Kristina S. Abrams

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.

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.

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.

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 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.

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.

Amplitude modulation detection patterns of the Budgerigar

In determining the Amplitude Modulation Detection thresholds of the English Budgerigar, several stimuli were used. Amplitude modulation (AM) is the time variation of a sound signals amplitude2. Using tone and noise carrier waveforms, MATLAB computed both AM and un-modulated stimuli; these signals were played through a speaker for the English Budgerigar. The bird discriminated between the modulated and un-modulated tones. Results show that this species of bird shows similar detection patterns as human beings. Based on the correlations between the bird and human data, the auditory system of the Budgerigar may possibly serve as a model for the human auditory system.

Amplitude‐modulation detection in reproducible modulation maskers: Correlation between Behavioral and Physiological Responses.

The use of reproducible noise maskers in studies of detection has proven useful to extend our understanding of coding and processing of complex sounds. In an effort to reveal potential neural mechanisms for the detection of amplitude‐modulation (AM) in the presence of modulation maskers, tetrode recordings were made from inferior colliculus neurons of awake rabbits using reproducible stimuli. Both rabbit and human behavioral data have been collected for the same set of reproducible maskers. The target AM and maskers were applied to the envelope of a 5 kHz carrier signal. Neural responses were recorded to stimuli with the level of target AM slightly above masked threshold for both rabbit and human. Neural detection thresholds were estimated based on average discharge rate and several temporal metrics, such as synchrony to the target AM, temporal reliability, and rapid fluctuation in the peri‐stimulus time histogram (PSTH) of responses. The hit and false‐alarm rates for neural detection of AM were estimated...

Noise localization ability in the Mongolian gerbil (Meriones unguiculatus)

Understanding localization ability is essential for comparison to physiological studies of binaural neurons. Heffner and Heffner [Beh. Neuro. 102, 422 (1998)] reported relatively poor ability of the gerbil to localize a 100 ms noise burst (approximately 75% correct at 27° separation.) Their experimental setup required the gerbil to enter an observing response compartment, initiating a noise burst from one of two speakers separated by the test angle. The animal was required to respond by entering a reporting compartment, positioned 90° to the right or left, regardless of speaker location. This required mapping from speaker location to response location. In this study, response mapping was avoided in an effort to improve performance. After an observing response (jumping on a platform in the center of a circular cage), the animal responded by moving directly towards the active speaker. The results of this study were consistent with those of Heffner and Heffner at small angles of separation. [For 180° separat...

Dependence of detection threshold estimates in rabbit on method of constant stimulus parameters

The goal of this study was to estimate behavioral detection thresholds in quiet and noise for subsequent physiological studies of responses to near‐threshold stimuli. The difficulty in measuring detection thresholds is maintaining stimulus control of behavior over schedule control. Tracking paradigms are efficient, but the large proportion of trials below threshold weakens stimulus control. The Method of Constant Stimuli controls the proportion of trials below, near, and above the SPL for a given percent correct. Here, percentages of trials at different SPLs and zero intensity catch trials were varied to determine proportions that yielded satisfactory stimulus control by a 500‐Hz tone in quiet. Trials were initiated by nose‐poke observing responses; a nose‐poke reporting response within a 3‐s window after tone onset resulted in food reinforcement. Reporting responses in the absence of tones resulted in timeouts. A metric for stimulus control was the ratio of the number of correct detections to the number ...