David B. Moody’s research while affiliated with Kresge Eye Institute and other places

Brief cochlear excitotoxicity produces temporary neural swelling and transient deficits in auditory sensitivity; however, the consequences of long-lasting excitotoxic insult have not been tested. Chronic intra-cochlear infusion of the glutamate agonist AMPA (a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid) resulted in functional deficits in the sound-evoked auditory brainstem response, as well as in behavioral measures of hearing. The electrophysiological deficits were similar to those observed following acute infusion of AMPA into the cochlea; however, the concentration-response curve was significantly shifted as a consequence of the slower infusion rate used with chronic cochlear administration. As observed following acute excitotoxic insult, complete functional recovery was evident within 7 days of discontinuing the AMPA infusion. Distortion product otoacoustic emissions were not affected by chronic AMPA infusion, suggesting that trauma to outer hair cells did not contribute to AMPA-induced deficits in acoustic sensitivity. Results from the current experiment address the permanence of deficits induced by chronic (14 day) excitotoxic insult as well as deficits in psychophysical detection of longer duration acoustic signals.

Studies of animal communication systems have been largely composed of comparisons with human language. Indeed, one of the most obvious reasons to study primate communication is to identify parallels between human and non-human primate signal production and use. With the exception of grunts, ¹ the signals used by human and non-human primate species tend to be acoustically different. These acoustic differences result from differences in vocal tract morphology and articulatory apparatuses (for reviews, see Snowden ² and Fitch and Hauser ³). Investigators have thus taken two distinctly different approaches to the study of primate communication skills. In one approach, primate communication abilities have been assessed by the extent to which they learn human communication systems, including speech, 4,5 sign language, ⁶⁻⁹ and arbitrary symbols. 10,11 This search for parallels with human language is a bias introduced by our familiarity with the syntax of human language and by the methods developed for analyzing human speech sounds. In this review, we will instead evaluate the production and perception of species-typical vocal signals by monkeys. We will focus on macaques because of the wealth of field and laboratory studies examining their vocalizations.

There is evidence that Japanese macaques (Macaca fuscata) are extremely sensitive to dynamic changes in the relative amplitudes of coo call harmonics during discrimination tests. To verify this evidence using more controlled stimulus configurations, the authors examined threshold sensitivity of macaque monkeys to amplitude increments added to the standard level of coo call harmonics. Psychophysical threshold determination methods paralleled those used previously to determine macaque sensitivity to amplitude increments added to vowel-like stimuli. Variation was detectable although thresholds were elevated relative to those obtained with vowel-like stimuli in another investigation (C. G. Le Prell, A. J. Niemiec, & D. B. Moody, 2001). This elevation was probably a function of natural amplitude modulation in the standard stimuli.

Gouzoules et al. (1984, Animal Behaviour,32, 182–193) presented evidence that semifree-ranging rhesus monkeys, Macaca mulatta, produce acoustically distinctive classes of scream vocalizations that carry different functional messages. To determine the perceptual validity of these vocal classes, we conducted psychophysical experiments on captive rhesus monkeys. We trained two monkeys to maintain contact with a metal response cylinder during presentation of nontarget stimuli, and to release the cylinder to report detection of target stimuli. For one subject, tonal screams served as nontarget stimuli and arched screams served as targets. These conditions were reversed for a second subject. Once natural exemplars were correctly discriminated, both subjects correctly generalized to synthetic targets. Variability in responses to nontarget stimuli, however, suggested that scream categories were not well defined following training. This result suggests that rhesus monkeys do not perceive categorical distinctions between arched and tonal screams, at least under the testing conditions implemented. Rather, our results provide evidence for a graded category. To explore which acoustic features are most important for classifying novel exemplars as tonal or arched screams, we ran several follow-up experiments with novel scream exemplars. Generalization trials suggested that variation in rate of frequency change, maximum frequency of the fundamental and harmonic structure may be important to the discrimination of screams.

Macaque monkeys, like humans, are more sensitive to differences in formant frequency than to differences in the frequency of pure tones (see Sinnott et al. (1987) J. Comp. Psychol. 94, 401–415; Pfingst (1993) J. Acoust. Soc. Am. 93, 2124–2129; Prosen et al. (1990) J. Acoust. Soc. Am. 88, 2152–2158; Sinnott et al. (1985) J. Acoust. Soc. Am. 78, 1977–1985; Sinnott and Kreiter (1991) J. Acoust. Soc. Am. 89, 2421–2429; for summary, see May et al. (1996) Aud. Neurosci. 3, 135–162). In the discrimination of formant frequency, it appears that the relevant cue for macaque monkeys is relative level differences of the component frequencies (Sommers et al. (1992) J. Acoust. Soc. Am. 91, 3499–3510). To further explore the result of Sommers et al., we trained macaque monkeys (Macaca fuscata) to report detection of a change in the spectral shape of multi-component harmonic complexes. Spectral shape changes were produced by the addition of intensity increments. When the amplitude spectrum of the comparison stimulus was modeled after the /ae/ vowel sound, thresholds for detecting a change from the comparison stimulus were lowest when intensity increments were added at spectral peaks. These results parallel previous data from human subjects, suggesting that both human and monkey subjects may process vowel spectra through simultaneous comparisons of component levels across the spectrum. When the subjects were asked to detect a change from a comparison stimulus with a flat amplitude spectrum, the subjects showed sensitivity that was relatively comparable to that of human subjects tested in other investigations (e.g. Zera et al. (1993) J. Acoust. Soc. Am. 93, 3431–3441). In additional experiments, neither increasing the dynamic range of the /ae/ spectrum nor dynamically varying the amplitude of the increment during the stimulus presentation reliably affected detection thresholds.

If temporal position of a frequency inflection is the most salient communication cue in Japanese macaque smooth early and smooth late high coos, then macaques should perceive coos differing only along the early-late dimension as belonging to different classes. The perceived similarity of synthetic coos and temporally reversed variants were evaluated, using multidimensional scaling of macaque discrimination latencies. Original calls and calls temporally reversed in the frequency domain could be discriminated if the peak was near a call endpoint but not if the frequency peak in the original call was near the coo midpoint. Perceived similarity of such calls was inversely related to the amount of frequency modulation. Temporal reversals of amplitude contours were also conducted. Although macaques are quite sensitive to amplitude increments, reversal of the relatively flat amplitude contours of these calls did not affect discrimination responses.

If temporal position of a frequency inflection is the most salient communication cue in Japanese macaque smooth early and smooth late high coos, then macaques should perceive coos differing only along the early–late dimension as belonging to different classes. The perceived similarity of synthetic coos and temporally reversed variants were evaluated, using multidimensional scaling of macaque discrimination latencies. Original calls and calls temporally reversed in the frequency domain could be discriminated if the peak was near a call endpoint but not if the frequency peak in the original call was near the coo midpoint. Perceived similarity of such calls was inversely related to the amount of frequency modulation. Temporal reversals of amplitude contours were also conducted. Although macaques are quite sensitive to amplitude increments, reversal of the relatively flat amplitude contours of these calls did not affect discrimination responses.

Research examining the discrimination of monaural phase change has suggested that temporal envelope shape, which varies with phase, may be an important cue. Much of that research employed stimuli consisting of three components, a center frequency (Fc), which is varied in phase, and an upper and lower sideband separated from the carrier by some frequency (delta F). As the phase of the center component is varied, both temporal envelope and temporal fine structure change. The present research explored the salience of both envelope and fine structure as cues in a phase discrimination task. Monkeys were trained to report detection of a change from a three-tone complex with 90 degrees starting phase for the center component to one in which the starting phase was smaller. In general, for the values of Fc tested, thresholds for phase change decreased as delta F increased. When tested with comparison stimuli that had a temporal envelope closely matched to that of the standard, but 0 degree starting phase, subjects had difficulty discriminating these stimuli from the standard for smaller delta F, but readily discriminated them at larger delta F values. These findings suggest that temporal envelope is a critical cue in discrimination of three-tone complexes on the basis of the starting phase of the center component at small values of delta F, but that other cues are used at larger delta F values.

Smooth early high (SEH) and smooth late high (SLH) coo calls differ in the temporal location of a frequency inflection and are generally used in different situations. Coo quality is also influenced by additional features, such as relative harmonic level, which may have communicative significance. The authors used multidimensional scaling to analyze the perceptual similarity of SEH and SLH coos. Neither the temporal position of the frequency inflection nor caller identity could explain the coo groupings. Only the temporal relationships of the relative harmonic levels consistently differed between stimulus clusters. Relative level manipulations were conducted on synthetic coo replicas, resulting in substantial stimulus space reorganization. Although temporal position of the frequency inflection may provide the basis for coo classification, the authors suggest that relative harmonic amplitude can also influence response properties.

Smooth early high (SEH) and smooth late high (SLH) coo calls differ in the temporal location of a frequency inflection and are generally used in different situations. Coo quality is also influenced by additional features, such as relative harmonic level, which may have communicative significance. The authors used multidimensional scaling to analyze the perceptual similarity of SEH and SLH coos. Neither the temporal position of the frequency inflection nor caller identity could explain the coo groupings. Only the temporal relationships of the relative harmonic levels consistently differed between stimulus clusters. Relative level manipulations were conducted on synthetic coo replicas, resulting in substantial stimulus space reorganization. Although temporal position of the frequency inflection may provide the basis for coo classification, the authors suggest that relative harmonic amplitude can also influence response properties.