A Comparison of Prairie Vole Audible and Ultrasonic Pup Calls and Attraction to Them by Adults of Each Sex

Rodent pups of many species emit both ultrasonic vocalizations (USVs) and calls spanning into a lower frequency range, audible to humans (AUDs), yet there has been little systematic comparison of these different call types, or analyses of how they might differ in signal function. Here the spectral and temporal characteristics of USV and AUD pup calls are described for the prairie vole (Microtus ochrogaster), a model used in studies of monogamous mating and biparental care, and a species with an unusually large functional and anatomical representation of auditory cortex. Findings provide a detailed description of each call type, including changes to a number of USV characteristics over pup development. Adult attraction to the playback of these two call types was tested in groups that differed in regards to sex and reproductive status. Separate groups included virgins as well as paired animals of each sex, tested at time points either prior to the birth of pups (associated with either mid or late gestation), or at postpartum time points (parents of 2-3 day olds and parents of 8-9 day olds). Adults were attracted to both USVs and AUDs, but group differences were found only in the attraction to USVs. Males were more attracted to USVs than females, and there were interactions of sex and reproductive status. Results suggest that pup vocal communication is quite sophisticated, and that USVs and AUDs may have different communicative functions. Terleph, T. A. (2011). Comparison of prairie vole audible and ultrasonic pup calls and attraction to them by adults of each sex . Behaviour, 148(11-13), 1275-1294

A Songbird Forebrain Area Potentially Involved in Auditory Discrimination and Memory Formation

Songbirds rely on auditory processing of natural communication signals for a number of social behaviors, including mate selection, individual recognition and the rare behavior of vocal learning - the ability to learn vocalizations through imitation of an adult model, rather than by instinct. Like mammals, songbirds possess a set of interconnected ascending and descending auditory brain pathways that process acoustic information and that are presumably involved in the perceptual processing of vocal communication signals. Most auditory areas studied to date are located in the caudomedial forebrain of the songbird and include the thalamo-recipient field L (subfields L1, L2 and L3), the caudomedial and caudolateral mesopallium (CMM and CLM, respectively) and the caudomedial nidopallium (NCM). This review focuses on NCM, an auditory area previously proposed to be analogous to parts of the primary auditory cortex in mammals. Stimulation of songbirds with auditory stimuli drives vigorous electrophysiological responses and the expression of several activity-regulated genes in NCM. Interestingly, NCM neurons are tuned to species-specifi c songs and undergo some forms of experience-dependent plasticity in-vivo. These activity-dependent changes may underlie long-term modifications in the functional performance of NCM and constitute a potential neural substrate for auditory discrimination. We end this review by discussing evidence that suggests that NCM may be a site of auditory memory formation and/or storage

Neural Coding of Temporal Information and Its Topography in the Auditory Cortex

The article discusses a study that focused on neural coding of temporal information and topography in the auditory cortex. The quest for a thorough understanding how highly complex stimuli are encoded poses a significant challenge for auditory neurosciences, such as human speech and animal vocal signals. The characteristics of cortical neurons have been attributed to the coding of temporal stimulus which features precise spike timing in the coding and firing rate of repetition sounds

Neural Correlates of Auditory Processing, Learning and Memory Formation in Songbirds

Songbirds have emerged as powerful experimental models for the study of auditory processing of complex natural communication signals. Intact hearing is necessary for several behaviors in developing and adult animals including vocal learning, territorial defense, mate selection and individual recognition. These behaviors are thought to require the processing, discrimination and memorization of songs. Although much is known about the brain circuits that participate in sensorimotor (auditory-vocal) integration, especially the “songcontrol” system, less is known about the anatomical and functional organization of central auditory pathways. Here we discuss findings associated with a telencephalic auditory area known as the caudomedial nidopallium (NCM). NCM has attracted significant interest as it exhibits functional properties that may support higher order auditory functions such as stimulus discrimination and the formation of auditory memories. NCM neurons are vigorously driven by auditory stimuli. Interestingly, these responses are selective to conspecific, relative to heterospecific songs and artificial stimuli. In addition, forms of experience-dependent plasticity occur in NCM and are song-specific. Finally, recent experiments employing highthroughput quantitative proteomics suggest that complex protein regulatory pathways are engaged in NCM as a result of auditory experience. These molecular cascades are likely central to experience-associated plasticity of NCM circuitry and may be part of a network of calcium-driven molecular events that support the formation of auditory memory traces

Response Properties of the Auditory Telencephalon in Songbirds Change with Recent Experience and Season

The caudomedial nidopallium (NCM) is a telencephalic auditory area that is selectively activated by conspecific vocalizations in zebra finches and canaries. We recently demonstrated that temporal and spectral dynamics of auditory tuning in NCM differ between these species [1]. In order to determine whether these differences reflect recent experience, we exposed separate groups of each species and sex to different housing conditions. Adult birds were housed either in an aviary with conspecifics (NORM), with heterospecifics (canary subjects in a zebra finch aviary, and vice versa: (CROSS)), or in isolation (ISO) for 9 days prior to testing. We then recorded extracellular multi-unit electrophysiological responses to simple pure tone stimuli (250–5000 Hz) in awake birds from each group and analyzed auditory tuning width using methods from our earlier studies. Relative to NORM birds, tuning was narrower in CROSS birds, and wider in ISO birds. The trend was greater in canaries, especially females. The date of recording was also included as a covariate in ANCOVAs that analyzed a larger set of the canary data, including data from birds tested outside of the breeding season, and treated housing condition and sex as independent variables. These tests show that tuning width was narrower early in the year and broader later. This effect was most pronounced in CROSS males. The degree of the short-term neural plasticity described here differs across sexes and species, and may reflect differences in NCM's anatomical and functional organization related to species differences in song characteristics, adult plasticity and/or social factors. More generally, NCM tuning is labile and may be modulated by recent experience to reflect the auditory processing required for behavioral adaptation to the current acoustic, social or seasonal context

Bilateral Multi-Electrode Neurophysiological Recordings Coupled to Local Pharmacology in Awake Songbirds

Here we describe a protocol for bilateral multielectrode neurophysiological recordings during intracerebral pharmacological manipulations in awake songbirds. This protocol encompasses fitting adult animals with head-posts and recording chambers, and acclimating them to periods of restraint. The adaptation period is followed by bilateral penetrations of multiple electrodes to obtain acute, sensory-driven neurophysiological responses before versus during the application of pharmacological agents of interest. These local manipulations are achieved by simultaneous and restricted drug infusions carried out independently for each hemisphere. We have used this protocol to elucidate how neurotransmitter and neuroendocrine systems shape the auditory and perceptual processing of natural, learned communication signals. However, this protocol can be used to explore the neurochemical basis of sensory processing in other small vertebrates. Representative results and troubleshooting of key steps of this protocol are presented. Following the animal\u27s recovery from head-post and recording chamber implantation surgery, the length of the procedure is 2 d

Computational Inference of Neural Information Flow Networks

Determining how information flows along anatomical brain pathways is a fundamental requirement for understanding how animals perceive their environments, learn, and behave. Attempts to reveal such neural information flow have been made using linear computational methods, but neural interactions are known to be nonlinear. Here, we demonstrate that a dynamic Bayesian network (DBN) inference algorithm we originally developed to infer nonlinear transcriptional regulatory networks from gene expression data collected with microarrays is also successful at inferring nonlinear neural information flow networks from electrophysiology data collected with microelectrode arrays. The inferred networks we recover from the songbird auditory pathway are correctly restricted to a subset of known anatomical paths, are consistent with timing of the system, and reveal both the importance of reciprocal feedback in auditory processing and greater information flow to higher-order auditory areas when birds hear natural as opposed to synthetic sounds. A linear method applied to the same data incorrectly produces networks with information flow to non-neural tissue and over paths known not to exist. To our knowledge, this study represents the first biologically validated demonstration of an algorithm to successfully infer neural information flow networks

Age related decline in female lar gibbon great call performance suggests that call features correlate with physical condition

Background: White-handed gibbons (Hylobates lar) are small Asian apes known for living in stable territories and producing loud, elaborate vocalizations (songs), often in well-coordinated male/female duets. The female great call, the most conspicuous phrase of the repertoire, has been hypothesized to function in intra-sexual territorial defense. We therefore predicted that characteristics of the great call would correlate with a caller’s physical condition, and thus might honestly reflect resource holding potential (RHP). Because measurement of RHP is virtually impossible for wild animals, we used age as a proxy, hypothesizing that great call climaxes are difficult to produce and maintain over time, and that older adults will therefore perform lower quality great calls than young adults. To test this we analyzed the great call climaxes of 15 wild lar gibbon females at Khao Yai National Park, Thailand and 2 captive females at Leo Conservation Center, Greenwich, CT. Results: Findings show that call climaxes correlate with female age, as young animals (n = 8, mean age: 12.9 years) produced climaxes with a higher frequency range (delta F0), maximum F0 frequency and duty cycle than old animals (n = 9, mean age: 29.6 years). A permuted discriminant function analysis also correctly classified calls by age group. During long song bouts the maximum F0 frequency of great call climaxes’ also decreased. Additional data support the hypothesis that short high notes, associated with rapid inhalation as an individual catches its breath, reflect increased caller effort. Older females produced more high notes than younger females, but the difference only approached statistical significance, suggesting that calling effort may be similar across different ages. Finally, for the first time in this species, we measured peak intensity of calls in captive females. They were capable of producing climaxes in excess of 100 dB at close range (2.7 m). Conclusions: Age and within-bout differences in the lar gibbon great call climax suggest that call features correlate with physical condition and thus the call may have evolved as an honest signal in the context of intra-sexual territorial defense and possibly also in male mate choice via sexual selection, although further testing of these hypotheses is necessary. Results: Findings show that call climaxes correlate with female age, as young animals (n = 8, mean age: 12.9 years) produced climaxes with a higher frequency range (delta F0), maximum F0 frequency and duty cycle than old animals (n = 9, mean age: 29.6 years). A permuted discriminant function analysis also correctly classified calls by age group. During long song bouts the maximum F0 frequency of great call climaxes’ also decreased. Additional data support the hypothesis that short high notes, associated with rapid inhalation as an individual catches its breath, reflect increased caller effort. Older females produced more high notes than younger females, but the difference only approached statistical significance, suggesting that calling effort may be similar across different ages. Finally, for the first time in this species, we measured peak intensity of calls in captive females. They were capable of producing climaxes in excess of 100 dB at close range (2.7 m). Conclusions: Age and within-bout differences in the lar gibbon great call climax suggest that call features correlate with physical condition and thus the call may have evolved as an honest signal in the context of intra-sexual territorial defense and possibly also in male mate choice via sexual selection, although further testing of these hypotheses is necessary

Neural Correlates of Experience-Induced Deficits in Learned Vocal Communication

Songbirds are one of the few vertebrate groups (including humans) that evolved the ability to learn vocalizations. During song learning, social interactions with adult models are crucial and young songbirds raised without direct contacts with adults typically produce abnormal songs showing phonological and syntactical deficits. This raises the question of what functional representation of their vocalizations such deprived animals develop. Here we show that young starlings that we raised without any direct contact with adults not only failed to differentiate starlings' typical song classes in their vocalizations but also failed to develop differential neural responses to these songs. These deficits appear to be linked to a failure to acquire songs' functions and may provide a model for abnormal development of communicative skills, including speech

Neural Processing of Short-Term Recurrence in Songbird Vocal Communication

BACKGROUND: Many situations involving animal communication are dominated by recurring, stereotyped signals. How do receivers optimally distinguish between frequently recurring signals and novel ones? Cortical auditory systems are known to be pre-attentively sensitive to short-term delivery statistics of artificial stimuli, but it is unknown if this phenomenon extends to the level of behaviorally relevant delivery patterns, such as those used during communication. METHODOLOGY/PRINCIPAL FINDINGS: We recorded and analyzed complete auditory scenes of spontaneously communicating zebra finch (Taeniopygia guttata) pairs over a week-long period, and show that they can produce tens of thousands of short-range contact calls per day. Individual calls recur at time scales (median interval 1.5 s) matching those at which mammalian sensory systems are sensitive to recent stimulus history. Next, we presented to anesthetized birds sequences of frequently recurring calls interspersed with rare ones, and recorded, in parallel, action and local field potential responses in the medio-caudal auditory forebrain at 32 unique sites. Variation in call recurrence rate over natural ranges leads to widespread and significant modulation in strength of neural responses. Such modulation is highly call-specific in secondary auditory areas, but not in the main thalamo-recipient, primary auditory area. CONCLUSIONS/SIGNIFICANCE: Our results support the hypothesis that pre-attentive neural sensitivity to short-term stimulus recurrence is involved in the analysis of auditory scenes at the level of delivery patterns of meaningful sounds. This may enable birds to efficiently and automatically distinguish frequently recurring vocalizations from other events in their auditory scene