Recovery from short-term adaptation in single neurons in the cochlear nucleus
Flint A. Boettcher, Richard J. Salvi and Samuel S. Saunders Hearing Research Laboratory, Department of Communicatioe Disorders and Sciences, SUNY-Buffalo, Buffalo, New York, U.S.A.
(Received 9 January 1990; accepted 28 March 1990)
Recovery from short-term adaptation was measured in single neurons in the cochlear nucleus using a forward masking stimulus paradigm. The response to a short-duration, low-level probe tone at a unit's characteristic frequency (CF) was measured before and after presentation of a masker tone at the unit's CF. The degree of adaptation was defined as the ratio of firing to the probe in the adapted and unadapted conditions. The level of the masker and time difference between the masker offset and probe onset ('DT') were varied. As DT increased, the response to the probe increased in most Primarylike, Primarylike-notch, and Chopper units. Recovery was approximately linear in log time for most of these units. However, approximately half the Pauser/Bnildup and On units showed very different recovery patterns, ranging from no adaptation to very non-linear recovery patterns. The results suggest that little alteration in the recovery process occurs between the auditory nerve and Primarylike, Primarylike-notch, and Chopper units, but that significant changes in the recovery process occur in Pauser-Buildup and On units.
Adaptation; Auditory nerve; Cochlear nucleus; Forward masking; Single unit
Introduction
The fo rward mask ing p a r a d i g m has been used in m a n y psychophys ica l exper iments to s tudy the t empora l resolving power of the aud i to ry sys tem (Zwislocki et al., 1959; Ell iot t , 1962; K i d d and Fe th , 1982; W i d i n and Viemeister , 1982; Nef f and Jes teadt , 1983). In most psychophys ica l experi- men t s using fo rward masking, the threshold for de tec t ing a br ief p robe s t imulus is de t e rmined in the presence of an in tense maske r s t imulus which precedes the probe . As the t empora l sepa ra t ion be tween masker and p r o b e (DT) increases, the threshold of the p robe decreases and approx i - mates quie t th reshold at a D T of 200-300 ms (Zwislocki et al., 1959; Elliott , 1962; W i d i n and Viemeister , 1982). Several others, using a f ixed p r o b e level and var iab le masker level, have also shown that fo rward mask ing does no t occur be-
Correspondence to: F.A. Boettcher, Hearing Research Labora- tory, 215 Parker Hall, SUNY-Buffalo, Buffalo, NY 14214, U.S.A.
y o n d a m a s k e r - p r o b e s e p a r a t i o n of severa l hund re d ms (Nelson and F r e y m a n , 1987; Car lyon , 1988).
The fo rward mask ing p a r a d i g m has also been used in phys io logica l exper imen t s to m o n i t o r the recovery f rom shor t - t e rm a d a p t a t i o n at the single neuron level. The recovery f rom shor t - t e rm adap - ta t ion is expressed b y a g radua l increase in f i r ing ra te as the t ime in terval be tween maske r offset and p r o b e onset increases (Smith, 1977; 1979; Har r i s and Dal los , 1979). Superf ic ia l ly , the single uni t results ob t a ined f rom the aud i to ry nerve have some in teres t ing para l le l s wi th the psychophys ica l data , i.e., mask ing and a d a p t a t i o n decrease as the D T increases and recovery typ ica l ly takes 200 -300 ms in bo th doma ins (Har r i s and Dal los , 1979; Salvi et al., 1986). Thus, the psychophys ica l term, fo rward m a s k i n g , has f requent ly been used inter- changeab ly with the concep t of shor t - t e rm a d a p t a - t ion in physiology.
Desp i te the qual i ta t ive s imilar i t ies be tween shor t - t e rm a d a p t a t i o n at the aud i to ry nerve and fo rward mask ing in the psychophys ica l doma in ,
there are some critical quantitative differences be- tween the psychophysical and single unit data. For example, 'masking' at the single unit level is limited to a range of less than 50 dB re threshold, whereas the psychophysical dynamic range is much wider, typically 80 dB or greater. Similarly, the effect of masker duration extends over a much longer time interval in the psychophysical domain (up to 1000 ms) than at the physiological level (usually less than 150 ms). Relkin and Turner (1988), using an adaptive procedure to measure forward masking, reported that the amount of masking in auditory nerve units was never greater than 21 dB. In addition, Carlyon (1988) has sug- gested that recovery is a linear in log time process in psychophysics and an exponential process in the auditory nerve. These discrepancies suggest that central auditory system may influence for- ward masking, and thus fine temporal resolution, more than was previously believed.
It has been suggested that the recovery from forward masking may be explained by properties of the inner hair cell-auditory nerve fiber synapse (Westerman and Smith, 1987). However, the elec- trical stimulation literature provides several inter- esting results suggesting a central component to forward masking. Fredrickson and Gerken (1978) reported that the behavioral threshold for detect- ing electrical stimulation of the cochlear nucleus was increased if the electrical stimulus was pre- ceded by an acoustic stimulus. Since the electrical stimulus bypassed the hair cell-auditory nerve syn- apse, the effect of the masker likely occurred proximal to the auditory nerve. Shannon (1983) described 'forward masking' of electrical stimula- tion in several patients with cochlear implants. In this case, both the 'masker' and the 'probe ' were electrical stimuli which activated the auditory nerve directly since the hair cells were missing. Interestingly, the time needed for complete re- covery of sensitivity exceeded the values reported for acoustic stimulation.
Based on the discrepancies between the psycho- physical and auditory nerve data, it would appear that the central auditory pathway contributes to the psychophysical phenomenon of forward mask- ing. Exactly how the central pathways contribute to the phenomenon of forward masking is not yet understood since there have been few systematic
studies of recovery from short-term adaptation in the central auditory pathway. Thus, the purpose of this experiment was to examine recovery from short-term adaptation at the single unit level of the CN and to compare data with that previously collected for the auditory nerve.
To our knowledge, only two studies have used the forward masking stimulus paradigm to ex- amine the recovery from short-term adaptation proximal to the auditory nerve. Watanabe and Simada (1971) used a noise masker plus a probe tone at unit characteristic frequency and measured the recovery of threshold in units in the cochlear nucleus (CN) and the inferior colliculus (IC). The threshold decreased as the interval between masker and probe increased. Unfortunately, the data from different classes of units were not compared quantitatively. Schreiner (1980) reported on re- covery from adaptation in single units of the me- dial geniculate body. His results suggested that post-stimulus suppression, as well as short-term adaptation, contributed to ' forward masking' ef- fects.
Methods
Subjects and surgery Healthy chinchillas (Chinchilla lanigera) aged
1-2 years were used as subjects. All animals were anesthetized initially with a mixture of ketamine (35 mg/kg) and xylazine (1 mg/kg). Ketamine (30 mg/kg) was then administered every 1-2 h throughout each experiment to maintain a steady level of anesthesia. Each subject was tracheoto- mized to prevent obstruction of the airway. The right pinna and bony ear canal were removed in order to place the sound source with probe tube close to the tympanic membrane. A 25 gauge needle was inserted into the bulla to prevent the buildup of negative middle ear pressure.
A silver ball electrode was placed on the round window to monitor the whole-nerve action poten- tial (AP). The threshold of the AP was determined using clicks generated by a pulse generator (0.1 ms positive electric pulses). The electrical signal from the round window was amplified (50,000 times), filtered (30-3,000 Hz pass; Grass P511 amplifier), and relayed to an oscilloscope (Tetronix, 5440). If the visual detection threshold of the AP increased
by more than 10 dB, the experiment was terminated. Furthermore, if at any time unit thresholds exceeded the range reported by Salvi et al. (1978), the experiment was terminated. This prevented the possibility that the AP response elicited by clicks remained unchanged while local- ized regions of the cochlea shifted in sensitivity.
A dorsoposterior approach to the CN was utilized. The bone overlying the cerebellum was removed. Portions of the cerebellum were aspirated in order to expose the dorsal cochlear nucleus. Glass micropipettes filled with 3M NaC1 and with resistances of 5-15 MI2 were utilized to record from single units in the CN. The electrode resis- tance was monitored throughout the experiment using the Dagan amplifier; if the resistance in- creased above 15 MI2, the electrode was withdrawn and a new electrode was substituted. This pre- vented the possibility that auditory nerve fibers were mistaken for CN units, since we are not able to record from nerve fibers with electrodes that have resistances less than 20 MI2. With the aid of an operating microscope, each electrode was di- rected toward the CN with a manual micro- manipulator. The electrode was advanced into the CN using a remote-controlled microdrive (Burleigh Inchworm or Trent-Wells hydraulic microdrive).
Spike discharges were amplified (Dagan Cell Explorer, Model 8700; ×10 output, 0 -3 kHz), relayed to an audio monitor (Grass AMB, 0.1 to 3 kHz, variable gain), and then fed in parallel to a window discriminator (W-P Instruments 120) and to an oscilloscope. The output of the window discriminator was relayed to a custom-built neural clock (10 Its resolution) located on the bus of a PDP 11/23 computer system. The data were stored on disc for off-line analysis.
Stimulus control Tones and broad-band noise generated by a
Wavetek function generator and a Rockland Pro- grammable Oscillator (Model 5100) were routed through electronic switches (Grason Stadler, Model 1287B) and then relayed through a mixer, custom-built programmable attenuators, a sum- ming amplifier, a power amplifier (Southwest Technical, Model 207A), a bias network with step- up transformer, and finally to the sound source located in a sound attenuating booth. The sound
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source was a modified Stax earphone similar to the design of Sokolich (1977). The earphone was calibrated using a probe tube microphone (Etymotics) placed in close proximity to the tympanic membrane of the animal. The duration and timing of the acoustic stimuli were under computer control.
Data collection Tone bursts (20 ms duration, rise-fall 1 ms)
were used as search stimuli while advancing the electrode into the CN. Once a single unit was encountered, spontaneous rate was measured over a 10 s interval. An automated tuning curve pro- gram (Salvi et al., 1978) was then utilized to determine the characteristic frequency (CF) and threshold of the unit. Threshold was based on a 1-spike increase in firing rate between the tone-on (50 ms) and tone-off (50-ms) intervals.
Classification stimuli Units were categorized based on the shape of
the PST histogram, using schemes described by several investigators (Pfeiffer, 1966; Godfrey et al., 1975a,b; Rhode et al., 1983a,b; Rhode and Smith, 1986a,b). In the first series of experiments, units were classified based on the shape of the PST histogram (500 gs bins) to the masker stimuli in the forward-masking paradigm (see below), pre- sented + 30 dB re threshold. In some experiments, classification was double-checked by examining the shape of the PST histogram (500 Its bins) to 25 ms tone bursts (200 presentations) presented at + 30 dB re unit threshold at CF. There were no differences in classification between the two pro- cedures. The resolution utilized in classification was much finer than that used in the Figures in the text (500 gs bins in classification and 2 ms bins in the Figtires) and it may be difficult to discriminate between unit types in the Figures. The larger bins were used in the Figures so that the entire stimulus cycle could be presented.
Forward masking stimuli All stimuli used in the forward masking para-
digm were pure tones. Both the probe and masker were presented at the CF of each unit. The stimu- lus paradigm for collecting ' forward masking' data is shown in Fig. 1. Each 1-second stimulus cycle
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quantified by the value of R-Pm/R-Pc.
consisted of a control probe (Pc: 20 ms, + 15 dB re threshold at CF), a masker (M: 100 ms, variable level), and a masked probe (Pm: identical char- acteristics as the control probe). Spontaneous rate was monitored in the first 20 ms of each cycle. The time between the offset of the masker and the onset of the masked probe (DT) was 2, 5, 10, 20, 40, 100, or 200 ms.
The 'forward masking' data were analyzed using spike counts obtained from PST liistograms with 2 ms bin widths. The metric for determining the extent of recovery from short-term adaptation was the 'normalized probe rate,' defined as the firing rate to the masked probe divided by the firing rate to the control probe. The analysis window was 20 ms for the control and masked probe responses. The duration of the window was constant for all responses, but the starting times for analysis were varied based on response latency, so that spike counting began at the beginning of each response.
R e s u l t s
A total of 115 units in the CN were studied using the forward masking stimulus paradigm. Units were segregated into five categories based on the shape of the PST histogram to tone bursts at unit CF. These categories were then used to organize the forward masking data.
Recovery functions
Primaryfike units A total of 38 Primarylike units were studied in
this experiment. The CFs ranged from 107 to 14,015 Hz, the thresholds ranged from - 5 to 40 dB SPL, and the SRs ranged from 0 to 136 spikes/s. Fig. 2 (left) shows PST histograms for one Primarylike unit (22.541), collected using the forward masking paradigm. Histograms are shown for six DT values, with the masker set at + 45 dB re threshold. Note that as the DT increased, the response to the masked probe increased. The re- covery functions for the unit, in the upper right of Fig. 2, show that as the DT decreased, the normal- ized probe rate decreased for a given masker level. In this example, increasing the masker intensity to levels above + 30 dB failed to depress the N P R further. For masker levels of + 30 dB and above, recovery was approximately linear in log time over the DT values of 10 to 200 ms. The majority of Primarylike units (89%) responded in a manner similar to unit 22.541; namely with linear recovery in log time. However, many Primarylike units showed a significant effect of masker level, such that increasing the masker intensity caused a de- crease in the NPR at a given DT.
Two Primarylike units had recovery functions which were not linear in log time. For example, the center right panel of Fig. 2 shows recovery functions for a Primarylike unit (22.001) which were approximately exponential in log time. Little recovery occurred over the first 40 ms for higher intensity maskers. This plateau was followed by very rapid recovery between 40 and 200 ms. Be- cause these two units with exponential recovery were atypical, the data were not included in the group data for Primarylike units shown below, nor were they included in the group regression analy- sis shown below.
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The group mean recovery functions for Primarylike units are shown in the lower fight panel of Fig. 2. As the masker level increased, the normalized probe rate tended to decrease at a given DT. For example, the average decrement in the probe response for a 5 ms DT ranged from approximately 21% at a masker level of + 15 dB to approximately 76% at a masker level of + 60 dB. The effect of masker level on the normalized probe rate was most pronounced at shorter DTs. At a given masker level, the N P R increased with the D T and recovery was approximately linear in log time. Quantitative measures of the group re- covery data are described below, with comparison of Primarylike units to other unit types.
Primarylike-notch units A total of 25 Primarylike-notch units were
studied. The CFs ranged from 261 to 12,156 Hz, the thresholds ranged from - 6 . 5 to 30 dB SPL, and the SRs ranged from 0 to 126 spikes/s. The majority (80%) of Primarylike-notch units had re- covery functions similar to those seen for Primary- like units. An example of one such unit (31.658) is shown in the upper right panel of Fig. 3. The lower masker levels resulted in recovery funct ions with shallow slopes and low levels of adaptation. Recovery was approximately linear in log time for masker levels of +45 and + 60 dB. The N P R increased with the D T and as the masker level increased, the N P R decreased at a given DT. For example, for a masker level of +45 dB re threshold, the N P R increased from 0.32 at a D T of 5 ms to 0.99 at a D T of 100 ms.
In contrast, five of 25 Primarylike-notch units had recovery patterns which differed from those seen in Primarylike units. Fig. 3 (left) shows the PST histograms for Primarylike-notch unit 12.658 obtained with the forward-masking stimulus paradigm. PST histograms are shown for six D T values at a masker level of + 45 dB re threshold. As can be seen from the histograms, the greatest decrement in N P R occurred for a 10 ms D T (NPR = 0.32) as opposed to 5 ms (NPR--0 .52) . As shown in the recovery function (Fig. 3, center right), unit 12.658 exhibited a non-linear recovery pattern at higher masker levels.
Fig. 3, lower right shows mean recovery func- tions for 25 Primarylike-notch units at 4 masker
levels. The average function for a masker level of + 15 dB showed little adaptat ion and the slope of the curve was very shallow. Adaptat ion and re- covery processes are more apparent at higher masker levels. The decrement in N P R increased with increasing masker level at a given DT. For example, at a D T of 5 ms, the decrement in N P R was approximately 42% for a masker level of + 30 dB, whereas the decrement was approximately 70% for a masker level of +60 dB. Recovery was approximately linear-in-log time when averaged across units and was nearly complete at 200 ms. At masker levels of +45 and + 6 0 dB, the re- covery functions tended to flatten out at short DTs, presumably due to the effect of the 5 units with the greatest decrement at 10 ms rather than 5 ms. Nevertheless, in the time interval of interest (10-200 ms), the recovery functions were ap- proximately linear in log time and it was thus possible to quantitatively compare results with other unit classes, as described below.
Chopper units A total of 31 Chopper units were studied with
the forward masking stimulus paradigm. The CFs ranged from 230 to 16,700 Hz, the thresholds ranged from - 1 0 to 31 dB SPL, and the SRs ranged from 0 to 155 spikes/s. The vast majority of units had thresholds less than 25 dB SPL. Fig. 4 (left) shows PST histograms (left) and recovery functions (upper right) for unit 38.001 collected with the forward-masking stimulus paradigm. Histograms are shown for 6 DTs collected with a masker level of + 45 dB re threshold. In general, the response to the masked probe decreased as D T decreased. For example, the N P R obtained with a + 60 dB masker level and a D T of 5 ms was 0.05, whereas at a D T of 100 ms the N P R was 0.78. The slopes of the recovery functions increased with masker level up to +45 dB; however, all the recovery functions intersected and were 85 to 90% recovered by 200 ms.
The effect of masker level on the mean recovery functions of 31 Chopper units is shown in Fig. 4 (lower right panel). The normalized probe rate decreased as D T decreased for all masker levels and the N P R decreased with increased masker level at a given DT. All the recovery functions were approximately linear in log time.
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Fig. 2. (Left Panel): Post-stimulus time (PST) histograms (bin width 1 ms) for unit 22.541 (Spontaneous rate: 68.6 sp/s) collected with a forward masking paradigm. Data obtained at DTs shown in upper fight of each histogram. Stimulus conditions for each panel are: probe level: +15 dB re threshold, masker level: +45 dB, masker and probe frequency: 4,334 Hz. (Right Panel): Recovery functions for units 22.541, 22.001 (Spontaneous rate: 59.5 sp/s) and mean recovery functions across Primarylike units at four masker
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Recovery functions for unit 38.001 and mean recovery functions across all Chopper units.
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s tudied. The C F s ranged f rom 400 to 7500 Hz, the thresholds ranged f rom - 5 to 63 dB SPL, and the SRs ranged f rom 0 to 170 sp ike s / s . The uppe r r ight panel of Fig. 5 i l lus t ra tes the fo rward mask- ing recovery pa t t e rns for one P a u s e r / B u i l d u p unit (14.849). The recovery funct ion of this uni t was qual i ta t ive ly s imilar to that found in Pr imary l ike units, i.e., as D T increased, the normal ized p r o b e ra te also increased. However , the rate of recovery in the first 20 ms was more r ap id than that seen in most Pr imaryl ike and Choppe r units. Of 16 P a u s e r / B u i l d u p units, eight had recovery func- t ions which were s imilar to those for uni t 14.849.
The remain ing eight P a u s e r / B u i l d u p units had more unusual recovery funct ions. The midd le right pane l of Fig. 5 shows recovery funct ions for uni t 02.544. The PST h is tograms for this uni t (Fig. 5, left) had the charac ter i s t ic shape of a Pauser unit, wi th a peak of act ivi ty at s t imulus onset , a 7 ms quiescent per iod, and a r e sumpt ion of activity. The PTS h i s togram with 500/xs bins is shown at the upper left to accentua te the fact that the h i s togram shape is a Pauser. As the separa t ion of maske r and p robe increased, the m a x i m u m de- crease in N P R occurred at a D T of 40 ms, ra ther than at 5 ms as descr ibed for most P r imary l ike units. No te the lack of act ivi ty in the PST histo- g r am ob ta ined with a D T of 40 ms. The recovery funct ions were ' U - s h a p e d ' and the m a x i m u m de- c rement in N P R occur red at mode ra t e DTs. Rela- t ively high N P R occur red at the shortest and longest DT. F o r example , at a masker level of + 45 dB, the N P R was 0.83 for a D T of 5 ms, the N P R was 0.03 at a D T of 40 ms, and the N P R was 1.0 at a D T of 200 ms. The ' U - s h a p e d ' recovery funct ion r ema ined fair ly s table across maske r level. I t is also in teres t ing to no te that the N P R was a pp rox ima te ly 1.25 with a masker level of + 15 dB and a D T of 5 ms. In this condi t ion ,
Fig. 6. (Upper panels): PST histograms for Pauser/Buildup unit 19.658 (Spontaneous rate: 54.8 sp/s) Data obtained at DTs shown in upper right of each histogram. Stimulus condi- tions for each panel were: probe level: + 15 dB re threshold, Masker level: +45 dB. (Lower panel): Recovery functions for
unit 19.658. Masker levels: See key.
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Fig. 7. (Left panel): PST histograms for On-I unit 37.658 (Spontaneous rate: 0.0 sp/s) Histogram conditions: DT: 5 ms, masker levels shown in upper right of each histogram, probe level + 15 dB re threshold. (Right panel): Recovery functions for units 37.658
and 18.658 (Spontaneous rate: 137.2 sp/s)
136
right), with the peak response at +45 dB re threshold.
Fig. 6 shows the recovery functions and PST histograms for one Pauser/Buildup unit collected with the forward-masking stimulus paradigm. Note the gradual increase in firing rate across the dura- tion of the masker. The shape of the histogram for the probe tone does not appear to be a Buildup pattern; this difference in PST histogram shapes between short tones and long tones at CF is not uncommon for Pauser/Buildup units (Godfrey et al., 1975a). At high masker levels, the response to the masked probe is difficult to recognize at short DTs due to the high firing rate at the end of the masking stimulus. This made it difficult to esti- mate the firing rate to the masked probe. In order to analyze the response to the masked probe it was necessary to subtract the firing rate in the time interval immediately following the masker, using the data obtained with a DT of 100 or 200 ms, from the firing rate in the interval immediately following the masker when the D T was 5 or 10 ms. The result of the subtraction should ap- proximate the firing rate to the masked probe for the short DT. After subtracting out the after- discharges, the response to the masked probe was still greater than that obtained to the control probe at short DTs. For example, at a D T of 5 ms, the N P R was 1.6 when the masker intensity was + 60 dB and 1.2 when the masker level was + 45 dB. This enhanced response occurred only for DTs of 5 and 10 ms.
On units A total of 5 On units were studied. Fig. 7 (left)
shows a series of PST histograms collected from an On-I unit (37.658) during presentation of the forward-masking stimulus paradigm. The histo- grams show the results obtained at a DT of 5 ms at masker levels of 15, 30, 45, and 60 dB re threshold. There are three distinct peaks in the histograms due to the control probe, the masker, and the masked probe. This On-I unit showed virtually no adaptation at any D T or masker level. (Note the total number of spikes to the masked probe in the 60 dB masker level condition fell into two bins rather than one, consequently the re- sponse appears smaller than it actually was.) Re- covery functions for this unit are shown in Fig. 7
(upper right). The N P R was approximately 1.0 at all four masker levels at all DTs for this On-I unit.
The lower right panel of Fig. 7 shows the forward masking recovery functions for unit 18.658 (On-L) at four masker levels. In contrast to the preceding On-I unit described above, the On-L unit showed significant adaptat ion at short DTs and high masker levels. Recovery was approxi- mately linear in log time for this unit. Linear recovery in log time was seen in two On-L units; one On-L unit had a recovery pat tern which was more exponential in log time, with complete adap- tation at short DTs and nearly complete recovery between 40 and 100 ms.
Due to the small number of On units studied and the variety of response patterns across On units, it is not useful to a t tempt to group the data together.
Quantitative comparison of units
In order to quantitatively describe the trends seen in the sample of CN units with linear re- covery in log time, a recovery function was fit to the group data for each unit type with the equa- tion [NPR = 1 + b log (DT/K) ] . The term ' K ' represents the time for complete recovery and ' b ' represents the rate of recovery. Only the data with DTs of 10-200 ms were used in the regression analysis. Furthermore, in many units recovery functions for data collected at a masker level of + 15 dB did not show linear recovery in log time, due to lack of significant adaptat ion at this masker level. Thus, the data for a masker level of + 15 dB are not included in the analysis. Regression analy- sis results are shown in Table I. The results of regression analysis indicate that the rate of re- covery (b or slope) of Primarylike increased from 0.24 N P R / l o g ms to 0.39 N P R / l o g ms as the masker level increased from +30 to + 6 0 dB. Thus, a 10-fold increase in recovery time would result in a 39% increase in N P R for the + 60 dB masker. The recovery time (K) did not vary greatly or systematically across masker level for Primary- like units and remained in the range of 263 to 293 m s .
The rate of recovery of Primarylike-notch units increased as the masker level increased from 0.26 N P R / l o g ms at a masker level of + 30 dB to 0.52
N P R / l o g ms at a level of + 60 dB. The recovery t ime (K) r ema ined fair ly s table (207 to 272 ms) be tween the + 30 and + 60 dB maske r levels.
The rate of recovery of C h o p p e r units increased f rom 0.23 N P R / I o g ms at + 30 dB maske r level to 0.45 N P R / l o g ms at + 60 dB. The recovery t ime decreased across increas ing masker level, f rom 366 ms to 314 ms.
Because of the divers i ty of recovery pa t t e rns found across P a u s e r / B u i l d u p units, it is not useful to group all P a u s e r / B u i l d u p da t a together. Eight uni ts had recovery pa t t e rns which were approx i - ma te ly l inear- in- log- t ime. The rates of recovery for the uni ts increased over the range of masker levels up to + 45, then reached an a sympto te at 0 .36-0 .38 N P R / l o g ms. The var iab i l i ty m a y be due to the fact that on ly 8 Pauser units were inc luded at maske r levels of + 30 and + 45 dB and only 3 at the + 60 dB masker level. Because of the smal l n u m b e r of P a u s e r / B u i l d u p units wi th l inear re- covery in log time, the d a t a should be in te rp re ted caut iously.
Effect of spontaneous rate on recovery
Salvi et al. (1986) showed that aud i to ry nerve f ibers with low rates of spon taneous act ivi ty re-
137
covered more s lowly f rom fo rward mask ing than units wi th high SRs. To evalua te the re la t ionsh ip of SR to a d a p t a t i o n in the CN, uni ts were d iv ided into two groups, those with SR of 18 spikes pe r second or less ( ' l ow ' SRs) and those wi th ra tes greater than 18 s p i k e s / s . Resul ts for the two groups were fit to the l inear - in - log- t ime mode l and recovery rates and t imes were de t e rmine d for each group.
F o r Pr imary l ike units, the s lopes for the high SR group were cons is ten t ly s teeper than those of the low spon taneous group. A t + 45 and + 60 dB, the s lopes for the low SR group were 0.32 and 0.33 N P R / l o g ms respect ively, whereas for the high SR group the s lopes were 0.38 and 0.39 N P R / l o g ms, respect ively. Fu r the rmore , the re- covery t imes were longer for the low SR group at masker levels of + 45 and + 60 dB as c o m p a r e d to the high SR group, a l though the t rend was re- versed at the lower maske r level. Thus, there was a t endency for Pr imary l ike uni ts wi th high S R to recover more r ap id ly than low S R units at h igh masker levels, a resul t s imilar to tha t r epo r t ed for aud i to ry nerve f ibers (Salvi et al., 1986).
F o r P r imary l ike -no tch units, the d a t a were fa i r ly well fit wi th the log funct ion. The ra te of recovery was s imilar for the two groups at a maske r level of + 30 dB; at higher maske r levels the high S R uni ts recovered at a fas ter ra te than the low SR. F o r example , at + 45 dB, the ra te was 0.43 N P R / l o g ms for the high SR and 0.35 N P R / l o g ms for the low SR. Fu r the rmore , the recovery t ime (K) was shor ter for the uni ts with high SR than for the uni ts with low SR. Thus, P r imary l ike -no tch uni ts wi th high SRs recovered more r ap id ly than low SR uni ts which is cons is ten t wi th o ther uni t types analyzed.
The slopes of the recovery funct ions for the high SR C h o p p e r uni ts were typ ica l ly equal to or sl ightly greater than those for uni ts with low or m e d i u m SR. The recovery t imes (K) for the + 45 and + 60 dB cond i t ions were s imi lar for the high and low SR uni ts a l though at + 30 dB, the low SR units requi red somewha t longer to recover.
Because the n u m b e r of P a u s e r / B u i l d u p and On uni ts wi th l inear in log t ime recovery pa t t e rns was small , effects of SR on recovery were not invest i- ga ted in these uni t classes.
138
1.2
P R I M A R Y L I K E UNITS +15 DB M A S K E R LEVEL +30 DB MASKER L E V E L
Fig. 8. Effect of CF on recovery functions in Primarylike units. Masker level as shown above each graph. Units grouped by CF as shown in upper left panel.
Effect of CF on recovery
To determine if unit CF had an effect on the recovery from short-term adaptation, CN units were divided into low (CF < 1.0 kHz), medium (CF: 1.0-4.0 kHz), and high (CF > 4.0 kHz) CF groups and the mean recovery functions were computed for 4 masker levels.
The effect of CF on recovery of Primarylike units is shown in Fig. 8. No systematic differences were seen across the three CF groups, except at + 60 dB. At this level, the low CF units showed an unusual recovery pattern with a very shallow re- covery slope. The shallow slope at + 60 dB may be due to the small number of units in the low CF group at this masker level. Similar results (not shown) were seen for Primarylike-notch and Chopper units, i.e., no systematic differences in the time course of recovery as a function of CF. Because the number of Pauser/Buildup and On units with linear in log time recovery patterns was
small, effects of CF on recovery were not investi- gated in these unit classes.
Discussion
General recovery patterns and comparison of unit classes
The majority of Primarylike (89%), Primary- like-notch (80%), and Chopper (93%) units had recovery patterns which were approximately linear in log time. The choice of using linear analysis in log time was made as the greatest number of units were accommodated with this pattern as opposed to exponential recovery patterns. Furthermore, as described below, linear analysis in log time is consistent with many examinations of forward masking in the psychophysical domain.
As described below, auditory nerve fibers are often modelled with exponential equations. Very short temporal separations (less than 5 ms) were not examined in this project due to the difficulty
of separating the response to the masker from the response to the probe. This occurred in some units due to 'afterdischarges' which are a feature of CN responses (see Mast, 1970). There is thus some possibility that an exponential recovery pattern may be found in CN units if very short DTs were used (as in auditory nerve fibers).
For CN units, at a given masker intensity, the N P R decreased as D T decreased. At a given DT, the N P R decreased as the masker level increased. Depending on masker level, units required ap- proximately 200-450 ms for complete recovery from adaptation. There were a few exceptions in the three unit classes described above. Two Primarylike units had recovery patterns which were approximately exponential in log time instead of linear in log time. In addition, 20% of the Primary- like-notch units had the greatest decrease in N P R at a D T of 10 ms rather than 5 ms.
In contrast with the relatively homogeneous recovery pat terns seen in the Primarylike, Primarylike-Notch, and Chopper units, a variety of recovery patterns were seen in the Pauser / Buildup and On units. Approximately half the Pause r /Bu i ldup units had recovery patterns qualitatively similar to those in the Primarylike units, namely a decrease in N P R as the DT was decreased. However, the remainder of Pause r / Buildup units had recovery patterns that were U-shaped. A variety of recovery patterns were seen in the On units, including one unit which showed no adaptation at any masker level or DT. Several on units exhibited exponential recovery functions and several On units had linear recovery patterns in log time.
The rates of recovery of Primarylike, Primary- like-notch, and Chopper units increased as masker level increased. The rates did not differ greatly between unit classes, ranging from 0.03 to 0.12 N P R / I o g ms at low masker level to 0.39 to 0.52 N P R / I o g ms at + 60 dB masker level. The time to recovery was generally shortest in the Primary- like-notch units and longest in the Chopper units.
A limitation of the study is the fact that precise location of units was not determined. A major focus of the project was to compare forward mask- ing recovery patterns of CN units with PST histo- gram shapes of the units. It is likely that histologi- cal analysis of recording locations would be useful
139
in examinations of fine details of forward masking and temporal processing in the CN.
Comparison with previous studies: Auditory nerve Previous single unit studies of forward masking
in the auditory nerve have suggested that as the temporal separation between masker and probe increased, the response to the probe increased (Harris, 1977; Harris and Dallos, 1979; Smith, 1977; 1979; Salvi et al., 1986). Harris and Dallos (1979) suggested that recovery f rom adaptat ion may be described in terms of exponential or loga- rithmic functions. The goodness of fit of each equation depended on the range of D T values used. For DTs of 10 ms and greater, a logarithmic equation provided a good fit to their data, but inclusion of DTs of 2 and 5 ms resulted in an exponential form to the recovery functions in auditory nerve fibers.
In order to put our data into perspective, the data of Harris (1977) and Salvi et al. (1986) were fit to the equation: N P R = 1 + b log ( D T / K ) and compared to the present study in terms of rate and time of recovery. It should be noted that the comparison is not ideal; Harris (1977) used a probe + 15 dB re threshold as in the present study whereas Salvi et al. (1986) used a probe at + 10 dB. Furthermore, different masker intensities were used in each study. However, there was enough similarity between studies to warrant comparison.
Recovery times Fig. 9 (upper panel) shows recovery times for
auditory nerve and CN units with SRs less than 18 spikes/s plotted as a function of masker level. Auditory nerve data were taken from Salvi et al. (1986) while all CN data are from the present experiment. For CN units, the recovery times ranged from approximately 275 to 525 ms. The recovery times did not vary systematically across masker level in the Primarylike-notch units; re- covery times decreased with increasing masker level for Chopper units and decreased with in- creasing masker level for Primarylike units. The auditory nerve fibers had recovery times some- what longer than CN units. This may be due to the difference in probe characteristics: Salvi et al. used a 10 ms probe + 10 dB re threshold, whereas the present experiment used a 20 ms probe + 15
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Fig. 9. (Upper): Recovery times for units with low (A) and high SR (B) (Lower): Recovery rates for units with low (C) and high SR (D) Key: Closed squares: Primarylike; Triangles: Primarylike-notch; Open squares: Chopper; H: Auditory nerve data of Harris,
1977 (not divided by SR); S: Auditory nerve data (divided by SR) of Salvi et al., 1986.
dB re threshold. Harris (1977) reported that less masking occurred at higher probe levels; thus it might be expected that longer recovery times would be seen for the data of Salvi et al. Alterna- tively, the CN may in fact have slightly faster recovery times than the auditory nerve.
Fig. 9B shows recovery times for auditory nerve and CN units with high SR. For Primarylike units, recovery times did not vary consistently with masker level; recovery time increased with in- creased masker levels in Primarylike-notch units and decreased with increased masker level in Chopper units. It is not yet clear why the recovery times vary with masker level across the different types of units and units with different SR. The auditory nerve fibers had recovery times con- sistent with CN units. Although Harris (1977) did not classify auditory nerve fibers based on SR, his group data (from Fig. 3-2, Harris, 1977) showed recovery times of approximately 200 ms for a + 30 dB masker, consistent with the CN data and the auditory nerve data of Salvi et al. (1986).
Rates of recooery Fig. 9C shows recovery rates of auditory nerve
and CN units with low SR, plotted as a function of masker level. The rates of recovery were not remarkably different for Primarylike, Primarylike- notch, and Chopper units. For all unit classes, the rates of recovery increased as the masker level increased from + 30 to + 60 dB. Auditory nerve fibers (from Salvi et al., 1986) showed a somewhat faster rate of recovery at + 30 dB masker level compared to the CN units. Recovery rate de- creased slightly as masker level increased.
Fig. 9D shows recovery rates for auditory nerve and CN units with high SR. For all unit types, recovery rates increased as the masker level in- creased. The change in recovery rate as a function of masker level was greater for the high SR than the low SR units. The auditory nerve fibers have a much higher recovery rate than CN units at a masker level of + 30 dB, but rates were similar at higher masker levels. The data of Harris (1977) showed high recovery rates (approximately 0.5
N P R / l o g ms) at + 30 dB masker level. At higher masker levels, the rate of recovery dropped slightly, to fall in the range of the data collected in the CN.
Effect of CF Previous auditory nerve data has shown that
the recovery from adaptation does not vary across CF in auditory nerve fibers (Smith, 1977). Our results from the CN also showed no significant differences in the time course of recovery across CF.
Effect of masker level In the auditory nerve, the decrement in the
N P R was closely correlated with the increase in firing rate caused by the masker. That is, once the firing rate to the masker saturated, there was no further decrease in the NPR. Similar effects were seen in many CN units. However, in some CN units, the decrement in the N P R was more strongly correlated to masker SPL than to the firing rate caused by the masker.
While masker level effects were fairly straight- forward in the averaged data, a variety of patterns was found in the individual data. For example, as seen in Fig. 2, some Primarylike units showed an asymptote of masker level effect at masker intensi- ties of +30 dB. In the Pauser/Buildup units, masker level effects were more complex. For ex- ample, in Fig. 6 little masking occurred at the +15 dB masker level, enhanced responses oc- curred at short DTs at the + 3 0 - + 45 dB masker levels, and tittle effect occurred at + 60 dB at the short DTs. Thus, the relationship of masker level and adaptation is more complex in the CN than in the auditory nerve.
Thus, over a wide range of DTs (10-200 ms), there was little difference in the time course of recovery between most Primarylike, Primarylike- notch, and Chopper units and auditory nerve fibers. Furthermore, the times and rates of re- covery were similar between these units and those in the auditory nerve. This indicates that the time course of recovery seen in the auditory nerve is relayed through most Primarylike, Primarylike- notch, and Chopper units. However, the time course of recovery in the auditory nerve is greatly altered by some Pauser /Bui ldup which had un- usual 'U-shaped ' recovery patterns.
141
Comparison with previous data: CN. We are aware of only one previous study of
forward masking at the single unit level in the cochlear nucleus (Watanabe and Simada, 1971). They reported forward masking recovery func- tions which were qualitatively similar to those found in the present study for Primarylike units. However, the methodology used in the two studies were significantly different and this precludes di- rect comparison of the results.
Although not strictly a forward masking inves- tigation, the work of Starr (1965) is interesting in comparison to the present data. Starr determined the recovery of spontaneous activity in CN units after stimulation with pure tones at CF. In the majority of units (35 of 40), as the masker level or duration increased, the time for recovery of spon- taneous rate also increased. Start also suggested that units with rapid adaptation to the tonal stimulus showed faster recovery of spontaneous rate after stimulation than units with slow adapta- tion to the tonal stimulus. The firing rate to click stimuli was decreased after tonal stimulation in CN units. In the present study, we observed sig- nificant decreases in spontaneous rate after the masker. Furthermore, the duration of decreased spontaneous rate lengthened as the masker level increased, as Starr found in the majority of his units.
The observation from the present study that an On-I unit showed little or no recovery is consistent with data of Meller (1969) who showed that ' t ran- sient' units in the CN often respond best to a specific stimulus presentation rate, and were able to respond at high rates with little adaptation. Godfrey et al. (1975a) reported that On-I units may respond to each cycle of a low-frequency stimulus, suggesting tittle adaptat ion in the units. On-I units typically show little frequency selectiv- ity, but apparently are able to code very rapid changes in stimulus intensity.
Comparison with evoked response data In general, the forward masking recovery func-
tion of the human whole-nerve action potential to a click had an exponential form (Coats, 1964; Eggermont and Spoor, 1973). The rate of recovery increased with increased masker level, but the time to recovery did not vary systematically with masker
142
intensity. These results are consistent with those of the present study. In contrast, Abbas and Gorga (1981) found little effect of masker level on time constant of recovery of the whole-nerve AP of the cat.
Etholm (1969) used paired clicks to examine adaptation in the evoked response from the infe- rior colliculus and medial geniculate body. Inter- estingly, the maximum adaptation occurred at DTs of 25 to 50 ms, not at 5-15 ms. These results were thus similar to the recovery patterns seen in Pauser /Bui ldup units of the CN.
The effect of frequency on forward masking of evoked potentials has been examined in several ways. Arehole et al. (1987) reported little or no effect of frequency on the recovery from forward masking of the evoked response from the inferior colliculus, using maskers and probes of the same frequency. These results were similar to those of the present experiment.
Comparison with previous data: Psychophysics This discussion should be prefaced with the
statement that it is difficult to correlate the re- sponse of a single neuron with psychoacoustic data because of the difficulty in determining what neural measure would be equivalent to the behav- ioral detection threshold. Furthermore, there is little psychophysical data on forward masking in the chinchilla due to the difficulty of the listening task. The data that is available suggests linear recovery in log time for DTs of 10-80 ms (Salvi et al., 1986). Despite these limitations, there are in- teresting parallels between psychophysical results and data from the present study.
Recovery functions Fixed masker level studies of forward masking
in the psychophysical domain have suggested that recovery is a linear process in log time, with complete recovery occurring by 300-1000 ms (Zwislocki et al., 1959; Widin and Viemeister, 1979; Jesteadt et al., 1982). Fixed probe level studies have found similar trends in recovery, al- though Nelson and Freyman (1987) have sug- gested exponential recovery. Carlyon (1988), how- ever, found linear recovery in log time in psycho- physical examinations of forward masking, and
summarized evidence from other reports to con- clude that the recovery was linear in log time.
The data of the present study appear consistent with linear time course of recovery, at least over DTs of 10 to 200 ms. The majority of psycho- physical examinations of forward masking have found recovery times of 200-300 ms; this range is similar to the majority of Primarylike, Primary- like-notch, and Chopper units in the CN, espe- cially those with high SR. Interestingly, data from Zwislocki et al. (1959) shows forward masking effects occurring to 1000 ms. Some CN and audi- tory nerve units with low SR show very long recovery times, similar to the data of Zwislocki et al.
Effect of masker level In the present study, masker level did not ap-
pear to systematically affect recovery times, but increasing the masker level increased the rate of recovery. This is consistent with Duifhuis (1973), who showed that the masker level does not affect the recovery time but it does increase the rate of recovery. Thus, most single unit data from the CN are consistent with the psychophysical data.
Effect of frequency The CF of a unit did not appear to affect the
time course of recovery from forward masking in CN units in the present study. This was consistent with data of Zwislocki et al. (1959) and Harris et al. (1951) who found no frequency effects in for- ward masking. Several psychophysical reports, however, have found that more masking may oc- cur at lower frequencies, possibly due to faster growth of loudness at the lower frequencies (E1- liott, 1962; Jesteadt et al., 1982).
In conclusion, it appears that Primarylike, Primarylike-notch, and Chopper units in the CN show recovery from short-term adaptat ion in a manner similar to auditory nerve fibers. This sug- gests that the adaptive information f rom the audi- tory nerve is not significantly altered by these CN units, when the masker and probe signals are both at CF. However, Pauser /Bui ldup and On units appear to alter adaptive information from the auditory nerve. Further study will examine more closely the role of the Pauser /Bui ldup and On units in adaptive processing. In addition, future
e x p e r i m e n t s wil l e x a m i n e t he e f fec t s o f m a s k e r
p a r a m e t e r s o n a d a p t a t i o n in t he C N .
A c k n o w l e d g e m e n t s
T h e a u t h o r s w o u l d l ike to t h a n k D o n a l d
H e n d e r s o n a n d J a n e t So leck i f o r c o m m e n t s o n
ea r l i e r d r a f t s o f t h i s m a n u s c r i p t . P o r t i o n s o f t h i s
d o c u m e n t w e r e i n c l u d e d i n a d i s s e r t a t i o n b y t h e
f i r s t a u t h o r s u b m i t t e d to t h e U n i v e r s i t y o f T e x a s
a t D a l l a s .
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