Vocal Learning Species Research Articles

An exploration of rhythm perception in African penguins (Spheniscus demersus)

Rhythmic properties in penguin vocalizations may be unique to individuals. Rhythm perception is a cognitive ability previously thought to be exclusive to vocal-learning species who have the neurological complexities required to mimic conspecific and heterospecific vocalizations. Discovering rhythm perception in penguins would provide insight on penguins’ ability to recognize kin using auditory cues, and discount theories constraining rhythm perception to vocal-learning animals. The goal of this study was to learn if African penguins (Spheniscus demersus) could perceive changes in rhythm using a habituation-dishabituation paradigm. Subjects were 32–38 African penguins housed at the Seneca Park Zoo in Rochester, NY. Penguins were played four rhythms at 4 kHz and head turns per bird were counted in 24 sessions. Each session was composed of ten familiarization trials followed by six test trials that alternated between the familiar and novel rhythm. The number of head turns per bird did not significantly increase from the last three familiarization trials to the first novel test trial. Results were inconclusive in showing evidence for auditory rhythm perception in penguins. This may be because subjects met the habituation criterion in only 9 out of 24 sessions. More research on auditory rhythm perception in penguins is needed.

Predictive and tempo-flexible synchronization to a visual metronome in monkeys

Predictive and tempo-flexible synchronization to an auditory beat is a fundamental component of human music. To date, only certain vocal learning species show this behaviour spontaneously. Prior research training macaques (vocal non-learners) to tap to an auditory or visual metronome found their movements to be largely reactive, not predictive. Does this reflect the lack of capacity for predictive synchronization in monkeys, or lack of motivation to exhibit this behaviour? To discriminate these possibilities, we trained monkeys to make synchronized eye movements to a visual metronome. We found that monkeys could generate predictive saccades synchronized to periodic visual stimuli when an immediate reward was given for every predictive movement. This behaviour generalized to novel tempi, and the monkeys could maintain the tempo internally. Furthermore, monkeys could flexibly switch from predictive to reactive saccades when a reward was given for each reactive response. In contrast, when humans were asked to make a sequence of reactive saccades to a visual metronome, they often unintentionally generated predictive movements. These results suggest that even vocal non-learners may have the capacity for predictive and tempo-flexible synchronization to a beat, but that only certain vocal learning species are intrinsically motivated to do it.

Generalizing prosodic patterns by a non-vocal learning mammal

Prosody, a salient aspect of speech that includes rhythm and intonation, has been shown to help infants acquire some aspects of syntax. Recent studies have shown that birds of two vocal learning species are able to categorize human speech stimuli based on prosody. In the current study, we found that the non-vocal learning rat could also discriminate human speech stimuli based on prosody. Not only that, but rats were able to generalize to novel stimuli they had not been trained with, which suggests that they had not simply memorized the properties of individual stimuli, but learned a prosodic rule. When tested with stimuli with either one or three out of the four prosodic cues removed, the rats did poorly, suggesting that all cues were necessary for the rats to solve the task. This result is in contrast to results with humans and budgerigars, both of which had previously been studied using the same paradigm. Humans and budgerigars both learned the task and generalized to novel items, but were also able to solve the task with some of the cues removed. In conclusion, rats appear to have some of the perceptual abilities necessary to generalize prosodic patterns, in a similar though not identical way to the vocal learning species that have been studied.

Perceptual and cognitive enhancement with an adaptive timing partner: Electrophysiological responses to pitch change.

(ProQuest: ... denotes formula omitted.)When two people play music together, they need to control timing of their own actions while also adjusting their actions in response to those of other (Nowicki, Prinz, Grosjean, Repp, & Keller, 2013; Wing, Endo, Bradbury, & Vorberg, 2014). Having a partner who adapts can be satisfying. Patients playing a percussion instrument with a music therapist who entrains to them may gain a sense of freedom in expressing their emotion and feel empowered by experience (Bensimon, Amir, & Wolf, 2008; Winkelman, 2003).In many species, individuals synchronize their movements together, such as birds that fly in formation, fish that swim in schools, and fireflies that flash at same time (Buck, 1935, 1937, 1988; Partridge, 1982; Weimerskirch, Martin, Clerquin, Alexandre, & Jiraskova, 2001). More rare, but found in humans and a few vocal learning species, is ability to synchronize movement to a predictable auditory stimulus, such as beat in music (Patel & Iversen, 2014; Patel, Iversen, Bregman, & Schulz, 2009; Schachner, Brady, Pepperberg, & Hauser, 2009; Trainor, 2015). This ability is referred to as sensorimotor synchronization (SMS) and is defined as the coordination of rhythmic movement with an external rhythm (Repp & Su, 2013).In a typical musical performance, underlying beat or tempo produced is not completely steady, with deviations arising from several sources, such as internal time-keeping errors (Torre & Delignieres, 2008; Wing & Kristofferson, 1973a, 1973b), and deliberate deviations for expressive purposes (James, Michel, Britz, Vuilleumier, & Hauert, 2012; Rankin, Large, & Fink, 2009; Repp, 1992). Thus, for two or more people to play music together in synchrony, it necessarily involves mutual adjustments of phase alignment and tempo (period) to achieve SMS.The study of interpersonal synchrony is particularly important because empirical evidence indicates that synchronous movement promotes a sense of group affiliation. For example, walking or singing in synchrony with others increases cooperation, trust, and ratings of likability among participants (Hove & Risen, 2009; Kirschner & Tomasello, 2010; Valdesolo, Ouyang, & DeSteno, 2010; Wiltermuth & Heath, 2009). Synchronous movement to music even leads to enhanced prosocial instrumental helping in infants (Cirelli, Einarson, & Trainor, 2014; Cirelli & Trainor, 2015). Cirelli, Wan, and Trainor (2014) bounced 14-month-old infants to music facing an experimenter who bounced in synchrony with infant, or in antiphase (but at same tempo), or at a different tempo from infant. After this experience, infants were more likely to help experimenter by retrieving accidentally dropped items needed to complete a task if they had bounced at same tempo as experimenter (either in phase or antiphase) compared with if they bounced at a different tempo, whether faster or slower. Of interest to authors, this increase in helping after synchronous bouncing is targeted to bouncing partner and not to neutral strangers (Cirelli, Wan, et al., 2014), although it does apply to friends of synchronous bouncing partner (Cirelli & Trainor, 2015).It has been proposed that three core cognitive-motor skills are needed for people to engage in real-time interpersonal coordination-( a) propensity to synchronize movements, (b) ability to use anticipatory mechanisms during SMS, and (c) ability to divide attention (reviewed by Keller, Novembre, & Hove, 2014), reviewed in more detail below. In present study, we investigate perceptual/cognitive consequences of playing with an adaptive partner. In particular, during a difficult SMS task, we expect that an adaptive virtual partner that adjusts its onset times so as to place its upcoming tones closer to expectations of a musically untrained partner will reduce resource demands for that untrained partner compared with a virtual partner that does not adjust, leading to enhanced perceptual and cognitive processing of music. …

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos.

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.

Expression of androgen receptor in the brain of a sub-oscine bird with an elaborate courtship display

Sex steroids control vertebrate behavior by modulating neural circuits specialized for sex steroid sensitivity. In birds, receptors for androgens (AR) and estrogens (ERα) show conserved expression in neural circuits controlling copulatory and vocal behaviors. Male golden-collared manakins have become a model for evaluating hormonal control of complex physical courtship displays. These birds perform visually and acoustically elaborate displays involving considerable neuromuscular coordination. Androgens activate manakin courtship and AR are expressed widely in spinal circuits and peripheral muscles utilized in courtship. Using in situ hybridization, we report here the distributions of AR and ERα mRNA in the brains of golden-collared manakins. Overall patterns of AR and ERα mRNA expression resemble what has been observed in non-vocal learning species. Notably, however, we detected a large area of AR expression in the arcopallium, a forebrain region that contains a crucial premotor song nucleus in vocal learning species. These results support the idea that AR signaling both centrally and peripherally is responsible for the activation of male manakin courtship, and the arcopallium is likely a premotor site for AR-mediated displays

Distribution of language‐related Cntnap2 protein in neural circuits critical for vocal learning

Variants of the contactin associated protein-like 2 (Cntnap2) gene are risk factors for language-related disorders including autism spectrum disorder, specific language impairment, and stuttering. Songbirds are useful models for study of human speech disorders due to their shared capacity for vocal learning, which relies on similar cortico-basal ganglia circuitry and genetic factors. Here we investigate Cntnap2 protein expression in the brain of the zebra finch, a songbird species in which males, but not females, learn their courtship songs. We hypothesize that Cntnap2 has overlapping functions in vocal learning species, and expect to find protein expression in song-related areas of the zebra finch brain. We further expect that the distribution of this membrane-bound protein may not completely mirror its mRNA distribution due to the distinct subcellular localization of the two molecular species. We find that Cntnap2 protein is enriched in several song control regions relative to surrounding tissues, particularly within the adult male, but not female, robust nucleus of the arcopallium (RA), a cortical song control region analogous to human layer 5 primary motor cortex. The onset of this sexually dimorphic expression coincides with the onset of sensorimotor learning in developing males. Enrichment in male RA appears due to expression in projection neurons within the nucleus, as well as to additional expression in nerve terminals of cortical projections to RA from the lateral magnocellular nucleus of the nidopallium. Cntnap2 protein expression in zebra finch brain supports the hypothesis that this molecule affects neural connectivity critical for vocal learning across taxonomic classes.

Interspecies avian brain chimeras reveal that large brain size differences are influenced by cell-interdependent processes.

Like humans, birds that exhibit vocal learning have relatively delayed telencephalon maturation, resulting in a disproportionately smaller brain prenatally but enlarged telencephalon in adulthood relative to vocal non-learning birds. To determine if this size difference results from evolutionary changes in cell-autonomous or cell-interdependent developmental processes, we transplanted telencephala from zebra finch donors (a vocal-learning species) into Japanese quail hosts (a vocal non-learning species) during the early neural tube stage (day 2 of incubation), and harvested the chimeras at later embryonic stages (between 9–12 days of incubation). The donor and host tissues fused well with each other, with known major fiber pathways connecting the zebra finch and quail parts of the brain. However, the overall sizes of chimeric finch telencephala were larger than non-transplanted finch telencephala at the same developmental stages, even though the proportional sizes of telencephalic subregions and fiber tracts were similar to normal finches. There were no significant changes in the size of chimeric quail host midbrains, even though they were innervated by the physically smaller zebra finch brain, including the smaller retinae of the finch eyes. Chimeric zebra finch telencephala had a decreased cell density relative to normal finches. However, cell nucleus size differences between each species were maintained as in normal birds. These results suggest that telencephalic size development is partially cell-interdependent, and that the mechanisms controlling the size of different brain regions may be functionally independent.

Experimental Evidence for Synchronization to a Musical Beat in a Nonhuman Animal

The tendency to move in rhythmic synchrony with a musical beat (e.g., via head bobbing, foot tapping, or dance) is a human universal [1] yet is not commonly observed in other species [2]. Does this ability reflect a brain specialization for music cognition, or does it build on neural circuitry that ordinarily serves other functions? According to the "vocal learning and rhythmic synchronization" hypothesis [3], entrainment to a musical beat relies on the neural circuitry for complex vocal learning, an ability that requires a tight link between auditory and motor circuits in the brain [4, 5]. This hypothesis predicts that only vocal learning species (such as humans and some birds, cetaceans, and pinnipeds, but not nonhuman primates) are capable of synchronizing movements to a musical beat. Here we report experimental evidence for synchronization to a beat in a sulphur-crested cockatoo (Cacatua galerita eleonora). By manipulating the tempo of a musical excerpt across a wide range, we show that the animal spontaneously adjusts the tempo of its rhythmic movements to stay synchronized with the beat. These findings indicate that synchronization to a musical beat is not uniquely human and suggest that animal models can provide insights into the neurobiology and evolution of human music [6].

Anatomical and Functional Organization of Inhibitory Circuits in the Songbird Auditory Forebrain

Recent studies on the anatomical and functional organization of GABAergic networks in central auditory circuits of the zebra finch have highlighted the strong impact of inhibitory mechanisms on both the central encoding and processing of acoustic information in a vocal learning species. Most of this work has focused on the caudomedial nidopallium (NCM), a forebrain area postulated to be the songbird analogue of the mammalian auditory association cortex. NCM houses neurons with selective responses to conspecific songs and is a site thought to house auditory memories required for vocal learning and, likely, individual identification. Here we review our recent work on the anatomical distribution of GABAergic cells in NCM, their engagement in response to song and the roles for inhibitory transmission in the physiology of NCM at rest and during the processing of natural communication signals. GABAergic cells are highly abundant in the songbird auditory forebrain and account for nearly half of the overall neuronal population in NCM with a large fraction of these neurons activated by song in freely-behaving animals. GABAergic synapses provide considerable local, tonic inhibition to NCM neurons at rest and, during sound processing, may contain the spread of excitation away from un-activated or quiescent parts of the network. Finally, we review our work showing that GABA(A)-mediated inhibition directly regulates the temporal organization of song-driven responses in awake songbirds, and appears to enhance the reliability of auditory encoding in NCM.

Organization of the avian basal forebrain: chemical anatomy in the parrot (Melopsittacus undulatus).

Hodological, electrophysiological, and ablation studies indicate a role for the basal forebrain in telencephalic vocal control; however, to date the organization of the basal forebrain has not been extensively studied in any nonmammal or nonhuman vocal learning species. To this end the chemical anatomy of the avian basal forebrain was investigated in a vocal learning parrot, the budgerigar (Melopsittacus undulatus). Immunological and histological stains, including choline acetyltransferase, acetylcholinesterase, tyrosine hydroxylase, dopamine and cAMP-regulated phosphoprotein (DARPP)-32, the calcium binding proteins calbindin D-28k and parvalbumin, calcitonin gene-related peptide, iron, substance P, methionine enkephalin, nicotinamide adenine dinucleotide phosphotase diaphorase, and arginine vasotocin were used in the present study. We conclude that the ventral paleostriatum (cf. Kitt and Brauth [1981] Neuroscience 6:1551-1566) and adjacent archistriatal regions can be subdivided into several distinct subareas that are chemically comparable to mammalian basal forebrain structures. The nucleus accumbens is histochemically separable into core and shell regions. The nucleus taeniae (TN) is theorized to be homologous to the medial amygdaloid nucleus. The archistriatum pars ventrolateralis (Avl; comparable to the pigeon archistriatum pars dorsalis) is theorized to be a possible homologue of the central amygdaloid nucleus. The TN and Avl are histochemically continuous with the medial aspects of the bed nucleus of the stria terminalis and the ventromedial striatum, forming an avian analogue of the extended amygdala. The apparent counterpart in budgerigars of the mammalian nucleus basalis of Meynert consists of a field of cholinergic neurons spanning the basal forebrain. The budgerigar septal region is theorized to be homologous as a field to the mammalian septum. Our results are discussed with regard to both the evolution of the basal forebrain and its role in vocal learning processes.

Distribution of tyrosine hydroxylase-containing neurons and fibers in the brain of the budgerigar (Melopsittacus undulatus): general patterns and labeling in vocal control nuclei.

The distribution of tyrosine hydroxylase (TH) was mapped out in cells and fibers of the budgerigar (Melopsittacus undulatus) brain. Special attention was given to vocal control and auditory nuclei because budgerigars are a psittacine species in which both males and females are capable of lifelong vocal learning (Farabaugh et al. [1994] J. Comp. Psychol 108:81-92). The results show that TH staining in the central nucleus of the anterior archistriatum (AAc) resembled that of surrounding archistriatal fields, except for portions of the ventral archistriatum, which exhibited substantially more TH+ fibers. Fewer fibers and fiber baskets are present in the central nucleus of the lateral neostriatum (NLc) than in surrounding fields. Both the oval nuclei of the ventral hyperstriatum (HVo) and anterior neostriatum (NAo) exhibit less fiber staining than surrounding fields whereas fiber staining in the medial NAo (NAom) and magnicellular nucleus of the parolfactory lobe (LPOm) resemble that of surrounding fields. Staining in primary telencephalic auditory nuclei was extremely low. The only sex difference observed was slightly increased TH staining in LPOm of females compared with surrounding fields on some tissue sections. These findings are in contrast to previous findings in zebra finch (Poephila guttata), a close ended vocal learning songbird in which TH staining in vocal nuclei increases during development and remains greater than surrounding fields throughout adulthood. The present results therefore support the view that catecholamines act to inhibit vocal plasticity in adult vocal learning species. Several unique features of TH-immunoreactive (ir) cell groups were observed in the brainstem including sparsely scattered TH-ir somata immediately adjacent to the third ventricle, within the tectum, basal forebrain, archistriatum, and caudal neostriatum, and in the hippocampus. These latter populations have not been described in other avian species and resemble features of the catecholamine system generally found in either reptiles or mammals.