Normal behavioral discrimination of envelope statistics in budgerigars with kainate-induced cochlear synaptopathy.

Cochlear synaptopathy is a common pathology in humans associated with aging and potentially sound overexposure. Synaptopathy is widely expected to cause "hidden hearing loss," including difficulty perceiving speech in noise, but support for this hypothesis is controversial. Here in budgerigars (Melopsittacus undulatus), we evaluated the impact of long-term cochlear synaptopathy on behavioral discrimination of Gaussian noise (GN) and low-noise noise (LNN) signals processed to have a flatter envelope. Stimuli had center frequencies of 1-3kHz, 100-Hz bandwidth, and were presented at sensation levels (SLs) from 10 to 30dB. We reasoned that narrowband, low-SL stimuli of this type should minimize spread of excitation across auditory-nerve fibers, and hence might reveal synaptopathy-related defects if they exist. Cochlear synaptopathy was induced without hair-cell injury using kainic acid (KA). Behavioral threshold tracking experiments characterized the minimum stimulus duration above which animals could reliably discriminate between LNN and GN. Budgerigar thresholds for LNN-GN discrimination ranged from 40 to 60ms at 30dB SL, were similar across frequencies, and increased for lower SLs. Notably, animals with long-term 39-77% estimated synaptopathy performed similarly to controls, requiring on average a ∼7.5% shorter stimulus duration (-0.7±1.0dB; mean difference ±SE) for LNN-GN discrimination. Decision-variable correlation analyses of detailed behavioral response patterns showed that individual animals relied on envelope cues to discriminate LNN and GN, with lesser roles of FM and energy cues; no difference was found between KA-exposed and control groups. These results suggest that long-term cochlear synaptopathy does not impair discrimination of low-level signals with different envelope statistics.

Histological Correlates of Auditory Nerve Injury from Kainic Acid in the Budgerigar (Melopsittacus undulatus).

PURPOSE: Loss of auditory nerve afferent synapses with cochlear hair cells, called cochlear synaptopathy, is a common pathology in humans caused by aging and noise overexposure. The perceptual consequences of synaptopathy in isolation from other cochlear pathologies are still unclear. Animal models provide an effective approach to resolve uncertainty regarding the physiological and perceptual consequences of auditory nerve loss, because neural lesions can be induced and readily quantified. The budgerigar, a parakeet species, has recently emerged as an animal model for synaptopathy studies based on its capacity for vocal learning and ability to behaviorally discriminate simple and complex sounds with acuity similar to humans. Kainic acid infusions in the budgerigar produce a profound reduction of compound auditory nerve responses, including wave I of the auditory brainstem response, without impacting physiological hair cell measures. These results suggest selective auditory nerve damage. However, histological correlates of neural injury from kainic acid are still lacking. METHODS: We quantified the histological effects caused by intracochlear infusion of kainic acid (1 mM; 2.5 µL), and evaluated correlations between the histological and physiological assessments of auditory nerve status. RESULTS: Kainic acid infusion in budgerigars produced pronounced loss of neural auditory nerve soma (60% on average) in the cochlear ganglion, and of peripheral axons, at time points 2 or more months following injury. The hair cell epithelium was unaffected by kainic acid. Neural loss was significantly correlated with reduction of compound auditory nerve responses and auditory brainstem response wave I. CONCLUSION: Compound auditory nerve responses and wave I provide a useful index of cochlear synaptopathy in this animal model.

Mechanisms of masking by Schroeder-phase harmonic tone complexes in the budgerigar (Melopsittacus undulatus).

Schroeder-phase harmonic tone complexes can have a flat temporal envelope and rising or falling instantaneous-frequency sweeps within F0 periods, depending on the phase-scaling parameter C. Human tone-detection thresholds in a concurrent Schroeder masker are 10-15 dB lower for positive C values (rising frequency sweeps) compared to negative (falling sweeps), potentially due to cochlear mechanics, though this hypothesis remains controversial. Birds provide an interesting model for studies of Schroeder masking because many species produce vocalizations containing frequency sweeps. Prior behavioral studies in birds suggest less behavioral threshold difference between maskers with opposite C values than in humans, but focused on low masker F0s and did not explore neural mechanisms. We performed behavioral Schroeder-masking experiments in budgerigars (Melopsittacus undulatus) using a wide range of masker F0 and C values. Signal frequency was 2800 Hz. Neural recordings from the midbrain characterized encoding of behavioral stimuli in awake animals. Behavioral thresholds increased with increasing masker F0 and showed minimal difference between opposite C values, consistent with prior budgerigar studies. Midbrain recordings showed prominent temporal and rate-based encoding of Schroeder F0, and in many cases, marked asymmetry in Schroeder responses between C polarities. Neural thresholds for Schroeder-masked tone detection were often based on a response decrement compared to the masker alone, consistent with prominent modulation tuning in midbrain neurons, and were generally similar between opposite C values. The results highlight the likely importance of envelope cues in Schroeder masking and show that differences in supra-threshold Schroeder responses do not necessarily result in neural threshold differences.

Midbrain-Level Neural Correlates of Behavioral Tone-in-Noise Detection: Dependence on Energy and Envelope Cues.

Hearing in noise is a problem often assumed to depend on encoding of energy level by channels tuned to target frequencies, but few studies have tested this hypothesis. The present study examined neural correlates of behavioral tone-in-noise (TIN) detection in budgerigars (Melopsittacus undulatus, either sex), a parakeet species with human-like behavioral sensitivity to many simple and complex sounds. Behavioral sensitivity to tones in band-limited noise was assessed using operant-conditioning procedures. Neural recordings were made in awake animals from midbrain-level neurons in the inferior colliculus, the first processing stage of the ascending auditory pathway with pronounced rate-based encoding of stimulus amplitude modulation. Budgerigar TIN detection thresholds were similar to human thresholds across the full range of frequencies (0.5-4 kHz) and noise levels (45-85 dB SPL) tested. Also as in humans, thresholds were minimally affected by a challenging roving-level condition with random variation in background-noise level. Many midbrain neurons showed a decreasing response rate as TIN signal-to-noise ratio (SNR) was increased by elevating the tone level, a pattern attributable to amplitude-modulation tuning in these cells and the fact that higher SNR tone-plus-noise stimuli have flatter amplitude envelopes. TIN thresholds of individual neurons were as sensitive as behavioral thresholds under most conditions, perhaps surprisingly even when the unit's characteristic frequency was tuned an octave or more away from the test frequency. A model that combined responses of two cell types enhanced TIN sensitivity in the roving-level condition. These results highlight the importance of midbrain-level envelope encoding and off-frequency neural channels for hearing in noise.SIGNIFICANCE STATEMENT Detection of target sounds in noise is often assumed to depend on energy-level encoding by neural processing channels tuned to the target frequency. In contrast, we found that tone-in-noise sensitivity in budgerigars was often greatest in midbrain neurons not tuned to the test frequency, underscoring the potential importance of off-frequency channels for perception. Furthermore, the results highlight the importance of envelope processing for hearing in noise, especially under challenging conditions with random variation in background noise level over time.

Normal Tone-In-Noise Sensitivity in Trained Budgerigars despite Substantial Auditory-Nerve Injury: No Evidence of Hidden Hearing Loss.

Loss of auditory-nerve (AN) afferent cochlear innervation is a prevalent human condition that does not affect audiometric thresholds and therefore remains largely undetectable with standard clinical tests. AN loss is widely expected to cause hearing difficulties in noise, known as "hidden hearing loss," but support for this hypothesis is controversial. Here, we used operant conditioning procedures to examine the perceptual impact of AN loss on behavioral tone-in-noise (TIN) sensitivity in the budgerigar (Melopsittacus undulatus; of either sex), an avian animal model with complex hearing abilities similar to humans. Bilateral kainic acid (KA) infusions depressed compound AN responses by 40-70% without impacting otoacoustic emissions or behavioral tone sensitivity in quiet. Surprisingly, animals with AN damage showed normal thresholds for tone detection in noise (0.1 ± 1.0 dB compared to control animals; mean difference ± SE), even under a challenging roving-level condition with random stimulus variation across trials. Furthermore, decision-variable correlations (DVCs) showed no difference for AN-damaged animals in their use of energy and envelope cues to perform the task. These results show that AN damage has less impact on TIN detection than generally expected, even under a difficult roving-level condition known to impact TIN detection in individuals with sensorineural hearing loss (SNHL). Perceptual deficits could emerge for different perceptual tasks or with greater AN loss but are potentially minor compared with those caused by SNHL.SIGNIFICANCE STATEMENT Loss of auditory-nerve (AN) cochlear innervation is a common problem in humans that does not affect audiometric thresholds on a clinical hearing test. AN loss is widely expected to cause hearing problems in noise, known as "hidden hearing loss," but existing studies are controversial. Here, using an avian animal model with complex hearing abilities similar to humans, we examined for the first time the impact of an experimentally induced AN lesion on behavioral tone sensitivity in noise. Surprisingly, AN-lesioned animals showed no difference in hearing performance in noise or detection strategy compared with controls. These results show that perceptual deficits from AN damage are smaller than generally expected, and potentially minor compared with those caused by sensorineural hearing loss (SNHL).

Effects of Kainic Acid-Induced Auditory Nerve Damage on Envelope-Following Responses in the Budgerigar (Melopsittacus undulatus).

Sensorineural hearing loss is a prevalent problem that adversely impacts quality of life by compromising interpersonal communication. While hair cell damage is readily detectable with the clinical audiogram, this traditional diagnostic tool appears inadequate to detect lost afferent connections between inner hair cells and auditory nerve (AN) fibers, known as cochlear synaptopathy. The envelope-following response (EFR) is a scalp-recorded response to amplitude modulation, a critical acoustic feature of speech. Because EFRs can have greater amplitude than wave I of the auditory brainstem response (ABR; i.e., the AN-generated component) in humans, the EFR may provide a more sensitive way to detect cochlear synaptopathy. We explored the effects of kainate- (kainic acid) induced excitotoxic AN injury on EFRs and ABRs in the budgerigar (Melopsittacus undulatus), a parakeet species used in studies of complex sound discrimination. Kainate reduced ABR wave I by 65-75 % across animals while leaving otoacoustic emissions unaffected or mildly enhanced, consistent with substantial and selective AN synaptic loss. Compared to wave I loss, EFRs showed similar or greater percent reduction following kainate for amplitude-modulation frequencies from 380 to 940 Hz and slightly less reduction from 80 to 120 Hz. In contrast, forebrain-generated middle latency responses showed no consistent change post-kainate, potentially due to elevated "central gain" in the time period following AN damage. EFR reduction in all modulation frequency ranges was highly correlated with wave I reduction, though within-animal effect sizes were greater for higher modulation frequencies. These results suggest that even low-frequency EFRs generated primarily by central auditory nuclei might provide a useful noninvasive tool for detecting synaptic injury clinically.

Identifying cues for tone-in-noise detection using decision variable correlation in the budgerigar (Melopsittacus undulatus).

Previous studies evaluated cues for masked tone detection using reproducible noise waveforms. Human results founded on this approach suggest that tone detection is based on combined energy and envelope (ENV) cues, but detection cues in nonhuman species are less clear. Decision variable correlation (DVC) was used to evaluate tone-in-noise detection cues in the budgerigar, an avian species with human-like behavioral sensitivity to many complex sounds. DVC quantifies a model's ability to predict trial-by-trial variance in behavioral responses. Budgerigars were behaviorally conditioned to detect 500-Hz tones in wideband (WB; 100-3000 Hz) and narrowband (NB; 452-552 Hz) noise. Behavioral responses were obtained using a single-interval, two-alternative discrimination task and two-down, one-up adaptive tracking procedures. Tone-detection thresholds in WB noise were higher than human thresholds, putatively due to broader peripheral frequency tuning, whereas NB thresholds were within ∼1 dB of human results. Budgerigar average hit and false-alarm rates across noise waveforms were consistent, highly correlated across subjects, and correlated to human results. Trial-by-trial behavioral results in NB noise were best explained by a model combining energy and ENV cues. In contrast, WB results were better predicted by ENV-based or multiple-channel energy detector models. These results suggest that budgerigars and humans use similar cues for tone-in-noise detection.

Effects of selective auditory-nerve damage on the behavioral audiogram and temporal integration in the budgerigar.

Auditory-nerve fibers are lost steadily with age and as a possible consequence of noise-induced glutamate excitotoxicity. Auditory-nerve loss in the absence of other cochlear pathologies is thought to be undetectable with a pure-tone audiogram while degrading real-world speech perception (hidden hearing loss). Perceptual deficits remain unclear, however, due in part to the limited behavioral capacity of existing rodent models to discriminate complex sounds. The budgerigar is an avian vocal learner with human-like behavioral sensitivity to many simple and complex sounds and the capacity to mimic speech. Previous studies in this species show that intracochlear kainic-acid infusion reduces wave 1 of the auditory brainstem response by 40-70%, consistent with substantial excitotoxic auditory-nerve damage. The present study used operant-conditioning procedures in trained budgerigars to quantify kainic-acid effects on tone detection across frequency (0.25-8 kHz; the audiogram) and as a function of duration (20-160 ms; temporal integration). Tone thresholds in control animals were lowest from 1 to 4 kHz and decreased with increasing duration as in previous studies of the budgerigar. Behavioral results in kainic-acid-exposed animals were as sensitive as in controls, suggesting preservation of the audiogram and temporal integration despite auditory-nerve loss associated with up to 70% wave 1 reduction. Distortion-product otoacoustic emissions were also preserved in kainic-acid exposed animals, consistent with normal hair-cell function. These results highlight considerable perceptual resistance of tone-detection performance with selective auditory-nerve loss. Future behavioral studies in budgerigars with auditory-nerve damage can use complex speech-like stimuli to help clarify aspects of auditory perception impacted by this common cochlear pathology.

Persistent Auditory Nerve Damage Following Kainic Acid Excitotoxicity in the Budgerigar (Melopsittacus undulatus).

Permanent loss of auditory nerve (AN) fibers occurs with increasing age and sound overexposure, sometimes without hair cell damage or associated audiometric threshold elevation. Rodent studies suggest effects of AN damage on central processing and behavior, but these species have limited capacity to discriminate low-frequency speech-like sounds. Here, we introduce a new animal model of AN damage in an avian communication specialist, the budgerigar (Melopsittacus undulatus). The budgerigar is a vocal learner and speech mimic with sensitive low-frequency hearing and human-like behavioral sensitivity to many complex signals including speech components. Excitotoxic AN damage was induced through bilateral cochlear infusions of kainic acid (KA). Acute KA effects on cochlear function were assessed using AN compound action potentials (CAPs) and hair cell cochlear microphonics (CMs). Long-term KA effects were assessed using auditory brainstem response (ABR) measurements for up to 31 weeks post-KA exposure. KA infusion immediately abolished AN CAPs while having mild impact on the CM. ABR wave I, the far-field AN response, showed a pronounced 40-75 % amplitude reduction at moderate-to-high sound levels that persisted for the duration of the study. In contrast, wave I latency and the amplitude of wave V were nearly unaffected by KA, and waves II-IV were less reduced than wave I. ABR thresholds, calculated based on complete response waveforms, showed no impairment following KA. These results demonstrate that KA exposure in the budgerigar causes irreversible AN damage, most likely through excitotoxic injury to afferent fibers or synapses as in other species, while sparing ABR thresholds. Normal wave V amplitude, assumed to originate centrally, may persist through compensatory mechanisms that restore central response amplitude by downregulating inhibition. Future studies in this new animal model of AN damage can explore effects of this neural lesion, in isolation from hair cell trauma and threshold elevation, on central processing and perception of complex sounds.

Formant-frequency discrimination of synthesized vowels in budgerigars (Melopsittacus undulatus) and humans.

Vowels are complex sounds with four to five spectral peaks known as formants. The frequencies of the two lowest formants, F1and F2, are sufficient for vowel discrimination. Behavioral studies show that many birds and mammals can discriminate vowels. However, few studies have quantified thresholds for formant-frequency discrimination. The present study examined formant-frequency discrimination in budgerigars (Melopsittacus undulatus) and humans using stimuli with one or two formants and a constant fundamental frequency of 200 Hz. Stimuli had spectral envelopes similar to natural speech and were presented with random level variation. Thresholds were estimated for frequency discrimination of F1, F2, and simultaneous F1 and F2 changes. The same two-down, one-up tracking procedure and single-interval, two-alternative task were used for both species. Formant-frequency discrimination thresholds were as sensitive in budgerigars as in humans and followed the same patterns across all conditions. Thresholds expressed as percent frequency difference were higher for F1 than for F2, and were unchanged between stimuli with one or two formants. Thresholds for simultaneous F1 and F2 changes indicated that discrimination was based on combined information from both formant regions. Results were consistent with previous human studies and show that budgerigars provide an exceptionally sensitive animal model of vowel feature discrimination.

Midbrain Synchrony to Envelope Structure Supports Behavioral Sensitivity to Single-Formant Vowel-Like Sounds in Noise.

Vowels make a strong contribution to speech perception under natural conditions. Vowels are encoded in the auditory nerve primarily through neural synchrony to temporal fine structure and to envelope fluctuations rather than through average discharge rate. Neural synchrony is thought to contribute less to vowel coding in central auditory nuclei, consistent with more limited synchronization to fine structure and the emergence of average-rate coding of envelope fluctuations. However, this hypothesis is largely unexplored, especially in background noise. The present study examined coding mechanisms at the level of the midbrain that support behavioral sensitivity to simple vowel-like sounds using neurophysiological recordings and matched behavioral experiments in the budgerigar. Stimuli were harmonic tone complexes with energy concentrated at one spectral peak, or formant frequency, presented in quiet and in noise. Behavioral thresholds for formant-frequency discrimination decreased with increasing amplitude of stimulus envelope fluctuations, increased in noise, and were similar between budgerigars and humans. Multiunit recordings in awake birds showed that the midbrain encodes vowel-like sounds both through response synchrony to envelope structure and through average rate. Whereas neural discrimination thresholds based on either coding scheme were sufficient to support behavioral thresholds in quiet, only synchrony-based neural thresholds could account for behavioral thresholds in background noise. These results reveal an incomplete transformation to average-rate coding of vowel-like sounds in the midbrain. Model simulations suggest that this transformation emerges due to modulation tuning, which is shared between birds and mammals. Furthermore, the results underscore the behavioral relevance of envelope synchrony in the midbrain for detection of small differences in vowel formant frequency under real-world listening conditions.

Neural correlates of behavioral amplitude modulation sensitivity in the budgerigar midbrain.

Amplitude modulation (AM) is a crucial feature of many communication signals, including speech. Whereas average discharge rates in the auditory midbrain correlate with behavioral AM sensitivity in rabbits, the neural bases of AM sensitivity in species with human-like behavioral acuity are unexplored. Here, we used parallel behavioral and neurophysiological experiments to explore the neural (midbrain) bases of AM perception in an avian speech mimic, the budgerigar (Melopsittacus undulatus). Behavioral AM sensitivity was quantified using operant conditioning procedures. Neural AM sensitivity was studied using chronically implanted microelectrodes in awake, unrestrained birds. Average discharge rates of multiunit recording sites in the budgerigar midbrain were insufficient to explain behavioral sensitivity to modulation frequencies <100 Hz for both tone- and noise-carrier stimuli, even with optimal pooling of information across recording sites. Neural envelope synchrony, in contrast, could explain behavioral performance for both carrier types across the full range of modulation frequencies studied (16-512 Hz). The results suggest that envelope synchrony in the budgerigar midbrain may underlie behavioral sensitivity to AM. Behavioral AM sensitivity based on synchrony in the budgerigar, which contrasts with rate-correlated behavioral performance in rabbits, raises the possibility that envelope synchrony, rather than average discharge rate, might also underlie AM perception in other species with sensitive AM detection abilities, including humans. These results highlight the importance of synchrony coding of envelope structure in the inferior colliculus. Furthermore, they underscore potential benefits of devices (e.g., midbrain implants) that evoke robust neural synchrony.

Near-field discrimination of sound source distance in the rabbit.

The acoustical cues and physiological processing mechanisms underlying the perception of the distance of sound sources are not well understood. To understand the relation between physiology and behavior, a first step is to use an animal model to study distance sensitivity. The goal of these experiments was to establish the capacity of the Dutch-belted rabbit to discriminate between sound sources at two distances. Trains of noise bursts were presented from speakers that were located either directly in front of the rabbit or at a 45 ° angle in azimuth. The reference speaker was positioned at distances of 20, 40, and 60 cm from the subject, and the more distant test speaker was systematically moved to determine the smallest difference in distance that could be reliably discriminated by the subject. Noise stimuli had one of three bandwidths: wideband (0.1-10 kHz), low-pass (0.1-3 kHz), or high-pass (3-10 kHz). The mean stimulus level was 60 dB sound pressure level (SPL) at the location of the rabbit's head, and the level was roved over a 12-dB range from trial to trial to reduce the availability of level cues. An operant one-interval two-alternative non-forced choice task was used, with a blocked two-down-one-up tracking procedure to determine the distance discriminability. Rabbits were consistently able to discriminate two distances when they were sufficiently separated. Sensitivity was better when the reference distance was 60 cm at either azimuth (distance ratio = 1.5) and was worse when the reference distance was 20 cm (distance ratio = 2.4 at 0 ° and 1.75 at 45 °).

Suboptimal use of neural information in a mammalian auditory system.

Establishing neural determinants of psychophysical performance requires both behavioral and neurophysiological metrics amenable to correlative analyses. It is often assumed that organisms use neural information optimally, such that any information available in a neural code that could improve behavioral performance is used. Studies have shown that detection of amplitude-modulated (AM) auditory tones by humans is correlated to neural synchrony thresholds, as recorded in rabbit at the level of the inferior colliculus, the first level of the ascending auditory pathway where neurons are tuned to AM stimuli. Behavioral thresholds in rabbit, however, are ∼10 dB higher (i.e., 3 times less sensitive) than in humans, and are better correlated to rate-based than temporal coding schemes in the auditory midbrain. The behavioral and physiological results shown here illustrate an unexpected, suboptimal utilization of available neural information that could provide new insights into the mechanisms that link neuronal function to behavior.

Detection thresholds for amplitude modulations of tones in budgerigar, rabbit, and human.

Envelope fluctuations of complex sounds carry information that is -essential for many types of discrimination and for detection in noise. To study the neural representation of envelope information and mechanisms for processing of this temporal aspect of sounds, it is useful to identify an animal model that can -sensitively detect amplitude modulations (AM). Low modulation frequencies, which dominate speech sounds, are of particular interest. Yet, most animal -models studied previously are relatively insensitive to AM at low modulation -frequencies. Rabbits have high thresholds for low-frequency modulations, -especially for tone carriers. Rhesus macaques are less sensitive than humans to low-frequency -modulations of wideband noise (O'Conner et al. Hear Res 277, 37-43, 2011). Rats and -chinchilla also have higher thresholds than humans for amplitude -modulations of noise (Kelly et al. J Comp Psychol 120, 98-105, 2006; Henderson et al. J Acoust Soc Am 75, -1177-1183, 1984). In contrast, the budgerigar has thresholds for AM detection of wideband noise similar to those of human listeners at low -modulation frequencies (Dooling and Searcy. Percept Psychophys 46, 65-71, 1981). A -one-interval, two-alternative operant conditioning procedure was used to estimate AM -detection thresholds for 4-kHz tone carriers at low modulation -frequencies (4-256 Hz). Budgerigar thresholds are comparable to those of human subjects in a comparable task. Implications of these comparative results for temporal coding of complex sounds are discussed. Comparative results for masked AM detection are also presented.

Sound-localization ability of the Mongolian gerbil (Meriones unguiculatus) in a task with a simplified response map.

The characterization of ability in behavioral sound-localization tasks is an important aspect of understanding how the brain encodes and processes sound location information. In a few species, both physiological and behavioral results related to sound localization are available. In the Mongolian gerbil, physiological sensitivity to interaural time differences in the auditory brainstem is comparable to that reported in other species; however, the gerbil has been reported to have relatively poor behavioral localization performance as compared with several other species. In this study, the behavioral performance of the gerbil for sound localization was re-examined using a task that involved a simpler response map than in previously published studies. In the current task, the animal directly approached the speaker on each trial, thus the response map was simpler than the 90°-right vs. 90°-left response required in previous studies of localization and source discrimination. Although the general performance across a group of animals was more consistent in the task with the simpler response map, the sound-localization ability replicated that previously reported. These results are consistent with the previous reports that sound-localization performance in gerbil is poor with respect to other species that have comparable neural sensitivity to interaural cues.

Detection of tones in reproducible noise maskers by rabbits and comparison to detection by humans.

Processing mechanisms used for detection of tones in noise can be revealed by using reproducible noise maskers and analyzing the pattern of results across masker waveforms. This study reports detection of a 500-Hz tone in broadband reproducible noise by rabbits using a set of masker waveforms for which human results are available. An appetitive-reinforcement, operant-conditioning procedure with bias control was used. Both fixed-level and roving-level noises were used to explore the utility of energy-related cues for detection. An energy-based detection model was able to partially explain the fixed-level results across reproducible noise waveforms for both rabbit and human. A multiple-channel energy model was able to explain fixed-level results, as well as the robust performance observed with roving-level noises. Further analysis using the energy model indicated a difference between species: human detection was influenced most by the noise spectrum surrounding the tone frequency, whereas rabbit detection was influenced most by the noise spectrum at frequencies above that of the tone. In addition, a temporal envelope-based model predicted detection by humans as well as the single-channel energy model did, but the envelope-based model failed to predict detection by rabbits. This result indicates that the contributions of energy and temporal cues to auditory processing differ across species. Overall, these findings suggest that caution must be used when evaluating neural encoding mechanisms in one species on the basis of behavioral results in another.