Auditory Detection and Discrimination in Deaf Cats: Psychophysical and Neural Thresholds for Intracochlear Electrical Signals

Maike Vollmer,1 Ralph E. Beitel,2 and Russell L. Snyder2

 1Department of Physiology, J. W. Goethe-University, 60596 Frankfurt/Main, Germany; and  2Department of Otolaryngology, University of California, San Francisco, California 94143-0526


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Vollmer, Maike, Ralph E. Beitel, and Russell L. Snyder. Auditory Detection and Discrimination in Deaf Cats: Psychophysical and Neural Thresholds for Intracochlear Electrical Signals. J. Neurophysiol. 86: 2330-2343, 2001. More than 30,000 hearing-impaired human subjects have learned to use cochlear implants for speech perception and speech discrimination. To understand the basic mechanisms underlying the successful application of contemporary speech processing strategies, it is important to investigate how complex electrical stimuli delivered to the cochlea are processed and represented in the central auditory system. A deaf animal model has been developed that allows direct comparison of psychophysical thresholds with central auditory neuronal thresholds to temporally modulated intracochlear electrical signals in the same animals. Behavioral detection thresholds were estimated in neonatally deafened cats for unmodulated pulse trains (e.g., 30 pulses/s or pps) and sinusoidal amplitude-modulated (SAM) pulse trains (e.g., 300 pps, SAM at 30 Hz; 300/30 AM). Animals were trained subsequently in a discrimination task to respond to changes in the modulation frequency of successive SAM signals (e.g., 300/8 AM vs. 300/30 AM). During acute physiological experiments, neural thresholds to pulse trains were estimated in the inferior colliculus (IC) and the primary auditory cortex (A1) of the anesthetized animals. Psychophysical detection thresholds for unmodulated and SAM pulse trains were virtually identical. Single IC neuron thresholds for SAM pulse trains showed a small but significant increase in threshold (0.4 dB or 15.5 µA) when compared with thresholds for unmodulated pulse trains. The mean difference between psychophysical and minimum neural thresholds within animals was not significant (mean = 0.3 dB). Importantly, cats also successfully discriminated changes in the modulation frequencies of the SAM signals. Performance on the discrimination task was not affected by carrier rate (100, 300, 500, 1,000, or 1,500 pps). These findings indicate that 1) behavioral and neural response thresholds are based on detection of the peak pulse amplitudes of the modulated and unmodulated signals, and 2) discrimination of successive SAM pulse trains is based on temporal resolution of the envelope frequencies. Overall, our animal model provides a robust framework for future studies of behavioral discrimination and central neural temporal processing of electrical signals applied to the deaf cochlea by a cochlear implant.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Cochlear implants (CIs) have been used successfully in more than 30,000 hearing-impaired human subjects to restore speech perception and speech discrimination (e.g., Dorman 1993; NIH Consensus Statement 1995). Despite considerable variability in performance among individuals, most implant users have demonstrated gradual improvements in speech discrimination performance over time, and many are able to understand open set speech without lip reading (e.g., Doyle et al. 1991; Spivak and Waltzman 1990; Wilson et al. 1991). The successful application of CIs raises important questions regarding information processing in the auditory system. To understand the basic mechanisms that make "electrical hearing" possible, an essential requirement in auditory neuroscience is to investigate how electrical signals applied to the auditory nerve are represented in the central auditory system.

We have developed a behavioral model for deaf cats implanted with a cochlear prosthesis that allows collection of both psychophysical and electrophysiological data from the same animal (Beitel et al. 2000a,b). In this model, stimulation of surviving spiral ganglion cells activates central auditory pathways and, consequently, may result in the detection or perception of electrical signals by the deaf animal. The present study employs this model and addresses three important issues.

First, behavioral thresholds were estimated for unmodulated and sinusoidally amplitude-modulated (SAM) pulse trains with different carrier and modulation frequencies in the same deaf animals. Using unmodulated pulse trains, a number of behavioral studies have described the influence of simple electrical stimulus parameters (e.g., phase duration, stimulus frequency, stimulus duration) on detection thresholds (e.g., Beitel et al. 2000a; Pfingst and Morris 1993; Shannon 1985; Smith and Finley 1997). However, speech information for CI listeners in contemporary speech processing strategies is conveyed by high-frequency, amplitude-modulated stimuli (Brill et al. 1997; McDermott et al. 1992; Wilson et al. 1991), and relatively little research has been conducted on the effects of these temporally more complex electrical signals on detection threshold.

One important question concerning the processing of SAM pulse trains is whether detection threshold for these signals is based exclusively on detection of the peak amplitude of the modulated pulse train or whether threshold is influenced by temporal integration of the modulated carrier pulses. In preliminary studies, Beitel and colleagues (2000b) have hypothesized that the detection of unmodulated and SAM pulse trains is based on the amplitude of unmodulated current pulses or the maximum amplitude of the pulses in the modulated carrier, respectively. However, in these studies only two different SAM signals with identical modulation frequency were used, and detection thresholds were compared between different groups of animals. By extending the combinations of SAM carrier and modulation frequencies and by estimating behavioral thresholds for unmodulated and SAM pulse trains in the same animals and, thus, eliminating the influence of interindividual variability on threshold detection, the present study provides a more rigorous test for the hypothesis that the detection thresholds of unmodulated and SAM pulse trains are determined by the peak pulse amplitude of the signals.

Second, behavioral thresholds for unmodulated and SAM pulse trains were compared with the minimum neuronal thresholds estimated in the inferior colliculus (IC) and the primary auditory cortex (A1) of the deaf cats. The relationship between psychophysical detection of intracochlear electrical stimulation and the underlying activity of neural elements is poorly understood. For example, Pfingst (1988) has compared psychophysical thresholds in macaque monkeys and humans with auditory nerve thresholds in cats or squirrel monkeys. These indirect comparisons among different species and different laboratories showed that neural thresholds were consistently higher than psychophysical thresholds. However, Beitel and colleagues (2000a,b) have reported that the lowest neural thresholds recorded in the IC or the A1 were essentially the same as the psychophysical detection thresholds measured in the same deaf cats. The present study confirms these findings and extends them by determining electrophysiological thresholds for unmodulated and SAM pulse trains in the same isolated single neurons in the IC.

Finally, the results on psychophysical detection thresholds and neural thresholds for SAM signals provide a basis for addressing the issue of discrimination by deaf animals of temporally complex, amplitude-modulated signals. To our knowledge, the current study is the first behavioral investigation of temporal resolution in a deaf animal model. The ability to discriminate an increase in the modulation frequency of electrical pulse trains with different carrier frequencies was estimated using a successive discrimination paradigm. An important goal in this study was to investigate whether the discrimination of SAM signals was based only on differences in the modulation frequency or whether the rate of suprathreshold SAM carrier pulses had an additional influence on discriminative performance. The results indicate that the carrier pulse rate had no apparent effect on discrimination. This finding is clinically relevant, because it suggests that resolution of changes in the temporal envelopes of SAM pulsatile carriers provides major information for speech discrimination and, thus, for the quality of communication for CI users.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

This report includes results obtained from 11 neonatally deafened cats (Table 1). Most of the procedures used for deafening, implantation, behavioral training, surgical preparation, and physiological recording have been described in detail in previous reports (e.g., Beitel et al. 2000a,b; Leake et al. 1999; Raggio and Schreiner 1994; Snyder et al. 2000; Vollmer et al. 1999) and will be repeated here in an abbreviated form. All procedures followed the National Institutes of Health guidelines for care and use of laboratory animals.


                              
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Table 1. Behavioral training history

Deafening and cochlear implantation

Cats were deafened by daily intramuscular injections of neomycin sulfate (50-60 mg/kg body wt) for 16-25 days after birth. Profound hearing loss (>108 dB SPL) was confirmed by evoked auditory brain stem responses to clicks (0.2 ms/ph, 20 pps) and frequency following responses to tonal stimuli (500 Hz). Prior to implantation, acoustic thresholds were measured again; none of the animals demonstrated any residual hearing.

Before all surgical procedures the animals were sedated, and an intravenous catheter was inserted into the cephalic vein for fluid and drug administration. General anesthesia was induced with pentobarbital sodium (7-10 mg/kg iv) and maintained at a surgical areflexic level with supplementary intravenous infusion of pentobarbital sodium (2-6 mg · kg-1 · h-1) in Ringer solution.

In 9 of the 11 animals an electrode array was implanted on average 6.8 ± 0.5 (SD) wk after birth. Two cats (K55 and CH618) were long-term deafened animals implanted >4 yr after deafening. All electrode arrays were implanted through the round window into the scala tympani of the left cochlea using sterile surgical procedures. The implants consisted of four ball-shaped electrode contacts (200-300 µm diam) arranged as two bipolar offset-radial pairs (Beitel et al. 2000b). The electrodes were labeled 1-4 from their apical to basal cochlear location. A percutaneous connector allowed experimental access to the electrodes.

Electrical intracochlear stimulation

In this study, the electrodes were driven as bipolar pairs by computer-generated capacitively coupled, biphasic rectangular-wave current pulses (charge-balanced; 0.2 ms/phase). The stimulator was either an optically isolated constant current device (Vurek et al. 1981) or a custom-designed constant current source routinely used with CI patients in Geneva, Switzerland (M. Pelizzone, personal communication). The stimulation system was calibrated to a reference level of 0 dB = 1.0 µA peak-to-peak. This calibration applies to all psychophysical and neurophysiological thresholds reported below. For SAM pulse trains, the signal intensity refers to the maximum peak-to-peak amplitude of the modulated biphasic pulsatile carrier.

In nine cats, intracochlear electrical stimuli were delivered via apical contacts located approximately 9-11 mm from the round window (electrode pair 1,2). Due to electrode failures in cats K55 and K108, stimulation in these animals was delivered by electrode pairs 2,3 and 3,4, respectively (Table 1).

As required for a series of ongoing studies (cf. Leake et al. 1999; Snyder et al. 1995; Vollmer et al. 1999), 10 of the 11 cats received chronic passive electrical intracochlear stimulation [4 h/day, 5 days/wk, 2 dB above electrically evoked auditory brain stem response (EABR) threshold] during the present study. However, chronic passive stimulation had no apparent effect on behavioral or neural thresholds (unpublished data; cf. Beitel et al. 2000a), and the chronic passive stimulation histories are not reported in the present study.

Psychophysical procedures

Behavioral training was initiated at an average age of 14 wk in the kittens and at age >4 yr in the long-term deaf cats, K55 and CH618. The duration of behavioral training ranged between 11 and 34 wk with an average of 20.3 ± 6.78 (SD) wk (Table 1).

The behavioral training was based on a conditioned avoidance response (CAR) paradigm (Beitel et al. 2000a,b; Heffner and Heffner 1985). The cats were not food deprived. They were trained to lick a metal spoon on "safe" or "standard" signals to obtain a preferred food reward (meat puree) and to interrupt licking on "warning" or "comparison" signals to avoid a mild electrocutaneous shock (Fig. 1). Detection thresholds for all animals were estimated using unmodulated and SAM signals. Four of the animals were subsequently trained on a discrimination task using SAM signals.



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Fig. 1. A and B: conditioned avoidance paradigm (CAR) for detection of sinusoidal amplitude-modulated (SAM) signals. Line traces illustrate events that would result in a False Alarm during a safe trial (A) and either a Hit (correct detection) or a Miss (no detection) on a warning trial (B). Trials and intertrial intervals (ITI) are 1-s duration. Lick, cat is consuming reward; RT, reaction time. C and D: CAR paradigm for successive discrimination. Successive SAM waveforms (1-s duration) for Standard (C) and Comparison (D) trials. CS, conditioned stimulus; UCS, unconditioned stimulus.

Intracochlear electrode impedances were measured prior to each behavioral training session, and EABR thresholds were determined at regular intervals to assess the stability and reliability of the implanted system.

PSYCHOPHYSICAL DETECTION THRESHOLDS. The CAR paradigm used to determine detection thresholds (cf. Beitel et al. 2000a,b) is depicted schematically in Fig. 1, A and B. During psychophysical sessions, 70% of the trials were 1-s duration safe trials; 30% of the trials were 1-s duration warning trials. Intervals between successive trials were 1 s in duration. On safe trials (Fig. 1A) the individual trials were not identified by a signal. Contact with the spoon ("lick") was monitored by a computer (sampling rate, 50 Hz). While the cat was licking the spoon, food puree was delivered at a constant rate from a motor-driven syringe-pump.

On warning trials, capacitively coupled, biphasic rectangular-wave current pulses (charge-balanced; 0.2 ms/phase) served as the warning or conditioned stimulus (CS). The CS was either a train of unmodulated pulses (pulse rate, 30 or 100 pps) or a train of SAM pulses (pulse rate, 100, 300, or 500 pps; modulation frequency, 8 or 30 Hz; modulation depth, 100%). The stimulus parameters for the present study were chosen based on earlier and current studies in this laboratory investigating temporal resolution by neurons in the IC and A1 to electrical pulsatile stimulation (Schreiner and Raggio 1996; Snyder et al. 1995, 2000; Vollmer et al. 1999). Most IC neurons follow acoustic and electrical stimulus frequencies of 100 pps, but few neurons (<0.1%) can resolve pulse frequencies of >= 500 pps (e.g., Batra et al. 1989; Langner and Schreiner 1988; Snyder et al. 1995, 2000; Vollmer et al. 1999). In the cortex, the average following frequency to electrical stimulation is 12-14 pps (Schreiner and Raggio 1996), but studies using acoustic stimuli have shown that A1 neurons may follow pulse rates of 30 Hz and higher (Beitel et al. 1995; Liang et al. 1999).

During the initial training sessions, all warning signals were presented at a suprathreshold intensity sufficient to produce a behavioral reaction (pinnae movements, interruption in licking, etc.). At the end of a warning trial, an electric pulse or unconditioned stimulus (UCS; 140-210 ms duration, 60-Hz sinusoid) was applied to the spoon. If the cat remained in contact with the spoon, it received a mild electrocutaneous shock. The amplitude of the UCS was adjusted for each cat to the minimum intensity required to maintain avoidance behavior. A light located above the spoon was turned on and off simultaneously with the UCS to provide visual feedback for successful avoidance. To avoid the UCS, the animal was required to interrupt contact with the spoon during the 1-s warning trial and to refrain from licking the spoon until the light was turned off. Warning trials occurred randomly during a session, with the restriction that they could not occur in succession.

Once performance stabilized, threshold estimates (50% avoidance) were obtained using the psychophysical method of constant stimuli. During a session, a single pulse rate (e.g., 30 pps) or a single combination of one pulse rate and one envelope frequency (e.g., 300 pps/30 Hz) was used as the CS. Warning stimuli were presented randomly at six intensities (1-dB increments between adjacent intensities) that bracketed the estimated threshold. All other stimulus parameters (e.g., pulse rate, phase duration, modulation frequency, and stimulus duration) were held constant during each testing session. Stimulus generation and data acquisition were under computer control during experimental sessions. After each testing session, the False Alarm rate, p(FA), and the Hit rate, p(H), were calculated. False Alarms (Fig. 1A) occurred whenever a cat was not in contact with the spoon during the final 200 ms of a safe trial: p(FA) = total#FA/total#Safe trials. Hits (Fig. 1B) occurred whenever a cat was not in contact with the spoon during the final 200 ms of a warning trial, i.e., whenever a cat successfully avoided the UCS. The p(H) was calculated separately for each intensity of the CS by p(H) = #Avoidance Responses/#Warning trials. Testing was continued until threshold performance from session to session was within 3 dB. Based on results from three to five sessions, a correction of the data was calculated (Green and Swets 1966) to obtain the probability of detection, p(D), for each intensity of the CS: p(D) = [p(H) - p(FA)]/[1 - p(FA)]. A plot of p(D) as a function of stimulus intensity yields a psychometric function (Fig. 2). Psychophysical threshold was estimated by linear interpolation as the intensity at which p(D) = 50% (e.g., Beitel et al. 2000a,b; Heffner and Heffner 1985; Pfingst and Morris 1993; Smith and Finley 1997). For example, in Fig. 2 the psychophysical thresholds for 300/30 AM (300 pps carrier, SAM at 30 Hz) and 30 pps (indicated by arrows on the abscissa) were 44.7 and 45.1 dB, respectively. Thus, in this animal the threshold difference between the SAM and the unmodulated signal was 0.4 dB.



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Fig. 2. Psychometric functions showing probability of detection as a function of the intensity of unmodulated (30 pps) and SAM (300/30 AM) warning signals in cat CH618. Dashed line: 50% detection. Detection thresholds for the 2 signals are indicated by arrows.

Separate threshold estimates using a modified logistic function analysis (Allen and Wightman 1994) were conducted. Despite small differences in the thresholds of individual animals, both analyses yielded virtually the same overall results (paired t-test; P > 0.8). To maintain consistency with previous publications from our laboratory (Beitel et al. 2000a,b), only threshold data derived from linear interpolation will be presented in this report.

PSYCHOPHYSICAL THRESHOLDS FOR SUCCESSIVE DISCRIMINATION. The CAR paradigm used to evaluate an animal's ability to discriminate between successively presented standard and comparison signals is illustrated schematically in Fig. 1, C and D. In this paradigm, peak envelope amplitudes were set at 3 dB above detection threshold. During standard trials (70%), a SAM signal was delivered at a constant modulation frequency of 8 Hz and a constant carrier rate of 100, 300, 500, 1,000, or 1,500 pps (Fig. 1C). These frequencies span the majority of carrier frequencies used clinically in contemporary continuous interleaved samples (CIS) speech processing strategies (e.g., Brill et al. 1997; McDermott et al. 1992; Wilson et al. 1991). The standard signal was repeated continuously (1 s on, 1 s off) while the cat was licking the spoon. On comparison trials (30%), only the modulation frequency was changed (SAM = 30 Hz, 1-s duration), and cats were trained to discriminate this change in the SAM envelope frequency to avoid the UCS (Fig. 1D).

The discrimination task was difficult for deaf cats to learn. To facilitate learning during training sessions, the standard signal level was attenuated relative to the comparison signal level to provide a "loudness" cue. Using the psychophysical method of limits, the attenuation was reduced over several sessions and finally eliminated (cf. Fig. 9). Both standard and comparison signals were then presented at equal intensities, 3 dB above detection threshold. After discrimination performance was stabilized, the psychophysical method of constant stimuli was used to estimate thresholds. The procedural details have been described above. Five SAM frequencies of the CS (range during training: 10-48 Hz; 2- to 8-Hz increment between adjacent envelope frequencies) were presented randomly during a session with the carrier rate constant. For example, in Fig. 10A the discriminative function for the carrier frequency of 300 pps is based on modulation frequencies that ranged from 12 to 28 Hz, with equal increments between the adjacent SAM frequencies of 4 Hz. This procedure was repeated on different days to obtain estimates of thresholds for carriers of 100, 300, 500, 1,000, and 1,500 pps.

Electrophysiological recording procedures

At the conclusion of behavioral testing, the animals were sedated with ketamine/acepromazine. An intravenous catheter was inserted into the cephalic vein, and an areflexic surgical level of anesthesia was induced and maintained with pentobarbital sodium. Vital functions were monitored and maintained at physiological levels. The animal's head was stabilized in a head holder, and the IC and the A1 contralateral to the cochlear implant were exposed surgically for electrophysiological recording.

Tungsten microelectrodes were used to record electrically evoked responses to pulsatile search stimuli (0.2 ms/ph; 2-5 pps) from single neurons and multineuronal clusters in the IC and A1 from each cat (Raggio and Schreiner 1994; Snyder et al. 1990, 1991, 1995; Vollmer et al. 1999). Responses were recorded differentially, band-pass filtered, amplified, and monitored on an oscilloscope (Tektronix 565) and an audio monitor. Based on careful audio-visual monitoring, the stimulus intensity just sufficient to activate the neuron(s) was determined (audio-visual criteria). Thus, at the stimulus threshold intensity, each signal presentation produced a response 50-75% of the time; however, there was no neuronal response when the intensity of the signal was reduced by 1 dB.

In the IC, multineuronal cluster or single neuron thresholds for unmodulated pulse trains of 2-30 pps were determined at 100-µm intervals throughout each penetration (Snyder et al. 1995; Vollmer et al. 1999). Two to four complete penetrations through the IC were obtained in each physiological experiment (Fig. 5A). In the cortex, neuronal thresholds for 2 pps were recorded at intracortical depths of 600-1,200 µm (layer 4) (Raggio and Schreiner 1994). Penetrations were separated by approximately 500 µm, and a complete set of recording locations usually covered the anterior-posterior and the dorsal-ventral dimensions of the A1.

Where possible along an IC penetration, single neurons were isolated, and their threshold responses were recorded. Single-neuron activity was isolated from background noise and artifact using a window discriminator (BAK DIS-1). The stimuli used to estimate single neural thresholds were SAM pulse trains (300/30 AM) and unmodulated pulse trains (2-30 pps). The rates of the unmodulated pulses had no apparent effect on neural thresholds. Relatively few single neuron thresholds were obtained from A1 neurons, and these data will not be reported in the present study.

As determined by data analysis from all recording locations in the IC and the A1 of a given cat, the minimum neuronal threshold was defined as the lowest stimulus intensity that evoked a multineuronal or single neuron response. A comparison of minimum IC and A1 thresholds in 12 deaf cats (4 behaviorally trained cats included in the present study, 8 additional untrained animals; Fig. 3) indicates that minimum neuronal thresholds in the IC (mean: 41.7 dB) and the A1 (mean: 42.8 dB) are virtually identical when measured in the same animal (t-test, P > 0.3). The minimum neuronal threshold for a given animal was determined, therefore, by the lowest threshold estimated in the IC or the A1. Thus, only one threshold value from the most sensitive recording site in the IC or the A1 was used for comparison with the psychophysical threshold in the same animal.



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Fig. 3. Minimum A1 neural thresholds vs. minimum IC neural thresholds (4 trained and 8 untrained deaf cats). Line is x = y.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Psychophysical and neural thresholds

PSYCHOPHYSICAL THRESHOLDS FOR MODULATED AND UNMODULATED PULSE TRAINS. The present study estimated and compared psychophysical detection thresholds for SAM pulse trains and low-frequency, unmodulated pulse trains in the same animals. Figure 4A shows a plot of psychophysical thresholds for SAM signals (100/30 AM or 300/30 AM) versus psychophysical thresholds for unmodulated, low-frequency pulse trains (30 or 100 pps) estimated in six animals. The thresholds for SAM and unmodulated pulse trains ranged from 29.5 to 46.1 dB and 28.5 to 45.1 dB, respectively. The corresponding mean SAM and unmodulated thresholds were 37.2 ± 2.9 (SE) dB and 36.9 ± 2.9 (SE) dB, and the thresholds were strongly correlated (r = 0.99).



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Fig. 4. A: detection thresholds for SAM pulse trains (100/30 AM or 300/30 AM) vs. unmodulated pulse trains (30 or 100 pps) estimated for 6 cats. Line is x = y. B: behavioral threshold differences (SAM threshold minus unmodulated threshold).

Figure 4B illustrates the differences between detection thresholds for unmodulated and SAM signals for single animals. The mean threshold difference between the two signals was 0.3 ± 0.4 (SE) dB, a difference that was not significant (paired t-test; P > 0.5). These results suggest that, compared with unmodulated pulse trains (e.g., 30 pps), the high pulse rate carriers of the SAM signals (e.g., 300/30 AM) do not convey additional information for the detection of the warning signal.

MINIMUM NEURAL THRESHOLDS. Figure 5A illustrates the threshold distribution for one recording penetration as a function of IC depth in cat K117. Because minimum thresholds in the external and central nuclei of the IC were not different (paired t-test; P > 0.05), the minimum IC threshold was determined in each cat from measures across both subdivisions of the IC (cf. Vollmer et al. 1999). Figure 5, B and C, illustrates representative distributions of all IC and A1 thresholds, respectively, recorded in cat K117. In these examples the lowest threshold in the A1 (Fig. 5C; 32 dB) was 2 dB lower than the lowest threshold for the IC (Fig. 5B; 34 dB). According to our criteria for minimum neural threshold (cf. METHODS), in this animal the cortical threshold was used for comparison with the behavioral threshold (horizontal dashed line; 33.6 dB).



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Fig. 5. Distributions of neuronal thresholds in the IC and the A1 for unmodulated pulse trains. A: exemplary threshold distribution vs. IC depth for a single penetration in cat K117. Bold curve: 3-point smoothed spatial tuning curve. Vertical line: border between external (ICX) and central (ICC) nuclei of the inferior colliculus. , single neurons; open circle , multineuronal clusters. B: quantitative distribution of all IC thresholds measured in K117. C: quantitative distribution of all cortical thresholds measured in K117. D: quantitative distribution of all IC thresholds measured in 4 behaviorally trained cats. Thresholds are normalized to behavioral threshold. E: quantitative distribution of all normalized A1 thresholds measured in 6 behaviorally trained cats. Horizontal dashed lines in graphs A-E: normalized behavioral detection threshold = 0 dB. Arrows indicate minimum neural thresholds. n is number of thresholds.

Figure 5, D and E, shows the quantitative distributions of all IC and A1 thresholds, respectively, recorded in six behaviorally trained cats (cf. Fig. 6, A and B). The neuronal thresholds are normalized to the psychophysical threshold of each cat. Most of the neural thresholds are higher than the behavioral threshold. However, the close relationship that exists between minimum neural thresholds from both the IC and the A1 and psychophysical threshold is clearly displayed. Because relatively few neurons approximate the behavioral threshold, the distributions underscore the importance of a sufficient sampling size to verify this close relationship.



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Fig. 6. A: behavioral thresholds for SAM pulse trains vs. minimum neural thresholds for unmodulated pulse trains estimated for 6 cats. For each cat the lowest neural threshold measured in the IC (open circle ) or the A1 () is shown. Line is x = y. B: threshold differences (behavioral threshold minus neural threshold).

COMPARISON OF BEHAVIORAL AND MINIMUM NEURAL THRESHOLDS. Figure 6, A and B, shows the comparisons of minimum neural thresholds for unmodulated, low-frequency pulse trains and psychophysical thresholds for SAM signals for six cats. Due to incomplete sampling of IC thresholds for pulses in K98 and due to electrode failure before the IC experiment in K109, only the A1 thresholds recorded in these cats have been included in the analysis. In the remaining four cats, pulse thresholds were determined in both the IC and the A1. The average number of IC pulse thresholds obtained in each cat was 141. In each cortical experiment, neuronal thresholds for pulses were obtained from 52 to 160 recording sites (average: 107 per experiment).

The six minimum neural thresholds (see METHODS) shown in Fig. 6A were obtained from a total of 1,005 thresholds (IC: n = 562; A1: n = 443) recorded in the six animals. Two of the minimum neural thresholds shown in the figure were recorded in the IC (open circle ) and four in the A1 (). To minimize the influence of changes in detection threshold over time, only the psychophysical thresholds estimated closest to the time of the acute electrophysiological experiment (i.e., SAM thresholds) were included in the comparison with minimum neural thresholds. Because psychophysical detection thresholds for SAM and unmodulated pulses were virtually identical (Fig. 4, A and B), a comparison of minimum neural thresholds and behavioral thresholds for low-frequency unmodulated pulses would have demonstrated essentially identical results to those presented in Fig. 6.

Figure 6A illustrates the strong correlation (r = 0.93) obtained between the behavioral and minimum neural thresholds. Minimum neural thresholds from either the IC or the A1 were not consistently located below or above psychophysical thresholds. Psychophysical thresholds ranged from 30.6 dB (K98) to 47.8 dB (CH618); neural thresholds ranged from 29 dB (K98) to 51 dB (CH618). The mean values for psychophysical and minimum neural thresholds were 36.7 ± 2.5 (SE) dB and 36.5 ± 3.2 (SE) dB, respectively. It should be noted that the highest threshold values shown in Fig. 6A were obtained from a long deafened cat with very poor nerve survival (CH618; >4 yr of deafness, spiral ganglion cell density 1.3% of normal). Figure 6B shows the threshold differences between behavioral and neural thresholds among the six animals. These threshold differences ranged from -3.3 dB (K109) to 3.5 dB (K107). The average threshold difference [0.3 ± 1.1 (SE) dB] was not statistically significant (paired t-test; P > 0.8).

In summary, the results from Figs. 4 and 6 indicate that minimum neural thresholds for low-frequency unmodulated pulse trains are virtually identical to behavioral thresholds for either SAM or low-frequency unmodulated pulse trains. These findings suggest that the most sensitive neurons in the IC and the primary auditory cortex contribute to psychophysical detection of electrical stimulation of surviving ganglion cells in the deaf cochlea.

Single-neuron thresholds in the IC for modulated and unmodulated pulse trains

Neuronal response thresholds for SAM signals (300/30 AM) and unmodulated pulse trains were measured and compared in 127 single IC neurons (Fig. 7). The stimulus frequencies used to determine neural thresholds for unmodulated pulse trains ranged from 3 to 30 pps. Over this range, single-neuron response thresholds were not affected by the frequency of the unmodulated pulse train.



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Fig. 7. Single neuronal thresholds in the IC for SAM (300/30 AM) pulse trains vs. unmodulated pulse trains. Shaded area (bottom left) encloses neuronal thresholds that fell within the range of psychophysical thresholds. Line is x = y. n is number of neurons.

As illustrated in Fig. 7, neural thresholds for both SAM and unmodulated pulse trains cover a broad range of intensities (39-60 dB and 39-59 dB, respectively). The dispersion or scatter observed for the two threshold measures increases slightly at intensities of 49 dB or above. At these higher intensities, the standard step size of 1 dB is a larger step in absolute current than the current step at lower intensities. As a result, estimation of neural thresholds is less precise at higher intensities.

For the data illustrated in Fig. 7, the mean thresholds for SAM and unmodulated signals were 51.1 dB (359 µA) and 50.7 dB (343 µA), respectively, and neural thresholds for the two kinds of signals were strongly correlated (r = 0.96). The mean threshold difference for the two signals is relatively small (0.4 dB or 15.5 µA), but this difference was significant (paired t-test; t = 4.04; df = 126; P < 0.001).

When the comparison of neural thresholds was limited to stimulus intensities that fell within the ranges of psychophysical thresholds (cf. Figs. 4A and 6A), a different result was obtained. The psychophysically relevant threshold ranges are depicted by the shaded area in the bottom left of Fig. 7. The average neural thresholds (n = 13 pairs) were 40.9 ± 0.5 (SE) dB for SAM pulses and 40.7 ± 0.5 (SE) dB for unmodulated pulse trains, and the threshold difference was only 0.2 dB or 3.2 µA. This threshold difference was not significant (paired t-test; P > 0.2). These results are consistent with the psychophysical finding reported above that detection thresholds for SAM and unmodulated pulse trains are equivalent for the two kinds of signals (Figs. 2 and 4, A and B). However, we cannot rule out the possibility that the identical IC neural thresholds are due to the small sample size (n = 13 pairs), because 7 of 10 comparisons of 13 randomly selected pairs of SAM and unmodulated thresholds outside the psychophysical threshold range were also not significant (P > 0.05).

Effects of SAM carrier and envelope frequencies on psychophysical thresholds

An important issue in the current study was whether psychophysical thresholds for SAM signals were affected by the carrier frequency, the modulation frequency, or both when measured in the same animal. For example, interactions between carrier and modulation frequencies might influence behavioral detection of SAM pulse trains. In Fig. 8 psychometric functions for two animals (K119 and K55) show the probability of detection as a function of the intensity of SAM warning signals with different modulation and carrier frequencies. The slopes for the linear portion of the functions indicate that the probability of detection between 0.25 and 0.75 occurred within 2-3 dB, i.e., the slopes of the psychometric functions for SAM pulses (0.2 ms/ph) are comparable to the slopes of psychometric functions reported for 0.2 ms/ph unmodulated pulses (Beitel et al. 2000a). The slopes of these curves represent the range of slopes for all psychometric functions obtained in the cats included in this study (cf. Fig. 2).



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Fig. 8. Psychometric functions showing probability of detection as a function of the intensity for SAM warning signals in cats K119 (A) and K55 (B). The legend indicates the carrier and modulation frequencies. Dashed lines: 50% detection. The arrows depict the range of thresholds. The rank order of the detection thresholds does not change systematically with the parameters (carrier or envelope frequency) of the SAM signals.

The ranges of thresholds for the different signals are indicated by the arrows on the abscissae. Figure 8A illustrates psychometric functions for cat K119 for three different SAM signal combinations of 300/30 AM, 500/30 AM, and 300/8 AM. The lowest threshold was observed for 300/30 AM (29.5 dB), and the highest threshold was observed for 300/8 AM (30.6 dB). Thus in this animal the maximum threshold difference for the SAM signals was 1.1 dB.

Figure 8B depicts psychometric functions for cat K55 for the same three SAM signal combinations. The lowest threshold was obtained for 300/8 AM (36.5 dB) and the highest for 300/30 AM (37.5 dB); i.e., thresholds for the given SAM signals were within 1 dB.

An examination of the results shown in Fig. 8, A and B, indicate that the rank order of the detection thresholds did not change systematically with the parameters (carrier or envelope frequency) of the SAM signals. Thus, these results indicate that within the range of tested frequencies, detection thresholds are independent of the carrier and modulation frequencies.

Successive discrimination of SAM signals

The results in the preceding section provided essential information that guided our choice of stimuli used for training and testing cats on a successive discrimination task. Because our results show that detection thresholds and psychometric functions for different modulation frequencies are equivalent at a particular carrier rate, we reasoned that discrimination of a change in the envelope or modulation frequency should be based on temporal rather than amplitude or intensity cues. Thus, SAM signals with modulation and carrier frequencies similar to those reported in the preceding section were used to train four deaf cats on a successive discrimination task. Three cats were trained to discriminate SAM signals with carrier frequencies of 100, 300, and 500 pps. In addition, two of these animals were trained to discriminate SAM signals with higher carrier frequencies of 1,000 and 1,500 pps.

The immediate goals of our discrimination experiment were 1) to investigate whether deaf cats could be trained to discriminate SAM signals; 2) if so, to estimate the difference limens for successful discrimination; and 3) to determine whether a cat's ability to discriminate SAM signals was exclusively dependent on the animal's ability to resolve difference in the temporal structure of the modulating envelope or whether the animal's performance was influenced, as well, by the carrier frequencies.

As noted in METHODS, the standard signal (300/8 AM) was attenuated relative to the comparison signal (carrier peak intensity 3 dB above detection threshold) to provide a "loudness" cue during training on the successive discrimination task. Over several sessions the attenuation was reduced. In Fig. 9, A and B, the probability of detection when the standard signal was attenuated (4 to 1 dB attenuation) is shown by open symbols for two cats (K98 and K99). For example, in session 1, cat K98 (Fig. 9A) performed above detection threshold [p(D) = 50%; horizontal dashed line] for averaged trials with an intensity difference between standard and comparison signal of 4 dB, but performance deteriorated when the difference was reduced to 3 dB. Cat K99 (Fig. 9B) performed below threshold in the first training session despite an intensity difference between standard and comparison signal of 4 dB. In sessions 12 (K98) and 11 (K99) the attenuation was eliminated (filled symbols; 0 dB attenuation of the standard signal re comparison signal). Under this condition, detection thresholds and psychometric functions for all modulation and carrier frequency combinations used are virtually identical (cf. Fig. 8). In the last two training sessions, both cats were able to detect [p(D) = 50%] a change in the SAM envelope frequency (300/8 AM vs. 300/30 AM) without the aid of an attenuated standard signal. Discrimination thresholds and modulation difference limens (DL) were then determined based on the method of constant stimuli. Discriminative threshold testing could not be completed for cat K98.



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Fig. 9. A and B: learning profiles for 2 cats during successive discrimination training. Probability of detection when the Standard SAM signal (300/8 AM) was attenuated (4 to 1 dB) relative to the Comparison SAM signal (300/30 AM) is shown by open symbols. Over several sessions the levels of the "loudness" cues were reduced and finally eliminated (filled symbols; 0 dB attenuation). Each symbol indicates the probability of detection (method of limits) based on trials run at the attenuation shown in the legend. Dashed lines: 50% avoidance.

We investigated whether carrier frequencies influenced the animal's performance on the discrimination task. Note that the standard and comparison signals always had the same carrier rate in a given testing session, and the modulation frequency of the standard signal was 8 Hz throughout all behavioral testing. Figure 10, A, C, and E, shows performance functions for discrimination of the envelope frequencies of the comparison signals by cats K99, K148, and K146. The carrier rate of the signals varied between 100 and 1,500 pps. For cat K99, discrimination testing was concluded after training on three carrier frequencies (100, 300, and 500 pps). An animal's discrimination thresholds [p(Discrimination) = 50%] for the envelope or modulation frequency of the comparison signal were determined by linear interpolation from the dashed lines to the abscissae in Fig. 10, A, C, and E, and the ranges of thresholds are depicted by the arrows in each plot. In each animal, threshold testing was conducted within a 4-wk period, and each performance function for a given carrier frequency includes 3.6 ± 0.3 (SE) threshold sessions. During the time of testing, an animal's general behavior and various factors with possible influence on behavioral performance (e.g., device integrity, EABR thresholds, electrode impedances) remained stable.



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Fig. 10. Successive discrimination of SAM pulse trains by 3 cats. A, C, and E: discriminative functions showing probability of discrimination as a function of the modulation frequency of Comparison SAM signals. Parameter is carrier frequency. The Standard SAM signal was constant (8 Hz). Note the different scale on the abscissa in A. Thresholds (50% discrimination) were determined by linear interpolation from the dashed lines to the abscissae. Threshold ranges for different carrier frequencies are indicated by arrows. B, D, and F: modulation difference limens (DL) in Hz vs. signal carrier rate (pps).

For modulated signals with different carrier frequencies, the difference limens (DL = Comparison SAM frequency minus Standard SAM frequency) for successive discrimination of changes in the SAM envelope are illustrated in Fig. 10, B, D, and F. In cat K99 (Fig. 10, A and B), the estimated modulation frequencies required for discrimination of comparison signals with carrier frequencies of 100, 300, and 500 pps were 16.0, 15.9, and 17.5 Hz, respectively, which are equivalent to DLs of 8, 7.9, and 9.5 Hz. The mean DL was 8.4 ± 0.9 (SD) Hz, and all DLs were within 1.5 Hz. In cat K148 (Fig. 10, C and D), the DLs for comparison signals with carrier frequencies of 100, 300, 500, 1,000, and 1,500 pps were 4.2, 4.4, 4.7, 4.8, and 5.0 Hz, respectively. The mean DL was 4.6 ± 0.3 (SD) Hz, and all DLs were within 1 Hz. In cat K146 (Fig. 10, E and F), the DLs for comparison signals with the same carrier frequencies were 3.4, 4.9, 3.8, 3.3, and 4.1 Hz, respectively. All DLs were within 1.7 Hz with a mean DL of 3.9 ± 0.6 (SD) Hz. Although discriminative performance varied across animals, there was no effect of carrier frequency on discrimination thresholds in any of the trained cats (t-tests; P > 0.05).

For each cat, the slopes [p(Discrimination)/Comparison SAM (Hz)] of the discriminative functions between p(Discrimination) 0.25 and 0.75 were estimated by linear regression for the linear portion of the function. The animal with the poorest discriminative performance across all carrier frequencies (K99) had discriminative functions with the shallowest slopes, whereas the animal with the best performance (K146) had discriminative functions with the steepest slopes. However, the slopes did not change systematically with the carrier frequencies in any of the cats.

These results suggest that an animal's performance was based exclusively on the discrimination of changes in the envelope of the SAM signals, whereas changes in the carrier rate had no obvious effect on performance.


    DISCUSSION
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METHODS
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The current study has shown that 1) psychophysical detection thresholds for unmodulated and SAM pulse trains were virtually identical when measured in the same animals, and these thresholds were strongly correlated with the minimum neural response thresholds recorded in the IC or the A1 of the deaf cats; 2) response thresholds for IC neurons were virtually identical for unmodulated and SAM signals at stimulus intensities corresponding to those used in behavioral testing; and 3) deaf cats successfully discriminated differences in the modulation frequencies of SAM pulse trains. For both auditory detection and discrimination in the deaf cat, the carrier rate had no apparent effect on performance.

Psychophysical detection thresholds

In a preliminary study Beitel et al. (2000b) reported that behavioral thresholds for unmodulated and SAM pulse trains were essentially the same. From these findings it was hypothesized that psychophysical thresholds for unmodulated and SAM pulse trains are based on the detection of the peak pulse amplitude of the signal. Equal thresholds occur when the peak pulse amplitudes are equal, i.e., when the amplitude of unmodulated pulses equals the maximum envelope amplitude of SAM pulses. However, in this earlier study only two different combinations of SAM signals were used, and psychophysical thresholds for unmodulated pulse trains determined in one group of animals were compared with those for SAM pulse trains determined in another group of animals. The present study included additional combinations of SAM carrier and modulation frequencies and determined psychophysical detection thresholds for unmodulated and SAM signals in the same animals, i.e., differences in intracochlear electrode position, electrode impedances, spiral ganglion cell survival, etc., were identical for both threshold measures. The current results indicate that, within the ranges of tested frequencies, psychophysical detection thresholds for SAM (modulation frequency: 8-30 Hz, carrier rate: 100-500 pps) and unmodulated pulse trains (30-100 pps) were virtually identical and were independent of the carrier and the modulation frequencies of the SAM comparison signal (cf. Figs. 4, A and B, and 8). In other words, the effective threshold amplitude for unmodulated and SAM signals is equivalent to the peak amplitude of the pulses in the unmodulated or modulated carrier. Thus, our results strongly support the hypothesis that detection threshold for unmodulated and SAM pulse trains is determined by the peak pulse amplitude of the signal (Beitel et al. 2000b).

Several investigators have shown that psychophysical thresholds for unmodulated pulse trains are affected by pulse rate (Beitel et al. 2000a; Pfingst and Morris 1993; Shannon 1985). In the current study the thresholds estimated for unmodulated pulse trains presented at 30 or 100 pps were analyzed as a single data set in the comparisons of psychophysical thresholds (cf. Fig. 4). Although detection thresholds may be affected by pulse rate, the analysis based on data collected at 30 and 100 pps is justified by the fact that the threshold difference for short phase duration (0.2 ms/ph) unmodulated pulse trains delivered over a frequency range of 30-100 pps is <1 dB (Beitel et al. 2000a; Shannon 1985).

If psychophysical thresholds are determined by the peak pulse amplitude of the signal, the effective stimulus rate for SAM signals corresponds to the envelope frequency rather than to the carrier rate. Thus, the envelope frequency of SAM signals should affect detection threshold in a manner similar to that reported for the frequency of unmodulated pulse trains (Shannon 1989). Our finding that detection thresholds for low-frequency unmodulated pulse trains and SAM signals with low envelope frequencies are nearly identical is consistent with this hypothesis. However, future studies with broader ranges of envelope and carrier frequencies are required to evaluate the extent to which psychophysical detection of SAM signals is affected by the modulation rate.

Single-neuron thresholds in the IC for unmodulated and SAM pulse trains

We have shown for the first time that, within single IC neurons, thresholds for SAM and unmodulated, low-frequency pulse trains are significantly correlated. Moreover, for stimulus intensities that fell within the range of psychophysical thresholds (cf. Figs. 4A and 6A), single-neuron thresholds in the IC for the two kinds of signals were virtually identical (mean difference = 0.2 dB or 3.2 µA; cf. Fig. 7). These neural data are consistent with our finding that psychophysical thresholds for SAM and unmodulated pulse trains are based on the detection of the peak pulse amplitude of the signal (also cf. Beitel et al. 2000b). Thus, a reasonable conclusion is that peak pulse detection in IC neurons may contribute to psychophysical threshold detection for unmodulated and SAM pulsatile signals. Further, SAM carrier pulses delivered at intensities below the peak pulse detection level of IC neurons have no apparent effect on psychophysical detection. However, as noted in RESULTS, we cannot exclude the possibility that the identical thresholds obtained for SAM and unmodulated signals is due to the relatively small sample size of neurons with thresholds in the range of psychophysical thresholds.

When neural thresholds that were higher than the highest psychophysical thresholds were included in the analysis (cf. Fig. 7), our results show that IC neural thresholds for SAM signals were slightly (0.4 dB or 15.5 µA) but significantly higher than those for unmodulated pulse trains. This result may reflect methodological limitations in our recording procedures. At higher stimulus intensities the signal-to-noise ratio was relatively poor, and the stimulus artifact was relatively large for the higher frequency pulse rates of SAM signals compared with the low-frequency unmodulated pulse trains delivered at the same peak intensity. As a result, neural threshold responses to unmodulated pulse trains were easily detected by audio-visual monitoring, whereas responses to SAM pulse trains may have been obscured by stimulus artifact or noise. To reliably detect an audio-visual threshold response, we may have inadvertently increased the stimulus intensity of the SAM pulse trains by an average of 0.4 dB. Parkins and Colombo (1987) have suggested similar limitations of the threshold detection technique as the source for a small (<0.5 dB) but significant increase in auditory nerve fiber thresholds for electrical intracochlear stimulation when the frequency of unmodulated pulse trains (0.2 ms/ph) was increased from 156 to 625 pps.

However, there may have been a real physiological increase in neural thresholds associated with SAM signals in the present study. In this case, we are presently unable to explain this result.

Relationship between psychophysical and neural thresholds

It is noteworthy that psychophysical and minimum IC and A1 neural threshold values were remarkably close when directly compared in the same animals (cf. Fig. 6, A and B). These findings are consistent with the suggestion that neuronal activity in the auditory midbrain and the auditory forebrain contributes to behavioral detection in electrical hearing (Beitel et al. 2000a,b).

Our results may be contrasted to the discrepancies reported for comparisons of behavioral and auditory nerve fiber thresholds between species and across different laboratories (Pfingst 1988). These indirect comparisons indicated that neural thresholds are consistently and substantially higher than behavioral thresholds. A number of factors may have confounded these comparisons including interspecies differences, differences in the stimulating electrodes and the electrode placements, differences in duration of deafness and nerve survival, differences in the definition of thresholds, and sampling bias in recording auditory nerve fibers. In our model most of these factors were eliminated or controlled. In addition, spatial and temporal integration of excitatory activity at the level of the IC and the A1 may have enhanced the probability for recording low-threshold neurons in these central auditory structures.

The results of the current study demonstrate that when comparisons were made in the same animal, behavioral thresholds and minimum neural thresholds in the IC and the A1 were virtually identical (mean difference, 0.28 dB). This result highlights the advantage and validity of comparing behavioral and central neuronal thresholds in the same animal (Beitel et al. 2000a,b) and indicates that our deaf animal model provides a solid basis for assessing the relationship between behavioral and electrophysiological thresholds for intracochlear electrical stimulation.

Successive discrimination of SAM signals

At suprathreshold levels, the temporal structure of amplitude-modulated signals may play an important role in the central auditory processing that enables CI users to recognize speech (Shannon et al. 1995). An important goal in the present study was to train deaf cats to discriminate a change in the modulation frequency of SAM pulsatile carriers with the intention to use this animal model to investigate temporal resolution in the deaf auditory system. To our knowledge, this is the first study in a behavioral animal model to use stimuli that approximate the characteristics of stimuli used in signal processing strategies for contemporary cochlear implants.

Two issues that are relevant to the interpretation of discriminative performance in our study deserve additional comment. First, we have shown that an intensity difference between the standard and comparison stimuli facilitated learning, and in monkeys, frequency difference limens for electrical cochlear stimulation decreased as the stimulus intensity increased (Pfingst and Rai 1990). Although we eliminated the intensity difference between standard and comparison signals in the final stage of training in the successive discrimination task, we cannot exclude the possibility of a loudness cue. However, Zeng and Shannon (1995) have reported that a modulated high-frequency pulsatile carrier in CI users had the same underlying exponential loudness function as the unmodulated carrier, i.e., modulation had no effect on loudness. Further, in the present study, psychophysical threshold estimates for SAM signals similar to those used in the discrimination task have shown that at lower carrier frequencies (<= 500 pps) thresholds and suprathreshold levels of detection are similar for the different modulation or carrier frequencies (cf. Fig. 8).

Second, we have reported previously that at suprathreshold stimulus intensities most IC neurons are able to follow unmodulated pulses at rates of <= 40 pps but are unable to follow rates >100 pps (Snyder et al. 1995, 2000; Vollmer et al. 1999). These neurons are also able to follow SAM pulse trains at modulation frequencies of 8-40 Hz (Snyder et al. 2000), i.e., the range of modulation frequencies used in the successive discrimination training. Although the mean maximum following rate for A1 neurons to unmodulated electrical pulse trains is around 12-14 pps (Schreiner and Raggio 1996), studies using acoustical stimuli have shown that large populations of auditory cortical neurons discharged with maximum rates at modulation frequencies centered around 16-32 Hz (Beitel et al. 1995; Liang et al. 1999; Schreiner and Urbas 1986). Because the range of discrimination thresholds (11.3-17.5 Hz) for SAM modulation frequencies in the current study was well within the range of maximum following rates for IC and A1 neurons, and because the carrier rate and the peak current intensities of the standard and the comparison signals were the same during a testing session, we conclude that discrimination of the envelope frequency in the present study was based on a temporal rather than an intensity cue. Thus, it is likely that temporal encoding of the envelope frequencies by the auditory midbrain and by the primary auditory cortex contributes to successful performance in the discrimination task.

Finally, the finding that there were virtually no differences in discriminability of SAM signals as a function of carrier rate is consistent with the interpretation that performance in the discrimination task was based on temporal resolution of a difference in envelope frequencies between the standard and comparison signals. Although a proportion of the SAM carrier pulses were presented at suprathreshold levels, the carrier rate apparently did not affect the discrimination process. This interpretation is also consistent with the observation that most neurons in the IC are insensitive to the carrier rate but sensitive to the modulation frequency of SAM electrical pulsatile stimuli (Snyder et al. 2000).

Conclusions

Based on the results of the present study, we conclude the following. First, psychophysical and neural detection thresholds for low-frequency unmodulated pulse trains and SAM pulse trains with low modulation frequencies are based on peak pulse amplitude detection. Thus, we conclude that the effective psychophysical and neural stimulus rate of SAM signals is the modulation frequency rather than the carrier rate.

Second, psychophysical and neural thresholds for unmodulated and SAM pulse trains are virtually identical when measured in the same animal. Although any threshold estimation is dependent on specific criteria, and changes in these criteria may alter threshold values, it is unlikely that the strong association between behavioral and neural thresholds would be altered significantly by simple changes in the definition of threshold. We conclude that the behavioral and neurophysiological threshold comparisons reported above represent robustly correlated events in the perceptual and physiological domains because 1) both measures were affected similarly by variation of a key stimulus parameter (intensity); 2) both measures were based on antecedent neural activity evoked by electrical intracochlear stimulation of the auditory nerve; and 3) both measures were compared in the same animal, thus excluding many factors that contribute to intersubject variability.

Third, we conclude that neural temporal resolution of changes in the modulation frequencies between two successive signals allows deaf cats to discriminate SAM pulse trains. Presumably neural mechanisms in the IC and the A1 contribute to successful behavioral discrimination. The results suggest that our animal model provides a solid basis for future electrophysiological and behavioral studies of temporal resolution of intracochlear electrical signals in the deaf central auditory system. The reported findings also provide useful information for the design and calibration of contemporary speech processing strategies and, thus, for the quality of speech discrimination in CI users.


    ACKNOWLEDGMENTS

We thank E. Dwan, M. Fong, and S. Rebscher for technical assistance and P. Leake, C. Moore, M. Raggio, S. Rebscher, and C. Schreiner for participating in the collection of neurophysiological data.

This research was supported by National Institute on Deafness and Other Communication Disorders Contracts N01-DC-7-2105, N01-DC-0-2108, and Deutsche Forschungsgemeinschaft Vo 640/1-1.


    FOOTNOTES

Address for reprint requests: M. Vollmer, Dept. of Physiology II, J. W. Goethe-University, Theodor-Stern-Kai 7, 60596 Frankfurt/Main, Germany (E-mail: vollmer{at}itsa.ucsf.edu).

Received 18 August 2000; accepted in final form 19 July 2001.


    REFERENCES
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

0022-3077/01 $5.00 Copyright © 2001 The American Physiological Society