Species-specific Vocalizations Research Articles

Songbirds tradeoff auditory frequency resolution and temporal resolution

Physical tradeoffs may in some cases constrain the evolution of sensory systems. The peripheral auditory system, for example, performs a spectral decomposition of sound that should result in a tradeoff between frequency resolution and temporal resolution. We assessed temporal resolution in three songbird species using auditory brainstem responses to paired click stimuli. Temporal resolution was greater in house sparrows (Passer domesticus) than Carolina chickadees (Poecile carolinensis) and white-breasted nuthatches (Sitta carolinensis), as predicted based on previous observations of broader auditory filters (lower frequency resolution) in house sparrows. Furthermore, within chickadees, individuals with broader auditory filters had greater temporal resolution. In contrast to predictions however, temporal resolution was similar between chickadees and nuthatches despite broader auditory filters in chickadees. These results and the results of a model simulation exploring the effect of broadened auditory filter bandwidth on temporal resolution in the auditory periphery strongly suggest that frequency resolution constrains temporal resolution in songbirds. Furthermore, our results suggest that songbirds have greater temporal resolution than some mammals, in agreement with recent behavioral studies. Species differences in temporal resolution may reflect adaptations for efficient processing of species-specific vocalizations, while individual differences within species may reflect experience-based developmental plasticity or hormonal effects.

The Vocal Repertoire of Two Sympatric Species of Nectar-Feeding Bats (Glossophaga soricinaandG. commissarisi)

We recorded social vocalizations from two sympatric species of glossophagine bats, Glossophaga soricina and G. commissarisi, using habituated captive groups that were housed in separate flight cages. Whenever possible, the species-specific vocalization types were described in the light of the social context in which they were produced. Several vocalization types within each species’ repertoire had remarkable similarities to vocalization types in the other species’ repertoire. Out of these, four vocalization types with interspecific acoustic similarities (approach pulses, distress calls, aggressive trills, and alert calls) were used in similar behavioral contexts in both species. Approach pulses were produced whenever a bat was flying towards an already occupied roost. Distress calls were uttered whenever a bat was attacked by conspecifics or restrained by the observer, whereas aggressive trills were produced during aggressive encounters prior to physical contact. Alert calls were uttered when bats were disturbed or when several individuals were circling the same location. The interspecific similarity of both the social context and the acoustic structure of vocalization types suggest that the potential for interspecific communication is high in G. soricina and G. commissarisi.

Predicting stimulus-locked single unit spiking from cortical local field potentials

The rapidly increasing use of the local field potential (LFP) has motivated research to better understand its relation to the gold standard of neural activity, single unit (SU) spiking. We addressed this in an in vivo, awake, restrained mouse auditory cortical electrophysiology preparation by asking whether the LFP could actually be used to predict stimulus-evoked SU spiking. Implementing a Bayesian algorithm to predict the likelihood of spiking on a trial by trial basis from different representations of the despiked LFP signal, we were able to predict, with high quality and fine temporal resolution (2 ms), the time course of a SU's excitatory or inhibitory firing rate response to natural species-specific vocalizations. Our best predictions were achieved by representing the LFP by its wide-band Hilbert phase signal, and approximating the statistical structure of this signal at different time points as independent. Our results show that each SU's action potential has a unique relationship with the LFP that can be reliably used to predict the occurrence of spikes. This "signature" interaction can reflect both pre- and post-spike neural activity that is intrinsic to the local circuit rather than just dictated by the stimulus. Finally, the time course of this "signature" may be most faithful when the full bandwidth of the LFP, rather than specific narrow-band components, is used for representation.

Hemispheric differences in processing of vocalizations depend on early experience

An intriguing phenomenon in the neurobiology of language is lateralization: the dominant role of one hemisphere in a particular function. Lateralization is not exclusive to language because lateral differences are observed in other sensory modalities, behaviors, and animal species. Despite much scientific attention, the function of lateralization, its possible dependence on experience, and the functional implications of such dependence have yet to be clearly determined. We have explored the role of early experience in the development of lateralized sensory processing in the brain, using the songbird model of vocal learning. By controlling exposure to natural vocalizations (through isolation, song tutoring, and muting), we manipulated the postnatal auditory environment of developing zebra finches, and then assessed effects on hemispheric specialization for communication sounds in adulthood. Using bilateral multielectrode recordings from a forebrain auditory area known to selectively process species-specific vocalizations, we found that auditory responses to species-typical songs and long calls, in both male and female birds, were stronger in the right hemisphere than in the left, and that right-side responses adapted more rapidly to stimulus repetition. We describe specific instances, particularly in males, where these lateral differences show an influence of auditory experience with song and/or the bird's own voice during development.

Activation of frontal neocortical areas by vocal production in marmosets.

Primates often rely on vocal communication to mediate social interactions. Although much is known about the acoustic structure of primate vocalizations and the social context in which they are usually uttered, our knowledge about the neocortical control of audio–vocal interactions in primates is still incipient, being mostly derived from lesion studies in squirrel monkeys and macaques. To map the neocortical areas related to vocal control in a New World primate species, the common marmoset, we employed a method previously used with success in other vertebrate species: Analysis of the expression of the immediate early gene Egr-1 in freely behaving animals. The neocortical distribution of Egr-1 immunoreactive cells in three marmosets that were exposed to the playback of conspecific vocalizations and vocalized spontaneously (H/V group) was compared to data from three other marmosets that also heard the playback but did not vocalize (H/n group). The anterior cingulate cortex, the dorsomedial prefrontal cortex and the ventrolateral prefrontal cortex presented a higher number of Egr-1 immunoreactive cells in the H/V group than in H/n animals. Our results provide direct evidence that the ventrolateral prefrontal cortex, the region that comprises Broca's area in humans and has been associated with auditory processing of species-specific vocalizations and orofacial control in macaques, is engaged during vocal output in marmosets. Altogether, our results support the notion that the network of neocortical areas related to vocal communication in marmosets is quite similar to that of Old world primates. The vocal production role played by these areas and their importance for the evolution of speech in primates are discussed.

Rhesus Monkeys' Valuation of Vocalizations during a Free-Choice Task

Adaptive behavior requires that animals integrate current and past information with their decision-making. One important type of information is auditory-communication signals (i.e., species-specific vocalizations). Here, we tested how rhesus monkeys incorporate the opportunity to listen to different species-specific vocalizations into their decision-making processes. In particular, we tested how monkeys value these vocalizations relative to the opportunity to get a juice reward. To test this hypothesis, monkeys chose one of two targets to get a varying juice reward; at one of those targets, in addition to the juice reward, a vocalization was presented. By titrating the juice amounts at the two targets, we quantified the relationship between the monkeys' juice choices relative to the opportunity to listen to a vocalization. We found that, rhesus were not willing to give up a large juice reward to listen to vocalizations indicating that, relative to a juice reward, listening to vocalizations has a low value.

Primate auditory recognition memory performance varies with sound type

Neural correlates of auditory processing, including for species-specific vocalizations that convey biological and ethological significance (e.g., social status, kinship, environment), have been identified in a wide variety of areas including the temporal and frontal cortices. However, few studies elucidate how non-human primates interact with these vocalization signals when they are challenged by tasks requiring auditory discrimination, recognition and/or memory. The present study employs a delayed matching-to-sample task with auditory stimuli to examine auditory memory performance of rhesus macaques ( Macaca mulatta), wherein two sounds are determined to be the same or different. Rhesus macaques seem to have relatively poor short-term memory with auditory stimuli, and we examine if particular sound types are more favorable for memory performance. Experiment 1 suggests memory performance with vocalization sound types (particularly monkey), are significantly better than when using non-vocalization sound types, and male monkeys outperform female monkeys overall. Experiment 2, controlling for number of sound exemplars and presentation pairings across types, replicates Experiment 1, demonstrating better performance or decreased response latencies, depending on trial type, to species-specific monkey vocalizations. The findings cannot be explained by acoustic differences between monkey vocalizations and the other sound types, suggesting the biological, and/or ethological meaning of these sounds are more effective for auditory memory.

The primate cortical auditory system and neural representation of conspecific vocalizations.

Over the past decade, renewed interest in the auditory system has resulted in a surge of anatomical and physiological research in the primate auditory cortex and its targets. Anatomical studies have delineated multiple areas in and around primary auditory cortex and demonstrated connectivity among these areas, as well as between these areas and the rest of the cortex, including prefrontal cortex. Physiological recordings of auditory neurons have found that species-specific vocalizations are useful in probing the selectivity and potential functions of acoustic neurons. A number of cortical regions contain neurons that are robustly responsive to vocalizations, and some auditory responsive neurons show more selectivity for vocalizations than for other complex sounds. Demonstration of selectivity for vocalizations has prompted the question of which features are encoded by higher-order auditory neurons. Results based on detailed studies of the structure of these vocalizations, as well as the tuning and information-coding properties of neurons sensitive to these vocalizations, have begun to provide answers to this question. In future studies, these and other methods may help to define the way in which cells, ensembles, and brain regions process communication sounds. Moreover, the discovery that several nonprimary auditory cortical regions may be multisensory and responsive to vocalizations with corresponding facial gestures may change the way in which we view the processing of communication information by the auditory system.

Selectivity for Conspecific Vocalizations within the Primate Insular Cortex

Successful processing of species-specific vocalizations is important for effective social interaction—not only for humans but for all vocal animals. However, until recently, little was known of the neural mechanisms involved in processing vocal information. A functional imaging study by [Belin et

Discrimination of auditory gratings in birds

Auditory gratings (also called auditory ripples) are a family of complex, broadband sounds with sinusoidally modulated logarithmic amplitudes and a drifting spectral envelope. These stimuli have been studied both physiologically in mammals and psychophysically in humans. Auditory gratings share spectro-temporal properties with many natural sounds, including species-specific vocalizations and the formant transitions of human speech. We successfully trained zebra finches and budgerigars, using operant conditioning methods, to discriminate between flat-spectrum broadband noise and noises with ripple spectra of different densities that moved up or down in frequency at various rates. Results show that discrimination thresholds (minimum modulation depth) increased as a function of increasing grating periodicity and density across all species. Results also show that discrimination in the two species of birds was better at those grating periodicities and densities that are prominent in their species-specific vocalizations. Budgerigars were generally more sensitive than both zebra finches and humans. Both bird species showed greater sensitivity to descending auditory gratings, which mirrors the main direction in their vocalizations. Humans, on the other hand, showed no directional preference even though speech is somewhat downward directional. Overall, our results are suggestive of both common strategies in the processing of complex sounds between birds and mammals and specialized, species-specific variations on that processing in birds.

Over-representation of species-specific vocalizations in the awake mouse inferior colliculus

Social vocalizations are particularly important stimuli in an animal's auditory environment. Because of their importance, vocalizations should be strongly represented in auditory pathways. Mice commonly emit ultrasonic vocalizations with spectral content between 45 and 100 kHz. However, there is limited representation of these ultra-high frequencies (particularly those greater than 60 kHz) throughout the ascending auditory system. Here, we show that neurons in the inferior colliculus (IC) of mice respond strongly to conspecific vocalizations even though the energy in the vocalizations is above the neurons' frequency tuning curves. This results in an over-representation of species-specific vocalizations in the IC. In addition, neurons in mouse IC show selectivity among different vocalizations. Many vocalization-responsive neurons do not respond to the individual ultrasonic frequencies contained within the vocalizations, but they do respond to combinations of ultrasonic tones if the difference between the tones is within the excitatory frequency tuning curve. The combinations of tones that elicit responses are the quadratic and/or cubic intermodulation distortion components that are generated by the cochlea. Thus, the intermodulation distortions in the cochlea may provide a previously overlooked mechanism for auditory processing of complex stimuli such as vocalizations. The implication of these findings is that nonlinear interactions of frequencies, possibly caused by distortions in the system, may be used to enhance the sensitivity to behaviorally important stimuli.

Selective Increase in Representations of Sounds Repeated at an Ethological Rate

Exposure to sounds during early development causes enlarged cortical representations of those sounds, leading to the commonly held view that the size of stimulus representations increases with stimulus exposure. However, representing stimuli based solely on their prevalence may be inefficient, because many frequent environmental sounds are behaviorally irrelevant. Here, we show that cortical plasticity depends not only on exposure time but also on the temporal modulation rate of the stimulus set. We examined cortical plasticity induced by early exposure to 7 kHz tone pips repeated at a slow (2 Hz), fast (15 Hz), or ethological (6 Hz) rate. Certain rat calls are modulated near 6 Hz. We found that spectral representation of 7 kHz increased only in the ethological-rate-reared animals, whereas improved entrainment of cortical neurons was seen in animals reared in the slow- and fast-rate condition. This temporal rate dependence of spectral plasticity may serve as a filtering mechanism to selectively enlarge representations of species-specific vocalizations. Furthermore, our results indicate that spectral and temporal plasticity can be separately engaged depending on the statistical properties of the input stimuli.

A Spike-Timing Code for Discriminating Conspecific Vocalizations in the Thalamocortical System of Anesthetized and Awake Guinea Pigs

Understanding how communication sounds are processed and encoded in the central auditory system is critical to understanding the neural bases of acoustic communication. Here, we examined neuronal representations of species-specific vocalizations, which are communication sounds that many species rely on for survival and social interaction. In some species, the evoked responses of auditory cortex neurons are stronger in response to natural conspecific vocalizations than to their time-reversed, spectrally identical, counterparts. We applied information theory-based analyses to single-unit spike trains collected in the auditory cortex (n = 139) and auditory thalamus (n = 135) of anesthetized animals as well as in the auditory cortex (n = 119) of awake guinea pigs during presentation of four conspecific vocalizations. Few thalamic and cortical cells (<10%) displayed a firing rate preference for the natural version of these vocalizations. In contrast, when the information transmitted by the spike trains was quantified with a temporal precision of 10-50 ms, many cells (>75%) displayed a significant amount of information (i.e., >2SD above chance levels), especially in the awake condition. The computed correlation index between spike trains (R(corr), defined by Schreiber et al., 2003) indicated similar spike-timing reliability for both the natural and time-reversed versions of each vocalization, but higher reliability for awake animals compared with anesthetized animals. Based on temporal discharge patterns, even cells that were only weakly responsive to vocalizations displayed a significant level of information. These findings emphasize the importance of temporal discharge patterns as a coding mechanism for natural communication sounds, particularly in awake animals.

Can free-ranging rhesus monkeys (Macaca mulatta) extract artificially created rules comprised of natural vocalizations?

Though nonhuman animals lack anything like a set of grammatical structures in their natural vocalizations, studies now suggest that at least some animals can extract patterns from a structured input that appear abstract and rule-like. The authors continue this line of research by adding three new methodological contributions, specifically, tests of (1) a free-ranging animal population (as opposed to captive laboratory subjects), (2) a new taxonomic group (i.e., Old World monkeys: rhesus macaques, Macaca mulatta), and (3), the presentation of artificially sequenced strings of species-specific vocalizations (as opposed to artificial symbols or speech stimuli). Specifically, the authors created artificial strings of rhesus vocalizations in the pattern notated as AAB (i.e., two identical calls [AA] followed by a different one [B]) or ABB. Following habituation to AAB strings, rhesus monkeys showed significantly more orienting responses to novel ABB strings than to novel AAB strings. Further, following habituation to an ABB pattern, rhesus responded more in test trials to AAB than ABB. These results, combined with other parallel studies, suggest that animals can extract an identity relationship from an artificial sequence of sounds, and can do so even though the tokens are species-specific vocalizations that are never produced in this sequence.

Facilitatory Mechanisms Underlying Selectivity for the Direction and Rate of Frequency Modulated Sweeps in the Auditory Cortex

Neurons selective for frequency modulated (FM) sweeps are common in auditory systems across different vertebrate groups and may underlie representation of species-specific vocalizations. Studies on mechanisms of FM sweep selectivity have primarily focused on sideband inhibition. Here, we present the first evidence for facilitatory mechanisms of FM sweep selectivity. Facilitatory interactions were found in 46 of 264 (17%) neurons tuned in the echolocation range (25-60 kHz) in the auditory cortex of the pallid bat. These neurons respond poorly to individual tones but are facilitated by combinations of tones with specific spectral and temporal intervals. Facilitation neurons show remarkable sensitivity to sub-millisecond differences in time delays between the two tones. Interestingly, the range of delays eliciting facilitation is not fixed but varies systematically with frequency difference between the two tones. Properties of facilitation strongly predict selectivity for the direction and rate of FM sweeps. Together with previous studies, there appear to be at least three mechanisms underlying FM rate and direction selectivity: sideband inhibition, duration tuning, and facilitation. Interestingly, similar mechanisms underlie direction and velocity tuning in the visual system, suggesting the evolution of similar computations across sensory systems to process dynamic sensory stimuli.

Coevolution of auditory sensitivity and temporal resolution with acoustic signal space in three songbirds

Coevolution between senders and receivers is expected to produce a close match between signal design and sensory biology. We evaluated this hypothesis in songbirds by comparing aspects of acoustic signal space with the frequency range of auditory sensitivity and temporal resolution in tufted titmice, Baeolophus bicolor ; house sparrows, Passer domesticus ; and white-breasted nuthatches, Sitta carolinensis . Auditory measurements were made electrophysiologically from the scalp using two classes of auditory-evoked potentials: the auditory brain-stem response (ABR) and the envelope-following response (EFR). ABRs to tone-burst stimuli indicated maximum sensitivity from 2.2 to 3.2 kHz in all species, but 12–14 dB greater sensitivity in titmice than in sparrows and nuthatches at 6.4 kHz (the highest frequency tested). Modulation rate transfer functions based on EFRs to amplitude-modulated tones suggested greater temporal resolution in titmice and sparrows than in nuthatches. Conservation of the frequency range of maximum sensitivity across species resulted in a mismatch with the dominant frequency of song in sparrows. The mismatch may reflect auditory constraints coupled with selection for high-frequency song and relaxed selection for a close match between sender and receiver due to small territory size. Consistent with coevolution between senders and receivers, high-frequency sensitivity varied with the maximum frequency of species-specific vocalizations, whereas temporal resolution varied with the maximum rate of envelope periodicity. Enhanced high-frequency sensitivity of the titmouse may reflect a specialization for processing high-frequency communication signals such as alarm calls.

Visualizing vocal perception in the chimpanzee brain.

The study of nonhuman primate vocal-auditory behavior continues to provide novel insights into the origins of human language. However, data on the neural systems involved in the perception and processing of conspecific vocalizations in great apes are virtually absent in the scientific literature, yet are critical for understanding the evolution of language. Here we used positron emission tomography to examine the neurological mechanisms associated with the perception of species-specific vocalizations in chimpanzees. The data indicate right-lateralized activity in the chimpanzee posterior temporal lobe, including the planum temporale, in response to certain calls, but not others. In addition, important differences are apparent when these data are compared with those published previously from monkey species suggesting that there may be marked differences in the way chimpanzees and macaque monkeys perceive and process conspecific vocalizations. These results provide the first evidence of the neural correlates of auditory perception in chimpanzees and offer unprecedented information concerning the origins of hemispheric specialization in humans.

A voice region in the monkey brain

For vocal animals, recognizing species-specific vocalizations is important for survival and social interactions. In humans, a voice region has been identified that is sensitive to human voices and vocalizations. As this region also strongly responds to speech, it is unclear whether it is tightly associated with linguistic processing and is thus unique to humans. Using functional magnetic resonance imaging of macaque monkeys (Old World primates, Macaca mulatta) we discovered a high-level auditory region that prefers species-specific vocalizations over other vocalizations and sounds. This region not only showed sensitivity to the 'voice' of the species, but also to the vocal identify of conspecific individuals. The monkey voice region is located on the superior-temporal plane and belongs to an anterior auditory 'what' pathway. These results establish functional relationships with the human voice region and support the notion that, for different primate species, the anterior temporal regions of the brain are adapted for recognizing communication signals from conspecifics.

A voice region in the monkey brain

For vocal animals, recognizing species-specific vocalizations is important for survival and social interactions. In humans, a voice region has been identified that is sensitive to human voices and vocalizations. As this region also strongly responds to speech, it is unclear whether it is tightly associated with linguistic processing and is thus unique to humans. Using functional magnetic resonance imaging of macaque monkeys (Old World primates, Macaca mulatta) we discovered a high-level auditory region that prefers species-specific vocalizations over other vocalizations and sounds. This region not only showed sensitivity to the 'voice' of the species, but also to the vocal identify of conspecific individuals. The monkey voice region is located on the superior-temporal plane and belongs to an anterior auditory 'what' pathway. These results establish functional relationships with the human voice region and support the notion that, for different primate species, the anterior temporal regions of the brain are adapted for recognizing communication signals from conspecifics.

Coding of communication calls in the subcortical and cortical structures of the auditory system

The processing of species-specific communication signals in the auditory system represents an important aspect of animal behavior and is crucial for its social interactions, reproduction, and survival. In this article the neuronal mechanisms underlying the processing of communication signals in the higher centers of the auditory system--inferior colliculus (IC), medial geniculate body (MGB) and auditory cortex (AC)--are reviewed, with particular attention to the guinea pig. The selectivity of neuronal responses for individual calls in these auditory centers in the guinea pig is usually low--most neurons respond to calls as well as to artificial sounds; the coding of complex sounds in the central auditory nuclei is apparently based on the representation of temporal and spectral features of acoustical stimuli in neural networks. Neuronal response patterns in the IC reliably match the sound envelope for calls characterized by one or more short impulses, but do not exactly fit the envelope for long calls. Also, the main spectral peaks are represented by neuronal firing rates in the IC. In comparison to the IC, response patterns in the MGB and AC demonstrate a less precise representation of the sound envelope, especially in the case of longer calls. The spectral representation is worse in the case of low-frequency calls, but not in the case of broad-band calls. The emotional content of the call may influence neuronal responses in the auditory pathway, which can be demonstrated by stimulation with time-reversed calls or by measurements performed under different levels of anesthesia. The investigation of the principles of the neural coding of species-specific vocalizations offers some keys for understanding the neural mechanisms underlying human speech perception.