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Operating range and maximum response of single auditory nerve fibers
Bram Research, 184 (1980) 499-505 © Elsevier/North-Holland Biomedical Press
499
Operating range and maximum response of single auditory nerve fibers
ROBERT L. SMITH and MICHAEL L. BRACHMAN Institute ./or Sensory Research, Syracuse University, Syracuse, N.Y. 13210 (U.S.A.)
(Accepted November 1st, 1979)
Key words: auditory nerve - - elgth nerve - - dynamic range - - transient response - - operating range
cochlear nerve - - hearing - - intensity coding
Although the auditory system operates over an intensity range of 120 dB, a single auditory nerve fiber is generally considered to have an operating range of 20-50 dBS, 7. The estimate for an individual fiber is based on the range of sound intensity levels over which the average or steady-state firing rate increases with sound intensity, i.e. the range of intensities between threshold and saturation. However, auditory nerve responses also exhibit dynamic or transient components3,6,15. The purpose of this communication is to describe some situations where the operating range determined from the dynamic or onset response significantly exceeds that determined from the steady-state response. The data come from single units of the auditory nerve of Mongolian gerbils anesthetized with sodium pentobarbital. Glass micropipettes were inserted into the nerve, using the ventral approach developed by Sokolich la,14. The experimental techniques are described in more detail elsewhereg, 11. Responses were analyzed in the form of post-stimulus-time (PST) histograms, from which the number of spikes per bin and the firing rate in spikes per second were obtained. The latter was computed by dividing the number of spikes per bin by the product of the bin width and number of stimulus repetitions. Driven responses were determined by subtracting the spontaneous rate from the total number of spikes per second. For present purposes, the term steady state is applied to firing rates measured at least 30 msec after the onset of a stimulus. Although the response continues to decrease beyond that interval, the shape of the rate-intensity function appears to remain unchanged after the first few msec of response, as is discussed below. The onset response is defined as the maximum in firing rate that occurs near the onset of a stimulus and depends to some extent on the size of the time window over which responses are averaged. Since the location of the window varies somewhat with intensity, maxima are always located and computed from PST histograms with bin widths significantly smaller than the specified time window. The
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Fig 1. PST histograms showing the time course of the responses to wide-band noise bursts for various conditions. Sound-intensity level is 21 dB for the left-hand column and 53 dB for the right. Upper row" responses to 80 msec stlmuh with 'fast' rise-fall times (nominally l0/tsec). Bin width equals 1.28 msec Middle row: onset portions of the responses in the upper row. Bin width equals 160 ttsec. Lower row: responses to stimuh with 25 msec rise-fall times. Umt Ge-55-11 : CF -- 10 4 kHz.
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Fig 2. Plots of onset vs steady-state response for unit of Fzg 1 and the 'fast' rise-time stimulus. The onset response is the maximum firmg rate computed using a t~me window of the duration indicated. Tbe dashed lines are explained in the text.
results are characteristic of all the units whose responses were analyzed in the described manner, presently more than 50 units in 14 animals. Acoustic stimuli were produced by a 1/2 in Bruel and Kjaer condenser microphone housed in a hollow ear bar. After removal of the pinna, the ear bar was pressed and sealed against the external ear canal to obtain a closed acoustic system. Stimuli were characteristic frequency (CF) tones and noise bursts whose envelopes were shaped by Grason-Stadler electronic switches (model 829D or 1287B). Unless otherwise noted, the tone bursts had rise-fall times of 2.5 msec, while the noise bursts had 'fast' (i.e. nominally 10 #sec) rise-fall times. The noise was produced by a Grason-Stadler 455 C noise generator, using the 20 k H z setting and had a fairly fiat stapes velocity characteristic between 2 and 15 k H z l k Stimulus ]ntensities were specified either as sound intensity levels (IL), relative to the approximate threshold of a unit, or as sound pressure levels (SPL) near the tympanic membrane as determined from a median calibration curveL Stimulus durations ranged from 60 to 300 msec with the longer stimuli being repeated once per sec, and the shorter, up to 3 times per sec. In response to stimuli of constant sound intensity, auditory nerve fibers produce a maximum firing rate at onset followed by a decay or adaptation toward a steadystate. The PST histograms in the upper row of Fig. 1 are typical of those produced by tone or noise bursts with rise times of several msec or less~, a. It can be seen that the histogram on the left (Fig. 1A) closely resembles that on the right (Fig. IB), even though the ILs are 21 dB and 53 dB, respectively. For this unit an I L of 21 dB appears
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F~g. 3. Plots of driven response vs sound intensity level for a variety o f e x p e r mental c o n d m o n s The unfilled circles give the onset responses computed using intervals of a b o u t 1 msec. The filled c~rcles are steady-state responses multiphed by the indicated constants as discussed m the text The crosses are onset responses for stimuli with 25 msec rise t~mes (LRT), computed using 5 12 msec intervals. A : u m t Ge-55-11 of Figs. I and 2: spontaneous activity (SPA) equals 55 splkes/sec B: unit Ge-55-12: C F 2 02 kHz; 0 dB 1L -- 1 dB SPL; SpA -- 29 spikes/sec. C: umt Ge-30-7: CF 1.70 kHz; SpA 54 sp]kes/sec; 0 dB IL -- - - 8 dB SPL D- umt Ge-30-3: C F -- 15 7 k H z ; SpA 76 splkes/sec; 0 dB IL -- 40 dB SPL.
sufficient to produce a saturation of both steady-state and onset firing rates, but closer inspection of the first few msec of the responses reveals that differences occur m spite of the apparent saturation. The histograms in the middle row of Fig 1 are the initial portions of the responses shown in the top row, with the bm width reduced by a factor of 8. A 'neural-ringing' can be observed which may result from an interaction between refractory recovery and spike synchronization to the stimulus onset2,~, 8. For present purposes the important observation is that the height of the first peak in Fig. 1D ]s much greater than that in Fig. 1C. Hence, when sufficiently small bin widths are used, the onset response appears to continue to grow wtth intensity even though other measures of response have saturated. Differences in the growth of onset and steady-state responses can be demonstrated in more detail by plotting the onset firing rate vs steady-state for a number of
503 intensities. For example, in Fig. 2 each circle gives the onset and steady-state firing rates produced at a single intensity for the unit of Fig. 1. The arrows show the direction of increasing intensity. The onset rate was determined using a bin width of about I msec, a time window which roughly corresponds to the first mode in histograms such as those of Figs. 1C and D. The circles follow a monotonically increasing, positively accelerated function indicating that the ratio of onset to steady-state response increases with increasing sound intensity. When such data is viewed in terms of driven responses, a typical pattern emerges. In Fig. 2 the vertical cross has ordinate and abscissa values equal to the spontaneous rate of the unit so that each dashed line represents a constant ratio of driven responses. As can be seen, there exists a range of intermediate intensities where the ratio of driven onset to steady-state response is constant. At higher intensities the ratio increases. This pattern was observed in about 80 ~o of the units studied and some additional examples are given below. The pattern occurred m response to tone and noise bursts and appeared independent of CF although some units did not exhibit neural ringing in response to CF tones. In the remaining units, the points fell on a straight line for all intensities although intensities high enough to produce the positive acceleration may not always have been applied. The unit in Fig. 1 also shows a decrease in ratio at the lowest intensity which seemed to occur in some units but was not investigated in detail. Finally, the behavior of the onset response using a 1 msec window can be compared to that observed using a 10 msec window and is indicated by the triangles. For this unit, and m general, the ratio of driven onset to steady-state response was approximately constant for the 10 msec window in agreement with previous results s,tl. Hence, the triangles fall close to the lower dashed line. A more detailed analysis of results from several units, including that of Fig. 2, in&cates that beyond the first 2 msec of response the ratio of driven responses is independent of sound intensity. Consequently, the ratio of onset to steady-state response approaches the same value at all intensities as window size increases beyond 2 msec. According to the results described above, onset and steady-state rate-intensity functions have similar shapes at low intensities where the ratio of driven responses is constant. Since the ratio of responses increases at higher intensities, the onset function must grow at a relatively greater rate than does the steady-state function. In the situation where the steady-state response saturates, an increasing ratio implies that the onset response continues to increase and consequently exhibits a greater operating range. These relationships are illustrated for some typical units by the rate-intensity functions of Fig. 3. In Fig. 3A-C the steady-state rates have been multiplied by the appropriate constant so that the onset and steady-state functions coincide at low intensities. At the higher intensities the two functions diverge and the onset functions show less negative acceleration. In some of the units showing these effects, it was difficult to evaluate the increase in operating range since the onset rate saturated (e.g. Fig. 3A) or the steady-state rate showed a sloping saturation (Fig. 3C). However, about half of the units showed more explicit effects. For example, in Fig. 3B the steady-state rate appears to saturate near an intensity level of 20 dB, while the onset rate continues to increase monotonically for at least another 30 dB. A still greater
504 contrast is shown in Fig. 3D which is typical of some umts with high spontaneous rates. The steady-state response shows little reliable increase with intensity over the range shown, while the onset response increases monotonically over at least 50dB. The apparent increase m operating range is not hmlted to onset responses produced by stimuli with short rise tmaes. In several units, tone or noise bursts with long rise times, on the order of 25 msec, were applied producing results such as those in Fig. 1E and F where the ILs were the same as in Fig. 1A and B. The PSTs show a rise to a maximum followed by a decay toward a steady state. As intensity increases, the time delay to the maximum decreases and the height of the onset response increases. By comparing Figs. 1E and F, it can be seen that the onset response continues to increase in spite of the steady-state saturation. This increase in operating range is illustrated by the rate-intensity function in Fig. 3A. The crosses show the onset rate-intensity function in response to the stimuli with long rise times where the maximum rate was measured over a 5 msec interval. Surprisingly, this onset function appears to be proportional to that obtained with the shorter rise time and smaller bin width over much of the intensity range. To facihtate comparison, the rates were multiplied by an appropriate constant. A second example is shown m Fig. 3B, where the two onset functions have an even greater similarity. This report presents two examples of the differences between the dynamic and steady-state behavior of auditory nerve fibers. Taken alone, either of the results could be interpreted in terms of a specific mechanism that applied to a limited set of conditions. For example, the high onset peak in the response to stimuli with short rise times (Fig. 1C and D) is undoubtedly influenced by the synchronization between the stimulus onset and the first spike of the response. Latency histograms indicate that the first mode of the PST is almost entirely determined by the first spike 8. If the synchronization improved as the intensity increased, this spike would fall in a smaller and smaller time window resulting in an apparent increase m the computed number of spikes per second. Under these conditions it may be more appropriate to refer to the response as a probability of occurrence rather than a firing rate. On the other hand, the onset response for stimuli with long rise times can be explained in a rather different way x0. Previous results have suggested that, in the auditory periphery, a static saturation is followed by additive adaptation s-11. For a stimulus with a long rise time, as intensity is increased, saturation can occur earlier and earlier in the rising portion of the stimulus envelope causing the t~me delay to the peak to decrease. In addition, the amount of adaptation at the time of the maximum decreases since the duration of prior stimulation decreases, allowing the maximum rate to increase. Hence, a static saturation followed by adaptation produces a dynamic range that exceeds that of the static saturation alone. It is conceivablethat the same kinds of effects occur, albeit on a more rapid time scale, m response to the stimuli w~th shorter rise times. However, preliminary results, using slnusoidal amplitude modulation, suggest that neither of these explanations is sufficient and that an additional dynamic process is present which contributes to the response to rapidly time-varying stimuli. The operating range determined with the modulated stimuli appears larger than that predicted from the steady-state rate-intensity function and is closely related to the onset functionL
505 Questions remain concerning the extent and magnitude o f the dynamic effects. They must be investigated over a wider range of intensities, a larger n u m b e r of units, and in different species. I n the latter regard, previous results suggest that onset effects in the guinea pig are less prominent t h a n in the gerbilll,xL Furthermore, in apparent disagreement with our results, O z d a m a r and Dallos 4 indicate that onset responses in the gerbil have dynamic ranges o f only 20 dB. However, they used shorter inter-burst intervals than we did and their onset responses may have been reduced by adaptation6,L Based on the results we have reported above, we conclude that dynamic response characteristics may play a significant role in blidging the gap between the steady-state operating range of single units and the overall range of the auditory system. This research was supported by N S F G r a n t BNS76-14354 and N I H G r a n t NS03950.
1 Brachman, M. L. and Smith, R. L , Dynamic versus static characteristics of single auditory-nerve fibers, Neurosci. Abstr., 5 (1979) 16. 2 Goldstein, M. R and Kiang, N. Y. S., Synchrony of neural activity in electrical responses evoked by transient acoustic stimuli, J. acoust. Soc. Amer., 30 (1958) 107-114. 3 Nomoto, M., Suga, N. and Katsuki, Y., Discharge pattern and inhibition of primary auditorynerve fibers in the monkey, J. Neurophysiol.,. 27 (1964) 768-787. 40zdamar, O. and Dallos, P., Synchronous responses of the primary auditory fibers to the onset of tone burst and tb.elr relation to compound action potentials, Brain Research, 155 (1978) 169-175. 5 Klang, N. Y. S., A survey of recent developments in the study of auditory physiology, Ann. Otol. (St. Louis), 77 (1968) 656-675. 6 Klang, N. Y. S., Watanabe, T., Thomas, E. C. and Clark, L. F , Discharge Patterns of Single Fiber~ in the Cat's Auditory Nerve, Res. Monograph 35, MIT Press, Cambridge, Mass., 1965. 7 Sachs, M. B. and Abbas, P. J., Rate versus level functions for auditory-nerve fibers in cats: tone burst stimuli, J. acoust. Soc. Amer., 56 (1974) 1835-1847. 8 Smith, R. L., Short-Term Adaptation and Incremental Responses in Single Auditory-Nerve Fibers, P h . D . Dissertation and Special Report LSC-S-11 Institute for Sensory Research, Syracuse University, Syracuse, N.Y., 1973. 9 Smith, R. L., Short-term adaptation in single auditory-nerve fibers: some poststimulatory effects, J. Neurophysiol, 40 (1977) 1098-1112. 10 Smith, R L.,Someeffectsofstlmulusrlsetimeonresponsesofauditory-nervefibers,J.acoust.Soc. Amer., 65 (1979) S 83. 11 Smith, R. L., Adaptation, saturation, and physiological masking in single auditory-nerve fibers, J. acoust. Soc. Amer., 65 (1979) 166-178. 12 Smith, R. L. and Zwislocki, J. J., Short-term adaptatmn and incremental responses in single auditory-nerve fibers, Biol. Cyber., 17 (1975) 169-182 13 Sokolich, W. G., Some Electrophysiological Evidence for a Polarity Opposttion Mechanism of lnteraction between Inner and Outer Hair Cells in the Cochlea, Ph D. Dissertation and Special Report ISR-S-15, Institute for Sensory Research, Syracuse University, Syracuse, N.Y., 1977. 14 Sokolich, W. G. and Smith, R. L., Easy access to the auditory nerve m the Mongolian gerbil, J. acoust. Soc. Amer , 54 (1973) 283. 15 Tasakl, I., Nerve impulses in individual auditory-nerve fibers of guinea pig, J Neurophystol., 17 (1954) 97-122.
499
Operating range and maximum response of single auditory nerve fibers
ROBERT L. SMITH and MICHAEL L. BRACHMAN Institute ./or Sensory Research, Syracuse University, Syracuse, N.Y. 13210 (U.S.A.)
(Accepted November 1st, 1979)
Key words: auditory nerve - - elgth nerve - - dynamic range - - transient response - - operating range
cochlear nerve - - hearing - - intensity coding
Although the auditory system operates over an intensity range of 120 dB, a single auditory nerve fiber is generally considered to have an operating range of 20-50 dBS, 7. The estimate for an individual fiber is based on the range of sound intensity levels over which the average or steady-state firing rate increases with sound intensity, i.e. the range of intensities between threshold and saturation. However, auditory nerve responses also exhibit dynamic or transient components3,6,15. The purpose of this communication is to describe some situations where the operating range determined from the dynamic or onset response significantly exceeds that determined from the steady-state response. The data come from single units of the auditory nerve of Mongolian gerbils anesthetized with sodium pentobarbital. Glass micropipettes were inserted into the nerve, using the ventral approach developed by Sokolich la,14. The experimental techniques are described in more detail elsewhereg, 11. Responses were analyzed in the form of post-stimulus-time (PST) histograms, from which the number of spikes per bin and the firing rate in spikes per second were obtained. The latter was computed by dividing the number of spikes per bin by the product of the bin width and number of stimulus repetitions. Driven responses were determined by subtracting the spontaneous rate from the total number of spikes per second. For present purposes, the term steady state is applied to firing rates measured at least 30 msec after the onset of a stimulus. Although the response continues to decrease beyond that interval, the shape of the rate-intensity function appears to remain unchanged after the first few msec of response, as is discussed below. The onset response is defined as the maximum in firing rate that occurs near the onset of a stimulus and depends to some extent on the size of the time window over which responses are averaged. Since the location of the window varies somewhat with intensity, maxima are always located and computed from PST histograms with bin widths significantly smaller than the specified time window. The
500
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Fig 1. PST histograms showing the time course of the responses to wide-band noise bursts for various conditions. Sound-intensity level is 21 dB for the left-hand column and 53 dB for the right. Upper row" responses to 80 msec stlmuh with 'fast' rise-fall times (nominally l0/tsec). Bin width equals 1.28 msec Middle row: onset portions of the responses in the upper row. Bin width equals 160 ttsec. Lower row: responses to stimuh with 25 msec rise-fall times. Umt Ge-55-11 : CF -- 10 4 kHz.
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Ge-55-11
00 ~ ~ ~ J I00 200 STEADY STATE RESPONSE IN SPIKES PER SECOND
Fig 2. Plots of onset vs steady-state response for unit of Fzg 1 and the 'fast' rise-time stimulus. The onset response is the maximum firmg rate computed using a t~me window of the duration indicated. Tbe dashed lines are explained in the text.
results are characteristic of all the units whose responses were analyzed in the described manner, presently more than 50 units in 14 animals. Acoustic stimuli were produced by a 1/2 in Bruel and Kjaer condenser microphone housed in a hollow ear bar. After removal of the pinna, the ear bar was pressed and sealed against the external ear canal to obtain a closed acoustic system. Stimuli were characteristic frequency (CF) tones and noise bursts whose envelopes were shaped by Grason-Stadler electronic switches (model 829D or 1287B). Unless otherwise noted, the tone bursts had rise-fall times of 2.5 msec, while the noise bursts had 'fast' (i.e. nominally 10 #sec) rise-fall times. The noise was produced by a Grason-Stadler 455 C noise generator, using the 20 k H z setting and had a fairly fiat stapes velocity characteristic between 2 and 15 k H z l k Stimulus ]ntensities were specified either as sound intensity levels (IL), relative to the approximate threshold of a unit, or as sound pressure levels (SPL) near the tympanic membrane as determined from a median calibration curveL Stimulus durations ranged from 60 to 300 msec with the longer stimuli being repeated once per sec, and the shorter, up to 3 times per sec. In response to stimuli of constant sound intensity, auditory nerve fibers produce a maximum firing rate at onset followed by a decay or adaptation toward a steadystate. The PST histograms in the upper row of Fig. 1 are typical of those produced by tone or noise bursts with rise times of several msec or less~, a. It can be seen that the histogram on the left (Fig. 1A) closely resembles that on the right (Fig. IB), even though the ILs are 21 dB and 53 dB, respectively. For this unit an I L of 21 dB appears
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F~g. 3. Plots of driven response vs sound intensity level for a variety o f e x p e r mental c o n d m o n s The unfilled circles give the onset responses computed using intervals of a b o u t 1 msec. The filled c~rcles are steady-state responses multiphed by the indicated constants as discussed m the text The crosses are onset responses for stimuli with 25 msec rise t~mes (LRT), computed using 5 12 msec intervals. A : u m t Ge-55-11 of Figs. I and 2: spontaneous activity (SPA) equals 55 splkes/sec B: unit Ge-55-12: C F 2 02 kHz; 0 dB 1L -- 1 dB SPL; SpA -- 29 spikes/sec. C: umt Ge-30-7: CF 1.70 kHz; SpA 54 sp]kes/sec; 0 dB IL -- - - 8 dB SPL D- umt Ge-30-3: C F -- 15 7 k H z ; SpA 76 splkes/sec; 0 dB IL -- 40 dB SPL.
sufficient to produce a saturation of both steady-state and onset firing rates, but closer inspection of the first few msec of the responses reveals that differences occur m spite of the apparent saturation. The histograms in the middle row of Fig 1 are the initial portions of the responses shown in the top row, with the bm width reduced by a factor of 8. A 'neural-ringing' can be observed which may result from an interaction between refractory recovery and spike synchronization to the stimulus onset2,~, 8. For present purposes the important observation is that the height of the first peak in Fig. 1D ]s much greater than that in Fig. 1C. Hence, when sufficiently small bin widths are used, the onset response appears to continue to grow wtth intensity even though other measures of response have saturated. Differences in the growth of onset and steady-state responses can be demonstrated in more detail by plotting the onset firing rate vs steady-state for a number of
503 intensities. For example, in Fig. 2 each circle gives the onset and steady-state firing rates produced at a single intensity for the unit of Fig. 1. The arrows show the direction of increasing intensity. The onset rate was determined using a bin width of about I msec, a time window which roughly corresponds to the first mode in histograms such as those of Figs. 1C and D. The circles follow a monotonically increasing, positively accelerated function indicating that the ratio of onset to steady-state response increases with increasing sound intensity. When such data is viewed in terms of driven responses, a typical pattern emerges. In Fig. 2 the vertical cross has ordinate and abscissa values equal to the spontaneous rate of the unit so that each dashed line represents a constant ratio of driven responses. As can be seen, there exists a range of intermediate intensities where the ratio of driven onset to steady-state response is constant. At higher intensities the ratio increases. This pattern was observed in about 80 ~o of the units studied and some additional examples are given below. The pattern occurred m response to tone and noise bursts and appeared independent of CF although some units did not exhibit neural ringing in response to CF tones. In the remaining units, the points fell on a straight line for all intensities although intensities high enough to produce the positive acceleration may not always have been applied. The unit in Fig. 1 also shows a decrease in ratio at the lowest intensity which seemed to occur in some units but was not investigated in detail. Finally, the behavior of the onset response using a 1 msec window can be compared to that observed using a 10 msec window and is indicated by the triangles. For this unit, and m general, the ratio of driven onset to steady-state response was approximately constant for the 10 msec window in agreement with previous results s,tl. Hence, the triangles fall close to the lower dashed line. A more detailed analysis of results from several units, including that of Fig. 2, in&cates that beyond the first 2 msec of response the ratio of driven responses is independent of sound intensity. Consequently, the ratio of onset to steady-state response approaches the same value at all intensities as window size increases beyond 2 msec. According to the results described above, onset and steady-state rate-intensity functions have similar shapes at low intensities where the ratio of driven responses is constant. Since the ratio of responses increases at higher intensities, the onset function must grow at a relatively greater rate than does the steady-state function. In the situation where the steady-state response saturates, an increasing ratio implies that the onset response continues to increase and consequently exhibits a greater operating range. These relationships are illustrated for some typical units by the rate-intensity functions of Fig. 3. In Fig. 3A-C the steady-state rates have been multiplied by the appropriate constant so that the onset and steady-state functions coincide at low intensities. At the higher intensities the two functions diverge and the onset functions show less negative acceleration. In some of the units showing these effects, it was difficult to evaluate the increase in operating range since the onset rate saturated (e.g. Fig. 3A) or the steady-state rate showed a sloping saturation (Fig. 3C). However, about half of the units showed more explicit effects. For example, in Fig. 3B the steady-state rate appears to saturate near an intensity level of 20 dB, while the onset rate continues to increase monotonically for at least another 30 dB. A still greater
504 contrast is shown in Fig. 3D which is typical of some umts with high spontaneous rates. The steady-state response shows little reliable increase with intensity over the range shown, while the onset response increases monotonically over at least 50dB. The apparent increase m operating range is not hmlted to onset responses produced by stimuli with short rise tmaes. In several units, tone or noise bursts with long rise times, on the order of 25 msec, were applied producing results such as those in Fig. 1E and F where the ILs were the same as in Fig. 1A and B. The PSTs show a rise to a maximum followed by a decay toward a steady state. As intensity increases, the time delay to the maximum decreases and the height of the onset response increases. By comparing Figs. 1E and F, it can be seen that the onset response continues to increase in spite of the steady-state saturation. This increase in operating range is illustrated by the rate-intensity function in Fig. 3A. The crosses show the onset rate-intensity function in response to the stimuli with long rise times where the maximum rate was measured over a 5 msec interval. Surprisingly, this onset function appears to be proportional to that obtained with the shorter rise time and smaller bin width over much of the intensity range. To facihtate comparison, the rates were multiplied by an appropriate constant. A second example is shown m Fig. 3B, where the two onset functions have an even greater similarity. This report presents two examples of the differences between the dynamic and steady-state behavior of auditory nerve fibers. Taken alone, either of the results could be interpreted in terms of a specific mechanism that applied to a limited set of conditions. For example, the high onset peak in the response to stimuli with short rise times (Fig. 1C and D) is undoubtedly influenced by the synchronization between the stimulus onset and the first spike of the response. Latency histograms indicate that the first mode of the PST is almost entirely determined by the first spike 8. If the synchronization improved as the intensity increased, this spike would fall in a smaller and smaller time window resulting in an apparent increase m the computed number of spikes per second. Under these conditions it may be more appropriate to refer to the response as a probability of occurrence rather than a firing rate. On the other hand, the onset response for stimuli with long rise times can be explained in a rather different way x0. Previous results have suggested that, in the auditory periphery, a static saturation is followed by additive adaptation s-11. For a stimulus with a long rise time, as intensity is increased, saturation can occur earlier and earlier in the rising portion of the stimulus envelope causing the t~me delay to the peak to decrease. In addition, the amount of adaptation at the time of the maximum decreases since the duration of prior stimulation decreases, allowing the maximum rate to increase. Hence, a static saturation followed by adaptation produces a dynamic range that exceeds that of the static saturation alone. It is conceivablethat the same kinds of effects occur, albeit on a more rapid time scale, m response to the stimuli w~th shorter rise times. However, preliminary results, using slnusoidal amplitude modulation, suggest that neither of these explanations is sufficient and that an additional dynamic process is present which contributes to the response to rapidly time-varying stimuli. The operating range determined with the modulated stimuli appears larger than that predicted from the steady-state rate-intensity function and is closely related to the onset functionL
505 Questions remain concerning the extent and magnitude o f the dynamic effects. They must be investigated over a wider range of intensities, a larger n u m b e r of units, and in different species. I n the latter regard, previous results suggest that onset effects in the guinea pig are less prominent t h a n in the gerbilll,xL Furthermore, in apparent disagreement with our results, O z d a m a r and Dallos 4 indicate that onset responses in the gerbil have dynamic ranges o f only 20 dB. However, they used shorter inter-burst intervals than we did and their onset responses may have been reduced by adaptation6,L Based on the results we have reported above, we conclude that dynamic response characteristics may play a significant role in blidging the gap between the steady-state operating range of single units and the overall range of the auditory system. This research was supported by N S F G r a n t BNS76-14354 and N I H G r a n t NS03950.
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