Rationale and methodology for testing auditory cognition in songbirds

Songbirds, and in particular zebra finches, present a wonderful opportunity to study cognition in species that have evolved specialized abilities and brain structures for auditory cognition. The authors describe the rationale, methods, and apparatus used to test the auditory perceptual and cognitive abilities of songbirds. They have developed an operant conditioning system for conducting discrimination experiments simultaneously with several songbirds. The system uses specialized single-board computers, standard personal computers, CD-ROMs, and custom-written software to present stimuli, control training, and record responses. Also, the authors describe software to produce high-quality synthesized and naturally occurring acoustic stimuli for use in studies of auditory cognition. Typical results from a challenging frequency-range discrimination are included.     

A behavior analysis of absolute pitch: sex, experience, and species

Absolute pitch (AP) perception refers to the ability to identify, classify, and memorize pitches without use of an external reference pitch. In tests of AP, several species were trained to sort contiguous tones into three or eight frequency ranges, based on correlations between responding to tones in each frequency range and reinforcement. Two songbird species, zebra finches and white-throated sparrows, and a parrot species, budgerigars had highly accurate AP, they discriminated both three and eight ranges with precision. Relative to normally reared songbirds, isolate reared songbirds had impaired AP. Two mammalian species, humans and rats, had equivalent and weak AP, they discriminated three frequency ranges to a lackluster standard and they acquired only a crude discrimination of the lowest and highest of eight frequency ranges. In comparisons with mammals even isolate songbirds had more accurate AP than humans and rats.     

Auditory processing of vocal sounds in birds

The avian auditory system has become a model system to investigate how vocalizations are memorized and processed by the brain in order to mediate behavioral discrimination and recognition. Recent studies have shown that most of the avian auditory system responds preferentially and efficiently to sounds that have natural spectro-temporal statistics. In addition, neurons in secondary auditory forebrain areas have plastic response properties and are the most active when processing behaviorally relevant vocalizations. Physiological measurements show differential responses for vocalizations that were recently learned in discrimination tasks, and for the tutor song, a longer-term auditory memory that is used to guide vocal learning in male songbirds.     

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.     

Automated auditory recognition training and testing

Laboratory training and testing of auditory recognition skills in animals is important for understanding animal communication systems that depend on auditory cues. Songbirds are commonly studied because of their exceptional ability to learn complex vocalizations. In recent years, mounting interest in the perceptual abilities of songbirds has increased the demand for laboratory behavioural training and testing paradigms. Here, we describe and demonstrate the success of a method for auditory discrimination experiments, including all the necessary hardware, training procedures and freely-available, versatile software. The system can run several behavioural training and testing paradigms, including operant (go-nogo, stimulus preference, and two-alternative forced choice) and classical conditioning tasks. The software and some hardware components can be used with any laboratory animal that learns and responds to sensory cues. The peripheral hardware and training procedures are designed for use with songbirds and auditory stimuli. Using the go-nogo paradigm of the training system, we show that adult zebra finches learn to recognize and correctly classify individual female calls and male songs. We also show that learning the task generalizes to new stimulus classes; birds that learned the task with calls subsequently learned to recognize songs faster than did birds that learned the task and songs at the same time.     

Modelling the unpredictability of future biodiversity in ecological networks

We consider the question of how accurately we can hope to predict future biodiversity in a world in which many interacting species are at risk of extinction. Simple models assuming that species’ extinctions occur independently are easily analysed, but do not account for the fact that many species depend on or otherwise interact with each other. In this paper we evaluate the effect of explicitly incorporating ecological dependencies on the predictive ability of models of extinction. In particular, we compare a model in which species’ extinction rates increase because of the extinction of their prey to a model in which the same average rate increase takes place, but in which extinctions occur independently from species to species. One might expect that including this ecological information would make the prediction of future biodiversity more accurate, but instead we find that accounting for food web dependencies reveals greater uncertainty. The expected loss of biodiversity over time is similar between the two models, but the variance in future biodiversity is considerably higher in the model that includes species interactions. This increased uncertainty is because of the non-independence of species—the tendency of two species to respond similarly to the loss of a species on which both depend. We use simulations to show that this increase in variance is robust to many variations of the model, and that its magnitude should be largest in food webs that are highly dependent on a few basal species. Our results should hold whenever ecological dependencies cause most species’ extinction risks to covary positively, and illustrate how more information does not necessarily improve our ability to predict future biodiversity loss.     

Neural mechanisms of auditory species recognition in birds

Auditory communication in humans and other animals frequently takes place in noisy environments with many co‐occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species‐specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a ‘perceptual filter’‐based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species‐specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species‐recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.     

Auditory feedback is necessary for long-term maintenance of high-frequency sound syllables in the song of adult male budgerigars (<Emphasis Type="Italic">Melopsittacus undulatus</Emphasis>)

Among avian species that communicate using vocalization, songbirds (oscine Passeriformes), hummingbirds (Trochiliformes), and parrots (Psittaciformes) are vocal learners. Early studies showed that songbirds require auditory feedback for song development in young and maintenance in adults. To determine whether auditory feedback is also necessary for adult song maintenance in non-passerine species, we deprived adult male budgerigars (Psittaciformes) of auditory input by surgical cochlear removal. Songs of the deafened birds changed within 6 months after auditory deprivation. In postoperative songs, high narrowband syllables, which comprised frequency-modulated narrowband elements with relatively high fundamental frequencies of 2–4 kHz, decreased significantly. High harmonic broadband syllables, with fundamental frequencies ≥2 kHz, also decreased. The altered proportions of syllables were subsequently retained, and maintained 12 months after deafening. The sequence linearity score, a parameter representing the stereotypy of the syllable sequence, was higher than that before deafening. The inter-syllable silence was prolonged. Little change was observed in the songs of intact and sham-operated birds. The significant decrease in high-frequency syllables and song alteration followed by stabilization resembled the results with songbirds, although song stabilization took a long time in budgerigars. Therefore, our results suggest that psittacine budgerigars and oscine songbirds require auditory feedback similarly for adult song maintenance.     

Neural mechanisms of birdsong memory

The process through which young male songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorization followed by a period during which the individual develops its own vocalizations. The avian 'song system', a network of brain nuclei, is the probable neural substrate for the second phase of sensorimotor learning. By contrast, the neural representation of song memory acquired in the first phase is localized outside the song system, in different regions of the avian equivalent of the human auditory association cortex.     

Separate attentional resources for vision and audition

Current models of attention, typically claim that vision and audition are limited by a common attentional resource which means that visual performance should be adversely affected by a concurrent auditory task and vice versa. Here, we test this implication by measuring auditory (pitch) and visual (contrast) thresholds in conjunction with cross-modal secondary tasks and find that no such interference occurs. Visual contrast discrimination thresholds were unaffected by a concurrent chord or pitch discrimination, and pitch-discrimination thresholds were virtually unaffected by a concurrent visual search or contrast discrimination task. However, if the dual tasks were presented within the same modality, thresholds were raised by a factor of between two (for visual discrimination) and four (for auditory discrimination). These results suggest that at least for low-level tasks such as discriminations of pitch and contrast, each sensory modality is under separate attentional control, rather than being limited by a supramodal attentional resource. This has implications for current theories of attention as well as for the use of multi-sensory media for efficient informational transmission.     

Age effect of deafening on stereotyped song maintenance in adult male bengalese finches Lonchura striata domestica

Birdsong is a complex learned vocal behavior that relies on auditory experience for development.However,it appears that among different species of close-ended songbirds,there are some variations in the necessity of auditory feedback for maintaining stereotyped adult song.In zebra finches,the deterioration of adult songs following deafness depends on the birds' age.It is unknown whether this age effect is a general rule in other avian species as well.Therefore,we chose Bengalese finches,whose songs show more...     

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 (sub fields 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-specific 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.     

Conspecific-only experience during development reduces the strength of heterospecific song discrimination in Zebra Finches (Taeniopygia guttata): a test of the optimal acceptance threshold hypothesis

Conspecifics during development provide the most reliable sensory cues for species recognition in parental bird species. The Zebra Finch (Taeniopygia guttata) is a sexually dimorphic model species used for investigations of the behavioural cues and neurobiological substrates of species recognition. Regarding acoustic conspecific cues, theory predicts that exposure to both con- and heterospecific vocalisations and other environmental sounds results in more accurate auditory species discrimination, because diverse vocal cues during development shift optimal conspecific acceptance thresholds to be more restrictive to yield fewer acceptance errors. We tested the behavioural preferences of female and male Zebra Finches raised in an outdoor environment (Control) and female and male Zebra Finches reared in an indoor colony with exposure to Zebra Finches only (Restricted), to playbacks of songs of Zebra Finches, Zebra Finches cross-fostered by Bengalese Finches (Lonchura striata var. domestica), and Bengalese Finches. Several behavioural measures revealed minimal sexual dimorphism in discrimination but showed that Control subjects preferred conspecifics’ songs over either the songs of cross-fostered Zebra Finches or Bengalese Finches. Restricted Zebra Finches in contrast did not discriminate behaviourally between the three song types. These results support the concept of a shift in the species acceptance threshold in the restricted treatment resulting in more acceptance errors. We discuss future work to test the role of exposure to diverse vocal cues of both con- and heterospecifics in the ontogeny of song perception in this important laboratory model species for social recognition research.     

Representation of Early Sensory Experience in the Adult Auditory Midbrain: Implications for Vocal Learning

Vocal learning in songbirds and humans occurs by imitation of adult vocalizations. In both groups, vocal learning includes a perceptual phase during which juveniles birds and infants memorize adult vocalizations. Despite intensive research, the neural mechanisms supporting this auditory memory are still poorly understood. The present functional MRI study demonstrates that in adult zebra finches, the right auditory midbrain nucleus responds selectively to the copied vocalizations. The selective signal is distinct from selectivity for the bird''s own song and does not simply reflect acoustic differences between the stimuli. Furthermore, the amplitude of the selective signal is positively correlated with the strength of vocal learning, measured by the amount of song that experimental birds copied from the adult model. These results indicate that early sensory experience can generate a long-lasting memory trace in the auditory midbrain of songbirds that may support song learning.     

Learning to communicate

Of the few animal groups that learn their vocalizations, songbirds are uniquely amenable to molecular, physiological, and behavioral analyses of the neural features responsible for vocal learning. In order to communicate effectively as an adult, a young songbird recognizes and memorizes a model of his species-specific song during a developmentally critical period called sensory acquisition. Factors are now emerging that contribute to the length and strength of this learning phase. In a second critical period, known as sensorimotor learning, the young bird uses auditory feedback to perfect his motor performance, creating a match to the memorized model. New studies show that motor matching can persist beyond sensorimotor learning, and thus a role for the acquired model might also persist into adulthood. Fascinating in their own right, songbirds also provide optimism that mature brains have recourse to plasticity.     

Development of Auditory-Vocal Perceptual Skills in Songbirds

Songbirds are one of the few groups of animals that learn the sounds used for vocal communication during development. Like humans, songbirds memorize vocal sounds based on auditory experience with vocalizations of adult “tutors”, and then use auditory feedback of self-produced vocalizations to gradually match their motor output to the memory of tutor sounds. In humans, investigations of early vocal learning have focused mainly on perceptual skills of infants, whereas studies of songbirds have focused on measures of vocal production. In order to fully exploit songbirds as a model for human speech, understand the neural basis of learned vocal behavior, and investigate links between vocal perception and production, studies of songbirds must examine both behavioral measures of perception and neural measures of discrimination during development. Here we used behavioral and electrophysiological assays of the ability of songbirds to distinguish vocal calls of varying frequencies at different stages of vocal learning. The results show that neural tuning in auditory cortex mirrors behavioral improvements in the ability to make perceptual distinctions of vocal calls as birds are engaged in vocal learning. Thus, separate measures of neural discrimination and behavioral perception yielded highly similar trends during the course of vocal development. The timing of this improvement in the ability to distinguish vocal sounds correlates with our previous work showing substantial refinement of axonal connectivity in cortico-basal ganglia pathways necessary for vocal learning.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

Tactile Discrimination of Gratings: Psychophysical and Neural Correlates in Human and Monkey

Human and monkey performance on discriminating tactile gratings revealed comparable cross-species Weber functions. Neural data obtained while monkeys performed discriminations revealed some matching of neural and psychometric functions. Nearly constant firing rate differences occurred at discrimination threshold for unequal groove widths. Firing rate differences of some cells decreased on trials preceding discrimination errors, and thus predicted performance.     

Phenology and seed setting success of snowbed plant species in contrasting snowmelt regimes in the Central Pyrenees

Plant growth and performance in snowbed communities are strongly influenced by the length of the growing period remaining after the snowmelt date. Under the scenario of climate change, studying the phenological responses of snowbed species to variations in snowmelt date might be crucial to understand their ability to adapt and survive under changing conditions. We studied 13 plant species from contrasting biological and ecological groups (i.e. ‘snowbed specialists’, ‘preferential species’ and ‘generalist species’) growing in four snowbed plots with siliceous substrates in the Central Pyrenees. These species were monitored for two consecutive years and in two different microsites, namely the central part and the peripheral part of each snowbed plot. We characterised their phenological cycle and length and their success in seed setting, measured as the number of individuals succeeding in dispersing their seeds.     

Tactile discrimination of gratings: psychophysical and neural correlates in human and monkey.

Human and monkey performance on discriminating tactile gratings revealed comparable cross-species Weber functions. Neural data obtained while monkeys performed discriminations revealed some matching of neural and psychometric functions. Nearly constant firing rate differences occurred at discrimination threshold for unequal groove widths. Firing rate differences of some cells decreased on trials preceding discrimination errors, and thus predicted performance.