waveform and amplitude spectrum, respectively, of an ANN evoked by an 800 Hz pure tone presented at 44 dB. The basic properties of such neurophonics have been described in detail previously (Snyder and Schreiner, 1984,1985) and need only be summarized briefly here. Among the properties which indicate that these responses were of neural origins are a latency of 3-5 ms, the presence of adaptation in the amplitude of the response, and a complex spectral composition. The latency of the 800 Hz ANN in Fig. 1A was 3.5 ms and the waveform adapts with a short term time constant of approximately 10 ms. The spectral components in this response are seen
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Fig. 1. Auditory nerve neurophonic response to an X00 Hz tone at 44 dB SPL. The waveform is shown above and the amplitude spectrum is shown below. The waveform is plotted in tens of microvolts. The amplitude spectrum is expressed in dB re 0.1 p-v-.
in Fig. 1B and consisted of a series of three harmonic components: a fundamental component which matched the stimulus frequency and its second and third harmonics. The amplitudes of these components for this response were within 6 dB of one another. Fig. 2 illustrates a representative example of an 800 Hz AM-ANN waveform evoked by an 8 kHz carrier 100% amplitude modulated at a frequency of 800 Hz. The overall level of the stimulus was 44 dB, corresponding to the level of the pure tone in Fig. 1. The latency of this response was 2.2 ms, slightly shorter than that seen for the pure-tone ANN. In general, the latencies of the AM-ANNs of high-frequency carriers were shorter than those of pure-tone responses: a result that is consistent with a more basal cochlear for the AM neurophonics. The rates of adaptation seen in this 800 Hz AM-ANN were comparable to those seen in the pure-tone response. The spectral composition of the AM-ANN also consisted of several harmonics (Fig. 2B), the fundamental of which matches
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Fig. 2. An 800 Hz auditory nerve neurophonic evoked by an 8 kHz carrier that was amplitude modulated at a frequency of 800 Hz with an overall level of 44 dB. The waveform is plotted above and is expressed in tens of microvolts. The amplitude spectrum is plotted below and expressed in dB re 0.1 pV.
Fig. 3. A 600 Hz frequency following response evoked by an 8 kHz carrier that was amplitude modulated at a frequency of 600 Hz. The waveform is plotted above and is expressed in microvoltsX2. The amplitude spectrum is plotted below and expressed in dB re 0.02 nV.
the modulation frequency. The second harmonic was often equal in amplitude to the fundamental, as it was in this case. The other harmonics, however, were usually 20-30 dB down from the fundamental. When carrier frequencies above 6 kHz were employed, no response at the spectral components of the signal (i.e. the carrier frequency and the two side band frequency) was measurable. Fig. 3 illustrates the waveform and spectral composition of an AM-FFR evoked by an 8 kHz carrier amplitude modulated at 600 Hz with an overall level of 34 dB. The main features of the scalp recorded AM response (spectral composition, latency, adaptation) appeared virtually identical to an attenuated version of an AM-ANN of the same frequency.
tude (measured as the sum of the amplitudes of the first three harmonic components) is plotted as a function of stimulus amplitude. Several of these input/output (Z/O) functions are plotted in Figs. 4 and 5. In Fig. 4, I/O functions for AM-ANNs produced by five different carrier frequencies modulated at 800 Hz are plotted. Although the waveforms of these AM neurophonics were virtually identical, the form of their Z/O functions varied as a function of carrier frequency. The slope of the Z/O functions could vary from a simple saturating monotonic function (e.g. for the 10, 15, 20, and 30 kHz carriers), to monotonic functions with an inflection or dip in the I/O functions (5 kHz carrier). These variations were dependent upon the carrier frequency for recordings from single animal and could also differ from animal to animal. The sensitivity of the neurophonic, i.e. the stimulus level at which a detectable neurophonic could be recorded was also a function of carrier
Input/output functions The amplitude of the AM-ANN and AM-FFR varied strongly with stimulus level. The nature of this variation can be seen when response ampli-
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Fig. 4. AM-ANN amplitude expressed as the sum of the first three harmonic components of the AM-ANN as a function of stimulus level for five carrier frequencies, all amplitude modulated at 800 Hz.
Fig. 5. Two neurophonic responses (AM-ANN and AM-FFR) recorded m the same animal in response to the same stimulus and plotted as a function of stimulus level. Response amplitude is expressed as the sum of the first three harmonic components. Both responses were evoked by a 15 kHz tone amplitude modulated at 800 Hz.
frequency. In Fig. 4 Z/O functions for carrier frequencies to which the animal was most sensitive are located to the left; while carrier frequencies to which the animal is least sensitive are shifted to the right. Note that Z/O functions for those ‘most sensitive’ carrier frequencies saturated at relatively low-stimulus levels (25-35 dB SPL), while the frequencies to which the recording was less sensitive saturated at higher levels. This was true for both the scalp and nerve recorded responses. A comparison of the AM-ANN and AM-FFR for one carrier/modulation frequency combination is shown in Fig. 5. It illustrates that under similar stimulus conditions the Z/O functions for these two responses had virtually the same form. Both curves grew at approximately the same rate and saturated at approximately the same stimulus level (70 dB). The AM-FFR curve was simply shifted down, i.e. the amplitude of the AM-FFR was attenuated by lo-15 dB relative to the AMANN.
transfer f~nction.~ A more detailed examination of the effects of carrier frequency upon response amplitude is shown by examination of carrier transfer functions (CTFs), i.e. a plot of the amplitude of the response as a function of carrier frequency while holding constant modulation frequency and overall level. CTFs of the auditory-nerve neurophonic for two cats are shown in Fig. 6. The general shape and response amplitudes of these CTFs were similar: the m~imum response was approximately 10 PV and the CTFs were relatively flat between 6 and 15 kHz indicating that response amplitudes changed little when the carrier frequency was shifted within this range. Below 6 kHz and above 15 kHz response amplitudes decreased. The roll-off in the transfer function below 6 kHz can be attributed to an increase in the amount of activity phase-locked to the carrier itself or its lower side band. This increase in phase-locking to the spectral components in the Carrier
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Fig. 6. Carrier frequency transfer functions for the AM-ANN measured in two cats. The overatl level of the stimulus was 34 dB SPL. The modulation frequency was 800 Hz. Response amplitude (the sum of the first three harmonic components) is expressed in dB re 0.1 mV.
carrier diminished the number of spikes which were phase-locked to the envelope, i.e. to the modulation frequency. The roll-off above 15 kHz can be attributed the transfer function of the stimulus delivery system which decreased with a roll-off of 10 dB/octave above 15 kHz. The average roll-off above 15 kHz for the CTFs in Fig. 6 was 10 dB/octave. Therefore, most of the decrease in the CTF above 15 kHz can be attributed to the sound system.
The effect of modulation frequency upon response amplitude of the ANN for a fixed carrier frequency and amplitude is illustrated by the modulation transfer functions (MTFs) plotted in Figs. 7, 8 and 9. In Fig. 7 the MTFs for two cats emplo~g the same carrier frequency (12 kHz) and overall level (34 dB) are plotted. The CTF for these two animals was relatively flat between 200 Hz and about 22 kHz. At modulation frequencies above approximately 1.5 kHz the AM-ANN amplitude diminished at a rate of approximately 20 dB/octave. This roll-off in the MTF may be explained by mechanisms similar to those responsible for the roll-off of pure-tone phase-locking of auditory nerve fibers (Johnson, 1980; Palmer, 1982). In Fig. 8 response amplitude for three carrier frequencies (4, 12, and 20 kHz) is plotted as a function of modulation frequency. In the curve for the 4 kHz carrier the data points for modulation frequencies above 2 kHz were omitted
Fig. 7. AM-ANN modulation transfer functions for two cats. The carrier frequency was 12 kHz at a level of 34 dB. Response amplitude is expressed in dB re 0.1 mV.
since the responses were dominated by responses to the lower side band. These MTFs were fairly similar with a relatively flat course from 200 Hz to 2 kHz and a roll-off at about 2.5 dB/octave above 2 kHz. Fig. 9 illustrates three MTFs for the same carrier frequency (12 kHz) with stimulus level as a parameter and demonstrates that the low-pass characteristic of the MTF was relatively unaffected by stimulus level except at very low levels. Forward masking
The neural nature of these AM-neurophonic responses is most convincingly demonstrated by forward masking, the effects of which are illustrated in Figs. 10-13. The experiments illustrated in these figures employed the following forward masking paradigm. A 100 ms probe constant in level and frequency was preceded by a
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Fig. 8. Modulation transfer functions (MTFs) for the AM-ANN at three carrier frequencies: 4 kHz, diamonds; 12 kHz, squares; and 20 kHz, triangles. The overal% levels of the stimuli were held constant at 34 dB SPL. Response amplitude {the sum of the first harmonic components) is expressed in dB re 0.1 mV.
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Fig. 9. Modulation transfer functions (MTFs) for a 12 kHz carrier at three stimulus levels: 54 dB SPL. diamonds: 34 dB SPL. squares: and I4 dB SPL. triangles. Response amplitude i\ expressed in dB re 0.1 mV.
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150 ms masking stimulus. Both probe and masker were gated on and off with ramps of 5 ms. The interval between the masker off-set and the probe on-set was 0.1 ms. The intertrial interval, i.e. the interval between the end of the probe and the beginning of the next masker. was 300 ms. The response to the probe was recorded as a function of masker level and frequency. In Fig. 10 the probe consisted of an 8 kHz carrier amplitude modulated at 600 Hz with an overall level of 34 dB. The masker frequency was a pure tone of 7 kHz. The response to the probe is illustrated under three masking conditions: no masker; masker level at 70 dB: and at 90 dB. Without a forward masker (upper waveform) the probe response was dominated by the 600 Hz envelope frequency and showed the typical adaptation rate. When the response was preceded by a 70 dB masker (middle waveform), the probe response was almost completely suppressed initially and then slowly started to recover. The recovery from forward masking started about 20 ms after the masker off-set. however. it was still incomplete after 100 ms. When the masker level is raised to 90 dB (lower waveform). the response was completely abolished for the duration of the recording interval. The only sign of a response was the compound action potential (CAP) evoked by the off-set of the forward masker at the very beginning of the recording interval. Masking functions, i.e. plots of response amplitude to a constant probe as a function of masker level for a fixed masker frequency, allow the com-
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Fig. 10. Forward masking of an AM-ANN at three masker levels. The responses are evoked by a 34 dB SPL stimulus comlsting of an 8 kHz carrier modulated at 600 Hz. The upper response is evoked by the probe stimulus presented with a forward masking pure tone of 7 kHz presented at - 10 dB. The middle response is evoked by the same prohe stimulus which is forward masked hy the same masking stimulus at 70 dB. The lower response is evoked hy the probe stimulus whvzh is forward masked by the same masking stimulus raised to 90 dB SPL. In this and all subsequent figure5 the duration of the masking simulus was 150 ms. The intertrial interval was 300 ms and the interval between the masker and the prohe w:is 0.1 m\. The waveform is plotted in microvolts x 2.
parison of the effects of different masker frequencies on the response to the probe. In Fig. 11 the amplitude of the first 30 ms of the ANN probe response is plotted as open symbols for four masking frequencies (7.0 kHz, squares; 7.5 kHz, diamonds: 8.0 kHz, triangles; 8.5 kHz. circles). These curves are off-set by 30 dB from one another for clarity. Below the AM-ANN masking functions there are four AM-FFR masking functions plotted as filled symbols for the same probe and the same masking frequencies as employed for the AM-
Fig. 11. Forward masking functions for neurophonics evoked by a fixed probe stimulus an 8 kHz carrier modulated at 600 Hz with an overall level of 34 dB SPL. The upper curves (open symbols) represent the amplitude of the AM-ANN to the probe when it is preceded by four pure-tone maskers at the frequencies indicated of different frequency. The curves are off-set from one another by 30 dB for the sake of clarity. The lower curves (filled symbols) represent the amplitude of the AM-FFR to the same fixed probe preceded by the same frequency maskers. These curves are also off-set by 30 dB.
ANN functions. All eight masking functions had a similar form: they consisted of two segments. At low masker levels the slope of the function was shallow, i.e. the reduction in the response per dB increase in the masker level was smalt, while at higher masker levels the slope became abruptly very steep. The slope of the initial segment and the location of the break point between these two segments varied only slightly for all four masker frequencies, while the slope of the second segment varied more strongly with masker frequency. The masker frequency which produced the steepest roll-off for a given probe carrier frequency and level was termed the best masking frequency (BMF). In this case the BMF was 7 kHz. A comparison of the masking functions for the AMANN (above) and the AM-FFR (below) demonstrates that the curves for the same probe masker combinations in the two sets were parallel. Both sets of functions produced the same BMF. A plot of the masker level necessary to produce a 30% reduction in response amplitude for a given probe at each masker frequency produces an iso-depression contour - commonly called a forward masking tuning curve (FMTC). Such tuning curves can be interpreted as demonstrating the frequency dist~bution of fibers whose phase-
locked activity contribute to the response (Snyder and Schreiner, 1985). Fig. 12 illustrates such an FMTC for a response evoked by an 8 kHz probe modulated at 800 Hz at an overall level of 34 dB. The BMF. which defines the tip of this curve, in this case matched the carrier frequency. a general finding for low-level probe stimuli. This tuning curve was quite sharply ‘tuned’ (Q,,,
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Fig. 12. A forward masked tuning curve (30% &o-depression contour) for an AM-ANN response to an 8 kHz carrier frequency amplitude modulated at 800 Hz. The overall level of the probe is 14 dB SPL as indicated by the filled square.
x7
Peuk nnulysis It has been suggested that the neurophonics represent a series of CAPS having a common waveform and repeated at intervals corresponding to the fundamental period of the stimulus. In Fig. 14 a series of five pure-tone neurophonics evoked by tones that range from 200 to X00 Hz are illustrated. No common waveform is easily discernable in these responses and. if the major peak of each response is aligned (dashed vertical line), none of the secondary peaks are in clear align-
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Fig. 13. Four forward masked AM-ANN tuning curves. The probe consists of a 15 kHz carrier amplitude at 800 Hz. The probe was presented at four levels in 15 dB increments: 5. 20. 35. and SO dB SPL (filled symbols).
higher levels for the more intense probe signals. However, the magnitude of this shift was not identical to the 15 dB increase in the probe level. The resulting differences between probe level and FMTC tip level were + 5, + 2, I- 12, and + 15 dB, respectively, for increasing probe levels. The tips of the FMTCs also shifted toward lower frequencies as probe level was increased. The maximum shift was small (1000 Hz at 15 kHz in Fig. 13). but it increased progressively with probe level and was consistently observed. The Qr,, dB values of the curves illustrated in Fig. 13 were fairly variable with no systematic trends. The Q!30 dB values of these curves were relatively constant except for the highest probe level, where it increased significantly. The variability of the Qlo dS values was probably due to the signal-to-noise ratio of these responses which were recorded after averaging only 25 stimulus presentations. In summary, increasing the probe level systematically shifted the tips of the FMTCs to higher levels and to lower frequencies without dramatically increasing the b~~ndwidth of the curves except at the highest probe levels.
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Fig. 14. 10 ms segments of five pure-tone ANNs. The frequency of the tone employed ia indicated above and to the right of each response. All five tones were presented at 46 dB SPL. The amplitudes of the responses are indicated at the lower left. The major peaks in the responses are aligned at the dashed line.
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ment. It is a standard observation for all pure-tone neurophonics that the timing of secondary peaks depends strongly upon the stimulus frequency. In contrast. the comparable AM neurophonics illustrated in Fig. 15 showed a timing of secondary peaks which was independent of the modulation frequency. In all these AM responses a common waveform is discernable. It consists of two peaks separated by a constant interval. The interval between these peaks is indicated by the two vertical dashed lines and ranges from 0.6 to 0.8 ms depending upon the overall stimulus level. However, the amplitude relations between primary and secondary peaks appeared to be strongly affected by the modulation frequency.
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Fig. 15. 10 ms segments of five AM-ANNs. The fundamental frequencies of the stimuli employed are identical to those in the previous figure and are indicated above and to the right of each response. The overall level of all stimuli was 34 dB. The amplitude of the responses is indicated at the lower left. The earliest peak in these responses is aligned at the dashed lme on the left. The dashed line on the right is drawn through the largest secondary peak in each response. The interval between these two lines is 0.7 ms.
In this paper we have demonstrated that lowfrequency amplitude modulation (< 4 kHz) of high-frequency carrier tones ( > 4 kHz) produce neurophonic responses similar to those of lowfrequency pure tones. Both AM and pure-tone neurophonics have a number of features in common. Among these are their spectral composition: their adaptation rate; a latency, which is long relative to that of the cochlear microphonic; and their susceptibility to forward masking. These results suggest that both sets of neurophonics arise from the phase-locked activity summed across the ensemble of auditory nerve fibers (Snyder and Schreiner, 1985). Response waveform and spectral composition AM-neuropho~c responses are concluded to consist of a series of CAP-like responses evoked by different AM frequencies, since they have a common waveform consisting of two peaks separated by an interval of from 0.6 to 0.8 ms. This common waveform is repeated at the interval of the modulation frequency and is observable at all levels and modulation frequencies below 800 Hz. The mode of production of these CAPS is unclear, although there are several mechanisms that could account for them. What is clear is that both peaks arise from the same spatially restricted fiber population since the Q,, dB values for the FMTCs of these responses are comparable to those from single units and tone evoked CAPS (Abbas and
Gorga. 1981). This is in marked contrast to the click evoked CAPS (Antoli-Candela and Kiang, 1974). The dissimilarity between the waveform of the AM and pure-tone neurophonics may be attributable in part to the differences in the CAP produced by basal and apical locations of the cochlea as demonstrated with the ‘derived-CAPS’ (Don and Eggermont. 1978: Evans and Elberling, 1982). Inpi/
output futictions The effects of overall intensity on the response of auditory nerve fibers to AM signals has been previously examined (Smith and Brachman, 1980; Javel. 1980). These studies have demonstrated that the AM response amplitude, i.e. the vector strength of the response phase-locked to the fundamental (m~~dulation) frequency of the stimulus, was a strong non-monotonic function of the overall level. In contrast, the neurophonic is usually a saturating monotonic function or only a slightly nonmonotonic function of stimulus intensity. Using 100% modulation Javel (1980) observed that fibers with CFs below 1 kHz when driven by CF tones and modulated at low frequencies had non-monotonic .4M responses. However, high and low CF fibers when driven by high-frequency carriers modulated at low frequencies did not appear to have the same non-monotonic AM intensity functions or at least the AM response had a greatly increased dynamic range (see Figs. 1 and 7: Javel, 1980). The discrepancy between single and neurophonic intensity functions probably reflects the influence of the summation of a large number of fibers with different CFs and thresholds in the neurophonic recordings. Trunsfer functions
The high- and low-frequency roll-offs of CTFs can be explained by the combination of two factors: (1) increasing phase-locking to the primaries in the signal as the carrier frequency decreases below 6 kHz --- especially for high-modulation frequencies (Johnson, 1980): and (2) the sensitivity of the cat cochlea to frequencies between 6 and 30 kHz (Elliot et al., 1960; Liberman and Gang, 1978). Thus the amplitude of the AM-neuroph~?l~ic responses appear to faithfully reflect the sensitivity of the cochlea to high-frequency stimuli.
Only one study has attempted to measure systematically the MTF in auditory nerve fibers across a sufficiently broad frequency range (Palmer, 1982). This study found MTFs that had essentially a low-pass characteristic with cut-off frequencies that increased with increasing CF as would be predicted from the increasing tuning curve bandwidth of these fibers. In fibers with CFs above 6 kHz the average cut-off frequency was approximately 600 Hz with a maximum cut-off frequency of approximately 1000 Hz. This compares well to what was seen in the neuroph~~nic, if similar criteria for the estimation of the cut-off frequency are used. The effects of overall level and carrier frequency have not been examined in detail for auditory nerve fibers, but the results presented here for the auditory neurophonic would suggest that these parameters would have only minor influences on the transfer functions observed, as long as the stimulus level were at least 20 dB above threshold and the carrier frequency were above 6 kHz. At this stimulus level the bandwidth of the stimulated fibers will be sufficiently wide to admit the side-band frequencies and allow them to be effective in modulating the firing rate of the population. At carrier frequencies above 6 kH7. the transfer function of the phase-locking to the envelope becomes the dominating factor in detern~ining the MTF and tuning-cur~,e b~~nd~idth or phase-locking to the lower side-band or the carrier itself are of little importance. Forrrtard masking
The time course for the recovery from forward masking in the AM neurophonic is similar to that seen for pure-tone neurophonics (Snyder and Schreiner, 1985). The time constant for recover) from pure-tone maskers in both sets of neurophonics is dependent upon masker level and frequency and can be very long. up to several hundred milliseconds. This is tnuch longer than the recovery time constants seen in forward masking studies of the recovery of a simple firing rate (as opposed to phase-locked rate) of single auditory nerve fibers (Harris and Dallas, 1979: Smith. 1977). However. it is similar to time constants seen in studies which employ longer duration maskers and which measure the recovery of single unit and CAP responses (Young and Sachs, 1973:
90
Abbas and Gorga, 1981; Abbas, 1984). The pattern of recovery from forward masking of the response to a prolonged probe suggests that the steady-state activity evoked by the probe does not recover to its unmasked amplitude but to a level determined by the amount of adaptation produced by the masker. More specifically even a low-level probe maintains the amount of adaptation produced by a high-level masker (see Fig. 11, Snyder and Schreiner, 1985; and this study Fig. 10). The masking functions for the AM neurophonits have many similarities to those evoked by pure tones. They consist of two segments (a shallow low-level segment and a steeper high-level segment) in a manner similar to pure-tone masking functions for maskers below BMF. However, this is true for all AM masking functions in contrast to pure-tone neurophonic masking functions for maskers above BMF which consist of a single shallow segment. FMTCs of the neurophonic allow an estimation of the distribution along the cochlear spiral of fibers that have a similar phase in their phaselocking to the probe stimulus. AM-neurophonic FMTCs indicate that these responses arise from fiber populations with a very limited spread along the cochlea. Below 35 dB this spread approaches that seen for a single auditory nerve fiber, i:e. the Q ,(I dB for a neurophonic FMTC is comparable to the Q,, da for a single fiber tuning curve with the same tip frequency. At high-stimulus levels (above 30 dB) the spread of excitation is increased (as indicated by the Q30 dB of the tuning curves) but more strikingly the distribution of the fibers contributing to the response shifts apically. i.e. to lower frequencies in the cochlea. This shift to lower frequencies is progressive with increasing stimulus levels and is opposite to that seen in pure-tone neurophonic FMTCs, which shift basally, i.e. to higher frequencies with increasing stimulus levels. The shift in cochlear position seen in the AM-FMTCs corresponds to a smaller shift than that observed for the pure-tone ANN. In summary, we conclude that the neurophonits evoked by AM high-frequency signals are equivalent to those evoked by pure-tone signals at frequencies corresponding to the modulation frequencies of the AM signals. They are hypothesized to arise from the spatial summation of auditory
nerve activity phase-locked to the envelope of the stimulus. Like the pure-tone evoked responses, each AM neurophonic arises from a population of fibers which has a limited distribution along the cochlear spiral and which is centered at or very near the point of maximum excitation produced by the spectral components in the stimulus. However, unlike the pure-tone population the population contributing to the AM response has a limited distribution corresponding to the cochlear place which is maximally excited by the carrier frequency, even at fairly high-stimulus levels. At high-stimulus levels, the contributing AM population shifts slightly toward the apex in contrast to the pure-tone neurophonic which expands significantly (up to one octave) towards the cochlear base. Acknowledgements The authors would like to thank Thomas Chimento for comments on the manuscript. This work was supported by NIH grant NS-16361 and the Coleman Fund. References Abbas, P.J. (1984) Recovery from long-term and short-term adaptation of the whole nerve action potential. J. Acoust. Sot. Am. 74. 1541-1547. Abbas. P.J. and Gorga, M.P. (1981) AP responses in forward masking paradigms and their relationship to responses of auditory nerve fibers. J. Acoust. Sot. Am. 69, 492-499. Antoli-Candela, F. and Kiang. N.Y.S. (1974) Unit activity underlying N, potential. In: R.F. Nauton and C. Fernandez (Eds.). Evoked Electrical Activity in the Auditory Nervous system, Academic Press, New York, London, pp. 165-189. Don, M. and Eggermont, J.J. (1978) Analysis of the clickevoked brain stem potentials in man using high-pass noise masking. J. Acoust. Sot. Am. 63, 1084-1092. Elliot, D.N., Stein, L. and Harrison, M.J. (1960) Discrimination of absolute-intensity thresholds and frequency-difference thresholds in cats. J. Acoust. Sot. Am. 32, 380-384. Evans. E.F. and Elberling, C. (1982) Location specific components of the gross cochlear action potential. Audiology 21, 204-227. Gardi, J. and Merzenich, M.M.M. (1979) The effects of highpass noise on the scalp-recorded frequency following response (FFR) in humans and cats. J. Acoust. Sot. Am 65, 1491-1500. Greenberg, S., Marsh, J.T., Brown, W.S. and Smith. 3.C. (1987) Neural temporal coding of low pitch. I. Human frequency-
following
responses
to
complex
tones.
Hear.
Res.
25.
Harris.
D.M.
and Dalla.
P. (1979)
Forward
masking of audi-
tory RCIW fiber responses.J. Neurophysioi. Klang.
Sach>. M.B. (1YXl)
Responses of auditory-nerxt’
~~teristt~-frequents
Yl-114.
N.Y.S.
(1984)
information.
Peripheral
in: I. Da&n-Smith
olopv. Section
1. Vol.
Bethesda. Maryland.
III.
42. 10X3- 1107.
neural processing of auditor! (Ed.).
American
Handbook
SOCICI~.
Pt. 2. pp. 639-674.
C.E. and Urhas. J.V. modulation
Anterior
auditory
R.L.
(1977)
nerve fibers:
Javol. E. (1980) Coding of Ahl tones on the chinchilla nerve: Implications
Schreiner.
Smith.
for pitch of complex
auditor!
suppressor\
Res. 4. 309-324.
plitude
of Physi-
Phvslological
ttear.
fiber> to char-
tones and low-frrquencv
40. 1098-l
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Res. 21. 217-241. adaptation
Some pc>ststimulu\
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effect\.
.I
Neurophvaio.
112.
tones. J. Acnust.
sot. Am. 6X. 131-146. Johnwn.
I). (19X0)
\ynchrony Acoust Liherm;tn.
The
relatmnship
in rapowes
Sot. Am. 6X. M.C.
I 115-l
1..
tuning
Ryan. curve’\
spike rate and
fibers to tones. J.
122.
and K~;tng. N.Y.S.
fats. Acta Otolaryngoi. M&cc.
between
of auditory-nerve
(197X) Acoustic
trauma
in
Suppl. 35X. I-63.
A.
and
of
chinchilla.
Dalios.
P. 11976) J.
Acoust.
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Am.
60.
1146-1150. Mouahegian.
Cr.. Rupert.
t:wluation
~ng ;~nd cllmcal ph>\wl. Palmer.
A.L.
and
R.D.
(1978)
in man: Ma,k-
studies. Electroencephalogr.
C‘lin. Neuro-
45. 711-71X.
A.R. (19X2)
KLICI. A.. Green.
Encoding
G.G.R.
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Worden.
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and
of rapid amplitude the R.H.
sinusoidally
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Young.
(1986) Steady-state 3mplitudr-mndul;tted
Rrs. 23. 123-133.
(197X)
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Clin. Neurophysiol.
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neural reapwwa
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poaurr li35-
and Kay, to
fluctuations
Marsh.
(microphonic-like) troencrphalogr.
fibers in h!, ccchlear-nrrvc Otclrhin[,laryngol. 236. lY7--202. evoked
Stillman.
of frequency following potential5
(1973)
Recover\
nerve fibers. J. Acou\t.
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Auditory
Two auditory
n~ur[)ph(~ni~ responses - one recorded
auditor): newe (auditory &ted
(AM)
neurophonic responses to amplitude-modulated Transfer functions and forward masking
nerve n~ur~p~~ni~
high-frequency
or ANN)
comparable
spectral composition,
pure-tone
simllar
masker. The frequency dependence as a function
transfer functions or CTF) for carrter frequencies
and response anlplitud~
from 6 to 30 kHz.
Frequency
to: R.L. Snyder, Coleman
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U.S.A.
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of Califorma,
response: .Amplitude
and Epstein LaboraSan Francisco,
forward
stimulus can produce
upon the le\cl
were found
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prolonged
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frequency
monotonic
centered on the carrier frcqucncv.
as a function (nl(~ul~{tl(~ll
functions
frequrncles
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transfer functions or MTF)
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action potential\.
When sustained low-frequency stimuli are presented to the auditory system. sustained ensemble neural responses can be recorded both intracranially from several auditory nuclei as well as extracraniaiiy from the scalp. The term neurophonic has been applied to these responses in order to emphasize both their neural origins and their similarity to the cochlear microphonic (CM) (Weinberger et al.. 1969; Snyder and Schreiner. 1984, 1985). However, these neurophonic responses have longer latencies compared to the CM, more spectrally complex waveforms and display pronounced adaptation.
~‘orrev~w&ww
freyuency
of ln~dulati~n
from
masked tuning curve5 which Indicate that the AM
rcsponw~ amplitude
were flat for modulation
Introduction
tories. X71 blSE. University
ib dependent
by forward
functions were saturating
and MTFs
following
functions.
as a function
with similar data for single units and compound
neurophonic:
of this depression
masking
frequencwa varied hctwcen
re\ponae waveforms
rates of recovery
an unmodulated
which have restricted characteristic
( I/O)
responses. Thr AM
and similar
neurophomcs,
and duration
of stimulus level
were‘ alw measured. It was found that the 1/O
Auditory
rates of adaptation,
and one from the
~tin~ulati~~n of the cat cochlea with ~implitud~-rn~)~i-
neurophonic
of the depression is demonstrated
responses arise from fiber populations
compared
with pure-tone
responses. As with the pure-tone
depresston of the probe response. The amount
Response amplitude
following
tones. The carrier frequencies varied between 2 and 30 kHz. The modulation
400 and 3000 Hz. The AM responaea were compared to have d similar
followin, 0 response or t-I;Ri
from the scalp (frequency
- were obtained
tones:
CA
modulation:
Forward
masking
The stimuli usually employed to evoke neurophonic responses consist of low-frequency pure tones (between 100 Hz and 2 kHz) at levels below 90 dB SPL. However, one study has used amplitude modulation of low-frequency tones to evoke a very low-frequency neurophonic (Rees et al.. 1986). The most intensively studied ~leuroph~?ili~ in animals and humans is the one recorded from the scalp - the frequency following response or FFR (Moushegian et al., 197X; Worden and Marsh, 1978; Gardi and Merzenich, 1979: Rees et al., 1986; Greenberg et al.. 1987). In cats the auditory nerve neurophonic (ANN) and FFR have been demonstrated to be neural responses arising primarily from phase-locked activity in the ensemble of auditory nerve fibers (Snyder and Schreiner. 1984, 1985). Forward masking studies have demonstrated that the distribution of fibers which contribute to
” 1987 Elsevier Science Puhlishors H.V. (Biomedical
Division)
80
the pure-tone ANNs and FFRs are spatially highly restricted and that these fibers innervate sectors of the cochlea which are appropriate for the evoking frequencies (Snyder and Schreiner, 1985). The fibers in the most strongly contributing population have characteristic frequencies (CFs) ranging from the stimulus frequency up to approximately one octave above the stimulus frequency. The CF distribution of the fibers which are constructively contributing to the neurophonic depends upon the signal level having a bandwidth of l/3 octave or less at 10 dB above threshold (Snyder and Schreiner, 1985). Thus the neurophonic responses to low-frequency tones reflect the functional properties of auditory nerve fibers which innervate restricted sectors of the apical cochlea and consequently allow examination of their functional integrity. This is in marked distinction to the click and tone evoked action potentials (APs) and auditory brainstem responses (ABRs) which reflect primarily the activity in fibers innervating the cochlear base (Antoli-Candela and Kiang, 1974). In this study we have examined the ANNs and FFRs evoked by ~gh-frequency (> 4 kHzf tones sinusoidally amplitude modulated at frequencies between 200 Hz and 4 kHz. We have found that such amplitude modulated signals produce neurophonic responses which have many properties in common with those produced by low-frequency pure tones: the major frequency components of amplitude-modulated (AM) ANNs and FFRs match harmonics of the modulation or envelope frequency; they have relatively long latencies; and they display adaptation. Using forward masking techniques these AM neurophonics have been shown to arise from fibers whose characteristic frequencies approximate the carrier frequency. Therefore, AM-ANNs and AM-FFRs are presumed to arise as a consequence of a spatial summation of activity in auditory nerve fibers which innervate the cochlear base, which are most sensitive to the carrier frequency, and which phase-lock to the envelope of the stimulus. Thus despite their similarity to low-frequency, pure-tone evoked neurophonics, these AM responses arise from entirely different fiber populations.
Materials
and Methods
Animal surgery~ Experiments were conducted using JO adult cats obtained from a closed breeding colony at the University of California at Davis. The cats were given an otologic examination to ensure healthy external and middle ears. Each animal was initially anesthetized with an intramuscular injection of ketamine (10 mg/kg) and acepromazine (1 mg/kg). A catheter was inserted into the cephalic vein and lactated Ringer’s solution was continuously infused through the catheter. Supplementary doses of sodium pentobarbital were administered via this catheter in order to induce and maintain a surgical level of anesthesia. The scalp was incised and reflected to expose the posterolateral surface of the skull. The external ear canal was incised and a rigid hollow ear bar inserted and sealed. The auditory nerve was exposed via a burr hole made in the occipital bone and aspiration of the lateral cerebellum. Platinum-iridium ball electrodes were placed on either side of the auditory nerve as it exits the internal auditory meatus. Three silver wire electrodes were placed in the skin: one just below the pinna of the stimulated ear. one at the vertex. and one at the nape of the neck. Recording The ANN was recorded differentially using the two platinum-iridium ball electrodes on either side of the auditory nerve as it exits the internal meatus. The FFR was recorded using silver wires; the vertex electrode as the active and an electrode below the stimulated ear as the reference. An electrode through the skin at the nape of the neck served as the ground electrode for both recordings. The responses were initially amplified using a Princeton Applied Electronics battery powered amplifier (Model 113) and led through a second stage amplifier consisting of a 3A9 plug-in amplifier for a Tektronix 565 oscilloscope. The bandpass of the amplifiers was set to 30 Hz-30 kHz. The total gain varied depending upon the signal that was being recorded. The usual amplifications were 20000 X for the ANN and 100~ X for the FFR. The amplified signal was digitized using a 12 bit analogue-to-digital converter operating at a 20 kHz sampling rate and averaged using a
Xl
PURE
PDP11/23 computer. The averaged responses were obtained for a variable number of stimulus presentations, usually 100 for the ANN and 500 for the FFR. Stimulus generation Stimuli were generated by a Texas Instruments TMS 32010 ~crocomputer, which synthesized and shaped the signal digitally and transmitted the signal to a 16 bit deglitched DAC. The output rate of the stimulus generation system was varied between 60 and 120 kHz depending upon the carrier frequency of the stimulus and always exceeded the frequency of the upper side band by at least a factor of four. The output of the stimulus generation system was low-pass filtered at 15 or 35 kHz, fed through an attenuator and delivered via an equalizer/amplifier system to a STAX 54 electret headphone encased within an electrically shielded container. The output of this system is flat within it 6 dB variation at the tympanic membrane over the range of 100 Hz-15 kHz. Above 15 kHz the output rolled off at a rate of 10 dB/octave. All stimuli were gated on and off with 5 ms ramps and all stimulus levels are expressed in dB SPL (sound pressure level re: 20 FPa). Results Response
war!efarms Neurophonic responses elicited by pure tones and those elicited by AM tones have a number of features in common. Some of these features can be seen simply by examining the response waveforms. Fig. 1A and B illustrates the response waveform and amplitude spectrum, respectively, of an ANN evoked by an 800 Hz pure tone presented at 44 dB. The basic properties of such neurophonics have been described in detail previously (Snyder and Schreiner, 1984,1985) and need only be summarized briefly here. Among the properties which indicate that these responses were of neural origins are a latency of 3-5 ms, the presence of adaptation in the amplitude of the response, and a complex spectral composition. The latency of the 800 Hz ANN in Fig. 1A was 3.5 ms and the waveform adapts with a short term time constant of approximately 10 ms. The spectral components in this response are seen
TONE
ANN
BOOHZ
AT
4408
SPL
A
I
2 :-l_~:o 0. 0
10.0
20.
0
Tima
0 0.00
0. 98
1.95 Frequency
(msec)
2. 93
3.31
4. 88
(kHz>
Fig. 1. Auditory nerve neurophonic response to an X00 Hz tone at 44 dB SPL. The waveform is shown above and the amplitude spectrum is shown below. The waveform is plotted in tens of microvolts. The amplitude spectrum is expressed in dB re 0.1 p-v-.
in Fig. 1B and consisted of a series of three harmonic components: a fundamental component which matched the stimulus frequency and its second and third harmonics. The amplitudes of these components for this response were within 6 dB of one another. Fig. 2 illustrates a representative example of an 800 Hz AM-ANN waveform evoked by an 8 kHz carrier 100% amplitude modulated at a frequency of 800 Hz. The overall level of the stimulus was 44 dB, corresponding to the level of the pure tone in Fig. 1. The latency of this response was 2.2 ms, slightly shorter than that seen for the pure-tone ANN. In general, the latencies of the AM-ANNs of high-frequency carriers were shorter than those of pure-tone responses: a result that is consistent with a more basal cochlear for the AM neurophonics. The rates of adaptation seen in this 800 Hz AM-ANN were comparable to those seen in the pure-tone response. The spectral composition of the AM-ANN also consisted of several harmonics (Fig. 2B), the fundamental of which matches
82 AM-ANN
CARRIER-EKHZ.
BOOHZ
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100%.64DB
AM-FFR
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4.00
c
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CARRIER. ____
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, 10.0
I
,
20. 0 Time
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;
30
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20
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,
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,
,
40.
/
,
0
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0
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oo;+rT;bT;-
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0
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0
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0. 98
1.95 Frequency
2. 93
3.91
4. 88
(kHz)
0. 00
0. 98
1.95 Frequency
2. 93
3.91
4. 88
Fig. 2. An 800 Hz auditory nerve neurophonic evoked by an 8 kHz carrier that was amplitude modulated at a frequency of 800 Hz with an overall level of 44 dB. The waveform is plotted above and is expressed in tens of microvolts. The amplitude spectrum is plotted below and expressed in dB re 0.1 pV.
Fig. 3. A 600 Hz frequency following response evoked by an 8 kHz carrier that was amplitude modulated at a frequency of 600 Hz. The waveform is plotted above and is expressed in microvoltsX2. The amplitude spectrum is plotted below and expressed in dB re 0.02 nV.
the modulation frequency. The second harmonic was often equal in amplitude to the fundamental, as it was in this case. The other harmonics, however, were usually 20-30 dB down from the fundamental. When carrier frequencies above 6 kHz were employed, no response at the spectral components of the signal (i.e. the carrier frequency and the two side band frequency) was measurable. Fig. 3 illustrates the waveform and spectral composition of an AM-FFR evoked by an 8 kHz carrier amplitude modulated at 600 Hz with an overall level of 34 dB. The main features of the scalp recorded AM response (spectral composition, latency, adaptation) appeared virtually identical to an attenuated version of an AM-ANN of the same frequency.
tude (measured as the sum of the amplitudes of the first three harmonic components) is plotted as a function of stimulus amplitude. Several of these input/output (Z/O) functions are plotted in Figs. 4 and 5. In Fig. 4, I/O functions for AM-ANNs produced by five different carrier frequencies modulated at 800 Hz are plotted. Although the waveforms of these AM neurophonics were virtually identical, the form of their Z/O functions varied as a function of carrier frequency. The slope of the Z/O functions could vary from a simple saturating monotonic function (e.g. for the 10, 15, 20, and 30 kHz carriers), to monotonic functions with an inflection or dip in the I/O functions (5 kHz carrier). These variations were dependent upon the carrier frequency for recordings from single animal and could also differ from animal to animal. The sensitivity of the neurophonic, i.e. the stimulus level at which a detectable neurophonic could be recorded was also a function of carrier
Input/output functions The amplitude of the AM-ANN and AM-FFR varied strongly with stimulus level. The nature of this variation can be seen when response ampli-
--
L
-I 110
STIMULUS
LEVEL
CD5
30
SPL)
I
AM-ANN
8
40
50
I
I AM-FFR
STIMULUS
60
I
I
I
a0
90
100
I/O
70
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110
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Fig. 4. AM-ANN amplitude expressed as the sum of the first three harmonic components of the AM-ANN as a function of stimulus level for five carrier frequencies, all amplitude modulated at 800 Hz.
Fig. 5. Two neurophonic responses (AM-ANN and AM-FFR) recorded m the same animal in response to the same stimulus and plotted as a function of stimulus level. Response amplitude is expressed as the sum of the first three harmonic components. Both responses were evoked by a 15 kHz tone amplitude modulated at 800 Hz.
frequency. In Fig. 4 Z/O functions for carrier frequencies to which the animal was most sensitive are located to the left; while carrier frequencies to which the animal is least sensitive are shifted to the right. Note that Z/O functions for those ‘most sensitive’ carrier frequencies saturated at relatively low-stimulus levels (25-35 dB SPL), while the frequencies to which the recording was less sensitive saturated at higher levels. This was true for both the scalp and nerve recorded responses. A comparison of the AM-ANN and AM-FFR for one carrier/modulation frequency combination is shown in Fig. 5. It illustrates that under similar stimulus conditions the Z/O functions for these two responses had virtually the same form. Both curves grew at approximately the same rate and saturated at approximately the same stimulus level (70 dB). The AM-FFR curve was simply shifted down, i.e. the amplitude of the AM-FFR was attenuated by lo-15 dB relative to the AMANN.
transfer f~nction.~ A more detailed examination of the effects of carrier frequency upon response amplitude is shown by examination of carrier transfer functions (CTFs), i.e. a plot of the amplitude of the response as a function of carrier frequency while holding constant modulation frequency and overall level. CTFs of the auditory-nerve neurophonic for two cats are shown in Fig. 6. The general shape and response amplitudes of these CTFs were similar: the m~imum response was approximately 10 PV and the CTFs were relatively flat between 6 and 15 kHz indicating that response amplitudes changed little when the carrier frequency was shifted within this range. Below 6 kHz and above 15 kHz response amplitudes decreased. The roll-off in the transfer function below 6 kHz can be attributed to an increase in the amount of activity phase-locked to the carrier itself or its lower side band. This increase in phase-locking to the spectral components in the Carrier
0
5d”
.L.
10000
CARRIER
~.
.A
..__..A.-.
15000
FREQUENCY
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25000
.._i
30000
(Hz)
Fig. 6. Carrier frequency transfer functions for the AM-ANN measured in two cats. The overatl level of the stimulus was 34 dB SPL. The modulation frequency was 800 Hz. Response amplitude (the sum of the first three harmonic components) is expressed in dB re 0.1 mV.
carrier diminished the number of spikes which were phase-locked to the envelope, i.e. to the modulation frequency. The roll-off above 15 kHz can be attributed the transfer function of the stimulus delivery system which decreased with a roll-off of 10 dB/octave above 15 kHz. The average roll-off above 15 kHz for the CTFs in Fig. 6 was 10 dB/octave. Therefore, most of the decrease in the CTF above 15 kHz can be attributed to the sound system.
The effect of modulation frequency upon response amplitude of the ANN for a fixed carrier frequency and amplitude is illustrated by the modulation transfer functions (MTFs) plotted in Figs. 7, 8 and 9. In Fig. 7 the MTFs for two cats emplo~g the same carrier frequency (12 kHz) and overall level (34 dB) are plotted. The CTF for these two animals was relatively flat between 200 Hz and about 22 kHz. At modulation frequencies above approximately 1.5 kHz the AM-ANN amplitude diminished at a rate of approximately 20 dB/octave. This roll-off in the MTF may be explained by mechanisms similar to those responsible for the roll-off of pure-tone phase-locking of auditory nerve fibers (Johnson, 1980; Palmer, 1982). In Fig. 8 response amplitude for three carrier frequencies (4, 12, and 20 kHz) is plotted as a function of modulation frequency. In the curve for the 4 kHz carrier the data points for modulation frequencies above 2 kHz were omitted
Fig. 7. AM-ANN modulation transfer functions for two cats. The carrier frequency was 12 kHz at a level of 34 dB. Response amplitude is expressed in dB re 0.1 mV.
since the responses were dominated by responses to the lower side band. These MTFs were fairly similar with a relatively flat course from 200 Hz to 2 kHz and a roll-off at about 2.5 dB/octave above 2 kHz. Fig. 9 illustrates three MTFs for the same carrier frequency (12 kHz) with stimulus level as a parameter and demonstrates that the low-pass characteristic of the MTF was relatively unaffected by stimulus level except at very low levels. Forward masking
The neural nature of these AM-neurophonic responses is most convincingly demonstrated by forward masking, the effects of which are illustrated in Figs. 10-13. The experiments illustrated in these figures employed the following forward masking paradigm. A 100 ms probe constant in level and frequency was preceded by a
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Fig. 8. Modulation transfer functions (MTFs) for the AM-ANN at three carrier frequencies: 4 kHz, diamonds; 12 kHz, squares; and 20 kHz, triangles. The overal% levels of the stimuli were held constant at 34 dB SPL. Response amplitude {the sum of the first harmonic components) is expressed in dB re 0.1 mV.
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150 ms masking stimulus. Both probe and masker were gated on and off with ramps of 5 ms. The interval between the masker off-set and the probe on-set was 0.1 ms. The intertrial interval, i.e. the interval between the end of the probe and the beginning of the next masker. was 300 ms. The response to the probe was recorded as a function of masker level and frequency. In Fig. 10 the probe consisted of an 8 kHz carrier amplitude modulated at 600 Hz with an overall level of 34 dB. The masker frequency was a pure tone of 7 kHz. The response to the probe is illustrated under three masking conditions: no masker; masker level at 70 dB: and at 90 dB. Without a forward masker (upper waveform) the probe response was dominated by the 600 Hz envelope frequency and showed the typical adaptation rate. When the response was preceded by a 70 dB masker (middle waveform), the probe response was almost completely suppressed initially and then slowly started to recover. The recovery from forward masking started about 20 ms after the masker off-set. however. it was still incomplete after 100 ms. When the masker level is raised to 90 dB (lower waveform). the response was completely abolished for the duration of the recording interval. The only sign of a response was the compound action potential (CAP) evoked by the off-set of the forward masker at the very beginning of the recording interval. Masking functions, i.e. plots of response amplitude to a constant probe as a function of masker level for a fixed masker frequency, allow the com-
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Fig. 10. Forward masking of an AM-ANN at three masker levels. The responses are evoked by a 34 dB SPL stimulus comlsting of an 8 kHz carrier modulated at 600 Hz. The upper response is evoked by the probe stimulus presented with a forward masking pure tone of 7 kHz presented at - 10 dB. The middle response is evoked by the same prohe stimulus which is forward masked hy the same masking stimulus at 70 dB. The lower response is evoked hy the probe stimulus whvzh is forward masked by the same masking stimulus raised to 90 dB SPL. In this and all subsequent figure5 the duration of the masking simulus was 150 ms. The intertrial interval was 300 ms and the interval between the masker and the prohe w:is 0.1 m\. The waveform is plotted in microvolts x 2.
parison of the effects of different masker frequencies on the response to the probe. In Fig. 11 the amplitude of the first 30 ms of the ANN probe response is plotted as open symbols for four masking frequencies (7.0 kHz, squares; 7.5 kHz, diamonds: 8.0 kHz, triangles; 8.5 kHz. circles). These curves are off-set by 30 dB from one another for clarity. Below the AM-ANN masking functions there are four AM-FFR masking functions plotted as filled symbols for the same probe and the same masking frequencies as employed for the AM-
Fig. 11. Forward masking functions for neurophonics evoked by a fixed probe stimulus an 8 kHz carrier modulated at 600 Hz with an overall level of 34 dB SPL. The upper curves (open symbols) represent the amplitude of the AM-ANN to the probe when it is preceded by four pure-tone maskers at the frequencies indicated of different frequency. The curves are off-set from one another by 30 dB for the sake of clarity. The lower curves (filled symbols) represent the amplitude of the AM-FFR to the same fixed probe preceded by the same frequency maskers. These curves are also off-set by 30 dB.
ANN functions. All eight masking functions had a similar form: they consisted of two segments. At low masker levels the slope of the function was shallow, i.e. the reduction in the response per dB increase in the masker level was smalt, while at higher masker levels the slope became abruptly very steep. The slope of the initial segment and the location of the break point between these two segments varied only slightly for all four masker frequencies, while the slope of the second segment varied more strongly with masker frequency. The masker frequency which produced the steepest roll-off for a given probe carrier frequency and level was termed the best masking frequency (BMF). In this case the BMF was 7 kHz. A comparison of the masking functions for the AMANN (above) and the AM-FFR (below) demonstrates that the curves for the same probe masker combinations in the two sets were parallel. Both sets of functions produced the same BMF. A plot of the masker level necessary to produce a 30% reduction in response amplitude for a given probe at each masker frequency produces an iso-depression contour - commonly called a forward masking tuning curve (FMTC). Such tuning curves can be interpreted as demonstrating the frequency dist~bution of fibers whose phase-
locked activity contribute to the response (Snyder and Schreiner, 1985). Fig. 12 illustrates such an FMTC for a response evoked by an 8 kHz probe modulated at 800 Hz at an overall level of 34 dB. The BMF. which defines the tip of this curve, in this case matched the carrier frequency. a general finding for low-level probe stimuli. This tuning curve was quite sharply ‘tuned’ (Q,,,
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x7
Peuk nnulysis It has been suggested that the neurophonics represent a series of CAPS having a common waveform and repeated at intervals corresponding to the fundamental period of the stimulus. In Fig. 14 a series of five pure-tone neurophonics evoked by tones that range from 200 to X00 Hz are illustrated. No common waveform is easily discernable in these responses and. if the major peak of each response is aligned (dashed vertical line), none of the secondary peaks are in clear align-
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higher levels for the more intense probe signals. However, the magnitude of this shift was not identical to the 15 dB increase in the probe level. The resulting differences between probe level and FMTC tip level were + 5, + 2, I- 12, and + 15 dB, respectively, for increasing probe levels. The tips of the FMTCs also shifted toward lower frequencies as probe level was increased. The maximum shift was small (1000 Hz at 15 kHz in Fig. 13). but it increased progressively with probe level and was consistently observed. The Qr,, dB values of the curves illustrated in Fig. 13 were fairly variable with no systematic trends. The Q!30 dB values of these curves were relatively constant except for the highest probe level, where it increased significantly. The variability of the Qlo dS values was probably due to the signal-to-noise ratio of these responses which were recorded after averaging only 25 stimulus presentations. In summary, increasing the probe level systematically shifted the tips of the FMTCs to higher levels and to lower frequencies without dramatically increasing the b~~ndwidth of the curves except at the highest probe levels.
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ment. It is a standard observation for all pure-tone neurophonics that the timing of secondary peaks depends strongly upon the stimulus frequency. In contrast. the comparable AM neurophonics illustrated in Fig. 15 showed a timing of secondary peaks which was independent of the modulation frequency. In all these AM responses a common waveform is discernable. It consists of two peaks separated by a constant interval. The interval between these peaks is indicated by the two vertical dashed lines and ranges from 0.6 to 0.8 ms depending upon the overall stimulus level. However, the amplitude relations between primary and secondary peaks appeared to be strongly affected by the modulation frequency.
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Fig. 15. 10 ms segments of five AM-ANNs. The fundamental frequencies of the stimuli employed are identical to those in the previous figure and are indicated above and to the right of each response. The overall level of all stimuli was 34 dB. The amplitude of the responses is indicated at the lower left. The earliest peak in these responses is aligned at the dashed lme on the left. The dashed line on the right is drawn through the largest secondary peak in each response. The interval between these two lines is 0.7 ms.
In this paper we have demonstrated that lowfrequency amplitude modulation (< 4 kHz) of high-frequency carrier tones ( > 4 kHz) produce neurophonic responses similar to those of lowfrequency pure tones. Both AM and pure-tone neurophonics have a number of features in common. Among these are their spectral composition: their adaptation rate; a latency, which is long relative to that of the cochlear microphonic; and their susceptibility to forward masking. These results suggest that both sets of neurophonics arise from the phase-locked activity summed across the ensemble of auditory nerve fibers (Snyder and Schreiner, 1985). Response waveform and spectral composition AM-neuropho~c responses are concluded to consist of a series of CAP-like responses evoked by different AM frequencies, since they have a common waveform consisting of two peaks separated by an interval of from 0.6 to 0.8 ms. This common waveform is repeated at the interval of the modulation frequency and is observable at all levels and modulation frequencies below 800 Hz. The mode of production of these CAPS is unclear, although there are several mechanisms that could account for them. What is clear is that both peaks arise from the same spatially restricted fiber population since the Q,, dB values for the FMTCs of these responses are comparable to those from single units and tone evoked CAPS (Abbas and
Gorga. 1981). This is in marked contrast to the click evoked CAPS (Antoli-Candela and Kiang, 1974). The dissimilarity between the waveform of the AM and pure-tone neurophonics may be attributable in part to the differences in the CAP produced by basal and apical locations of the cochlea as demonstrated with the ‘derived-CAPS’ (Don and Eggermont. 1978: Evans and Elberling, 1982). Inpi/
output futictions The effects of overall intensity on the response of auditory nerve fibers to AM signals has been previously examined (Smith and Brachman, 1980; Javel. 1980). These studies have demonstrated that the AM response amplitude, i.e. the vector strength of the response phase-locked to the fundamental (m~~dulation) frequency of the stimulus, was a strong non-monotonic function of the overall level. In contrast, the neurophonic is usually a saturating monotonic function or only a slightly nonmonotonic function of stimulus intensity. Using 100% modulation Javel (1980) observed that fibers with CFs below 1 kHz when driven by CF tones and modulated at low frequencies had non-monotonic .4M responses. However, high and low CF fibers when driven by high-frequency carriers modulated at low frequencies did not appear to have the same non-monotonic AM intensity functions or at least the AM response had a greatly increased dynamic range (see Figs. 1 and 7: Javel, 1980). The discrepancy between single and neurophonic intensity functions probably reflects the influence of the summation of a large number of fibers with different CFs and thresholds in the neurophonic recordings. Trunsfer functions
The high- and low-frequency roll-offs of CTFs can be explained by the combination of two factors: (1) increasing phase-locking to the primaries in the signal as the carrier frequency decreases below 6 kHz --- especially for high-modulation frequencies (Johnson, 1980): and (2) the sensitivity of the cat cochlea to frequencies between 6 and 30 kHz (Elliot et al., 1960; Liberman and Gang, 1978). Thus the amplitude of the AM-neuroph~?l~ic responses appear to faithfully reflect the sensitivity of the cochlea to high-frequency stimuli.
Only one study has attempted to measure systematically the MTF in auditory nerve fibers across a sufficiently broad frequency range (Palmer, 1982). This study found MTFs that had essentially a low-pass characteristic with cut-off frequencies that increased with increasing CF as would be predicted from the increasing tuning curve bandwidth of these fibers. In fibers with CFs above 6 kHz the average cut-off frequency was approximately 600 Hz with a maximum cut-off frequency of approximately 1000 Hz. This compares well to what was seen in the neuroph~~nic, if similar criteria for the estimation of the cut-off frequency are used. The effects of overall level and carrier frequency have not been examined in detail for auditory nerve fibers, but the results presented here for the auditory neurophonic would suggest that these parameters would have only minor influences on the transfer functions observed, as long as the stimulus level were at least 20 dB above threshold and the carrier frequency were above 6 kHz. At this stimulus level the bandwidth of the stimulated fibers will be sufficiently wide to admit the side-band frequencies and allow them to be effective in modulating the firing rate of the population. At carrier frequencies above 6 kH7. the transfer function of the phase-locking to the envelope becomes the dominating factor in detern~ining the MTF and tuning-cur~,e b~~nd~idth or phase-locking to the lower side-band or the carrier itself are of little importance. Forrrtard masking
The time course for the recovery from forward masking in the AM neurophonic is similar to that seen for pure-tone neurophonics (Snyder and Schreiner, 1985). The time constant for recover) from pure-tone maskers in both sets of neurophonics is dependent upon masker level and frequency and can be very long. up to several hundred milliseconds. This is tnuch longer than the recovery time constants seen in forward masking studies of the recovery of a simple firing rate (as opposed to phase-locked rate) of single auditory nerve fibers (Harris and Dallas, 1979: Smith. 1977). However. it is similar to time constants seen in studies which employ longer duration maskers and which measure the recovery of single unit and CAP responses (Young and Sachs, 1973:
90
Abbas and Gorga, 1981; Abbas, 1984). The pattern of recovery from forward masking of the response to a prolonged probe suggests that the steady-state activity evoked by the probe does not recover to its unmasked amplitude but to a level determined by the amount of adaptation produced by the masker. More specifically even a low-level probe maintains the amount of adaptation produced by a high-level masker (see Fig. 11, Snyder and Schreiner, 1985; and this study Fig. 10). The masking functions for the AM neurophonits have many similarities to those evoked by pure tones. They consist of two segments (a shallow low-level segment and a steeper high-level segment) in a manner similar to pure-tone masking functions for maskers below BMF. However, this is true for all AM masking functions in contrast to pure-tone neurophonic masking functions for maskers above BMF which consist of a single shallow segment. FMTCs of the neurophonic allow an estimation of the distribution along the cochlear spiral of fibers that have a similar phase in their phaselocking to the probe stimulus. AM-neurophonic FMTCs indicate that these responses arise from fiber populations with a very limited spread along the cochlea. Below 35 dB this spread approaches that seen for a single auditory nerve fiber, i:e. the Q ,(I dB for a neurophonic FMTC is comparable to the Q,, da for a single fiber tuning curve with the same tip frequency. At high-stimulus levels (above 30 dB) the spread of excitation is increased (as indicated by the Q30 dB of the tuning curves) but more strikingly the distribution of the fibers contributing to the response shifts apically. i.e. to lower frequencies in the cochlea. This shift to lower frequencies is progressive with increasing stimulus levels and is opposite to that seen in pure-tone neurophonic FMTCs, which shift basally, i.e. to higher frequencies with increasing stimulus levels. The shift in cochlear position seen in the AM-FMTCs corresponds to a smaller shift than that observed for the pure-tone ANN. In summary, we conclude that the neurophonits evoked by AM high-frequency signals are equivalent to those evoked by pure-tone signals at frequencies corresponding to the modulation frequencies of the AM signals. They are hypothesized to arise from the spatial summation of auditory
nerve activity phase-locked to the envelope of the stimulus. Like the pure-tone evoked responses, each AM neurophonic arises from a population of fibers which has a limited distribution along the cochlear spiral and which is centered at or very near the point of maximum excitation produced by the spectral components in the stimulus. However, unlike the pure-tone population the population contributing to the AM response has a limited distribution corresponding to the cochlear place which is maximally excited by the carrier frequency, even at fairly high-stimulus levels. At high-stimulus levels, the contributing AM population shifts slightly toward the apex in contrast to the pure-tone neurophonic which expands significantly (up to one octave) towards the cochlear base. Acknowledgements The authors would like to thank Thomas Chimento for comments on the manuscript. This work was supported by NIH grant NS-16361 and the Coleman Fund. References Abbas, P.J. (1984) Recovery from long-term and short-term adaptation of the whole nerve action potential. J. Acoust. Sot. Am. 74. 1541-1547. Abbas. P.J. and Gorga, M.P. (1981) AP responses in forward masking paradigms and their relationship to responses of auditory nerve fibers. J. Acoust. Sot. Am. 69, 492-499. Antoli-Candela, F. and Kiang. N.Y.S. (1974) Unit activity underlying N, potential. In: R.F. Nauton and C. Fernandez (Eds.). Evoked Electrical Activity in the Auditory Nervous system, Academic Press, New York, London, pp. 165-189. Don, M. and Eggermont, J.J. (1978) Analysis of the clickevoked brain stem potentials in man using high-pass noise masking. J. Acoust. Sot. Am. 63, 1084-1092. Elliot, D.N., Stein, L. and Harrison, M.J. (1960) Discrimination of absolute-intensity thresholds and frequency-difference thresholds in cats. J. Acoust. Sot. Am. 32, 380-384. Evans. E.F. and Elberling, C. (1982) Location specific components of the gross cochlear action potential. Audiology 21, 204-227. Gardi, J. and Merzenich, M.M.M. (1979) The effects of highpass noise on the scalp-recorded frequency following response (FFR) in humans and cats. J. Acoust. Sot. Am 65, 1491-1500. Greenberg, S., Marsh, J.T., Brown, W.S. and Smith. 3.C. (1987) Neural temporal coding of low pitch. I. Human frequency-
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25.
Harris.
D.M.
and Dalla.
P. (1979)
Forward
masking of audi-
tory RCIW fiber responses.J. Neurophysioi. Klang.
Sach>. M.B. (1YXl)
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~~teristt~-frequents
Yl-114.
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(1984)
information.
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Bethesda. Maryland.
III.
42. 10X3- 1107.
neural processing of auditor! (Ed.).
American
Handbook
SOCICI~.
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C.E. and Urhas. J.V. modulation
Anterior
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R.L.
(1977)
nerve fibers:
Javol. E. (1980) Coding of Ahl tones on the chinchilla nerve: Implications
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Smith.
for pitch of complex
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Res. 4. 309-324.
plitude
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122.
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Marsh.
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Stillman.
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