ZENK activation in the nidopallium of black-capped chickadees in response to both conspecific and heterospecific calls.

Neuronal populations in the songbird nidopallium increase in activity the most to conspecific vocalizations relative to heterospecific songbird vocalizations or artificial stimuli such as tones. Here, we tested whether the difference in neural activity between conspecific and heterospecific vocalizations is due to acoustic differences or to the degree of phylogenetic relatedness of the species producing the vocalizations. To compare differences in neural responses of black-capped chickadees, Poecile atricapillus, to playback conditions we used a known marker for neural activity, ZENK, in the caudal medial nidopallium and caudomedial mesopallium. We used the acoustically complex 'dee' notes from chick-a-dee calls, and vocalizations from other heterospecific species similar in duration and spectral features. We tested the vocalizations from three heterospecific species (chestnut-backed chickadees, tufted titmice, and zebra finches), the vocalizations from conspecific individuals (black-capped chickadees), and reversed versions of the latter. There were no significant differences in the amount of expression between any of the groups except in the control condition, which resulted in significantly less neuronal activation. Our results suggest that, in certain cases, neuronal activity is not higher in response to conspecific than in response to heterospecific vocalizations for songbirds, but rather is sensitive to the acoustic features of the signal. Both acoustic features of the calls and the phylogenetic relationship between of the signaler and the receiver interact in the response of the nidopallium.

Development of a contact call in black-capped chickadees (Poecile atricapillus) hand-reared in different acoustic environments.

The tseet contact call, common to black-capped (Poecile atricapillus) and mountain chickadees (P. gambeli), is the most frequently produced vocalization of each species. Previous work has characterized the tseet call of black-capped and mountain chickadees from different geographic locations in terms of nine acoustic features. In the current study, using similar methods, the tseet call of black-capped chickadees that were hand reared with either conspecifics, heterospecifics (mountain chickadees), or in isolation from adult chickadees are described. Analysis of call features examined which acoustic features were most affected by rearing environment, and revealed that starting frequency and the slope of the descending portion of the tseet call differed between black-capped chickadees reared with either conspecific or heterospecific adults. Birds reared in isolation from adults differed from the other hand-reared groups on almost every acoustic feature. Chickadee tseet calls are more individualized when they are reared with adult conspecifics or heterospecifics compared to chickadees that are reared in isolation from adults. The current results suggest a role of learning in this commonly used contact call.

Neural correlates of threat perception: neural equivalence of conspecific and heterospecific mobbing calls is learned.

Songbird auditory areas (i.e., CMM and NCM) are preferentially activated to playback of conspecific vocalizations relative to heterospecific and arbitrary noise. Here, we asked if the neural response to auditory stimulation is not simply preferential for conspecific vocalizations but also for the information conveyed by the vocalization. Black-capped chickadees use their chick-a-dee mobbing call to recruit conspecifics and other avian species to mob perched predators. Mobbing calls produced in response to smaller, higher-threat predators contain more "D" notes compared to those produced in response to larger, lower-threat predators and thus convey the degree of threat of predators. We specifically asked whether the neural response varies with the degree of threat conveyed by the mobbing calls of chickadees and whether the neural response is the same for actual predator calls that correspond to the degree of threat of the chickadee mobbing calls. Our results demonstrate that, as degree of threat increases in conspecific chickadee mobbing calls, there is a corresponding increase in immediate early gene (IEG) expression in telencephalic auditory areas. We also demonstrate that as the degree of threat increases for the heterospecific predator, there is a corresponding increase in IEG expression in the auditory areas. Furthermore, there was no significant difference in the amount IEG expression between conspecific mobbing calls or heterospecific predator calls that were the same degree of threat. In a second experiment, using hand-reared chickadees without predator experience, we found more IEG expression in response to mobbing calls than corresponding predator calls, indicating that degree of threat is learned. Our results demonstrate that degree of threat corresponds to neural activity in the auditory areas and that threat can be conveyed by different species signals and that these signals must be learned.

Note types and coding in Parid vocalizations: the chick-a-dee call of the boreal chickadee (Poecile hudsonicus).

An important first step in characterizing a vocalization is to classify, describe, and measure the elements of that vocalization. Here, this methodology is employed to study the chick-a-dee call of the boreal chickadee (Poecile hudsonicus). The note types (A, B, C, D, and D(h)) in a sample of boreal chickadee calls are identified and described, spectral and temporal features of each note type are analyzed, and production phenomena in each note type are identified and quantified. Acoustic variability is compared across note types and individuals to determine potential features used for note-type and individual discrimination. Frequency measures appear to be the most useful features for identifying note types and individuals, though total duration may also be useful. Call syntax reveals that boreal chick-a-dee calls follow a general rule of note-type order, namely A-B-C-D(h)-D, and that any note type in this sequence may be repeated or omitted. This work provides a thorough description of the boreal chickadee chick-a-dee call and will serve as a foundation for future studies aimed at elucidating this call's functional significance within this species, as well as for studies comparing chick-a-dee calls across Poecile species.

Black-capped (Poecile atricapillus) and mountain chickadee (Poecile gambeli) contact call contains species, sex, and individual identity features.

The tseet contact call, common to both black-capped and mountain chickadees, is among the most frequently produced call of each species, but has remained little studied until now. In the current study, the authors characterized the tseet call of adult allopatric and sympatric black-capped and mountain chickadees in terms of nine acoustic features in a fashion similar to descriptive accounts of both species' chick-a-dee calls. Summary statistics, the potential for individual coding, and classification by linear discriminant analysis were used to describe the tseet call. The authors were able to correctly classify tseet calls in terms of which group or individual produced it with high accuracy. Furthermore, several acoustic features are highly individualized, indicating that the chickadees may use these features to identify signalers as individuals or members of a particular group.

Using network models of absolute pitch to compare frequency-range discriminations across avian species.

The spectral frequency ranges of song notes are important for recognition in avian species tested in the field. Frequency-range discriminations in both the field and laboratory require absolute pitch (AP). AP is the ability to perceive pitches without an external referent. The authors provided a network model designed to account for differences in AP among avian species and evaluated it against discriminative performance in eight-frequency-range laboratory tests of AP for five species of songbirds and two species of nonsongbirds. The model's sensory component describes the neural substrate of avian auditory perception, and its associative component handles learning of the discrimination. Using only two free parameters to describe the selectivity and the sensitivity of each species' auditory sensory filters, the model provided highly accurate predictions of frequency-range discrimination in songbirds and in a parrot species, but performance and its prediction were less accurate in pigeons: the only species tested that does not learn its vocalizations. Here for the first time, the authors present a model that predicted individual species' performance in frequency-range discriminations and predicted differences in discrimination among avian species with high accuracy.

Comparing black-capped (Poecile atricapillus) and mountain chickadees (Poecile gambeli): use of geometric and featural information in a spatial orientation task.

Since Cheng (Cognition 23:149-178, 1986) first proposed the "geometric module" in rats, a great deal of research has focused on how other species use geometric information and how geometric encoding may differ across species. Here, hand-reared and wild-caught black-capped chickadees and wild-caught mountain chickadees searched for food hidden in one corner in a rectangular environment. Previous research has shown that mountain chickadees do not spontaneously encode geometric information when a salient feature is present near the goal location. Using a slightly different training and testing procedure, we found that both hand-reared and wild-caught black-capped chickadees encoded geometric information, even in the presence of a salient landmark. Some, but not all, mountain chickadees also encoded geometric information. Overall, our results suggest that use of geometric information may be a less preferred strategy for mountain chickadees than for either wild-caught or hand-reared black-capped chickadees. To our knowledge, this is the first direct interspecies comparison of use of geometric information in a spatial orientation task.

Categorization and discrimination of "chick-a-dee" calls by wild-caught and hand-reared chickadees.

Bloomfield and Sturdy [Bloomfield, L.L., Sturdy, C.B. All chick-a-dee calls are not created equally. Part I. Open-ended categorization by sympatric and allopatric chickadees. Behav. Proc., in press] previously reported that black-capped chickadees (Poecile atricapillus) discriminate conspecific from heterospecific (mountain chickadee, P. gambeli) 'chick-a-dee' calls, and their ability to accurately discriminate and classify the calls as belonging to separate species' defined categories was largely unaffected by their prior experience with mountain chickadees and their calls. To further examine the potential influence of experience on discrimination and categorization, we compare wild-caught black-capped chickadees, wild-caught mountain chickadees, and black-capped chickadees hand-reared among either adult laboratory-housed black-capped chickadees or adult laboratory-housed mountain chickadees on a true category/pseudo category chick-a-dee call discrimination task. Irrespective of group assignment, hand-reared birds performed as well as wild-caught birds and did not show a conspecific- or rearing-specific advantage in discrimination, categorization or memorization of chick-a-dee calls. While vocal learning is under the influence of ontogenetic experience, the results derived from the current methods suggest that experience (or a lack thereof) does not affect categorization and memorization abilities.

All "chick-a-dee" calls are not created equally. Part I. Open-ended categorization of chick-a-dee calls by sympatric and allopatric chickadees.

Researchers trained 24 black-capped (Poecile atricapillus) and 12 mountain (P. gambeli) chickadees in an operant conditioning task to determine if they use open-ended categorization to classify "chick-a-dee" calls, and whether black-capped chickadees that had experience with mountain chick-a-dee calls (sympatric group) would perform this task differently than inexperienced black-capped chickadees (allopatric group). All experimental birds learned to discriminate between species' call categories faster than within a category (Experiment 1), and subsequently classified novel and original between-category chick-a-dee calls in Experiments 2 and 3 following a change in the category contingency. These results suggest that regardless of previous experience, black-capped and mountain chickadees classify their own and the other species' calls into two distinct, yet open-ended, species-level categories.

Feature weighting in "chick-a-dee" call notes of Poecile atricapillus.

Artificial neural networks were trained to discriminate between different note types from the black-capped chickadee (Poecile atricapillus) "chick-a-dee" call. Each individual note was represented as a vector of summary features taken from note spectrograms and networks were trained to respond to exemplar notes of one type and to fail to respond to exemplar notes of another type. Following initial network training, the network was presented novel notes in which individual acoustic features had been modified. The strength of the response of the network to each novel and shifted note was recorded. When network responses were plotted as a function of the degree of acoustic feature modification and training context, it became clear that modifications of some acoustic features had significant effects on network responses, while others did not. Moreover, the training context of the network also played a role in the responses of networks to manipulated test notes. The implications of using artificial neural networks to generate testable hypotheses for animal research and the role of context are discussed.

Frequency-range discriminations and absolute pitch in black-capped chickadees (Poecile atricapillus), mountain chickadees (Poecile gambeli), and zebra finches (Taeniopygia guttata).

The acoustic frequency ranges in birdsongs provide important absolute pitch cues for the recognition of conspecifics. Black-capped chickadees (Poecile atricapillus), mountain chickadees (Poecile gambeli), and zebra finches (Taeniopygia guttata) were trained to sort tones contiguous in frequency into 8 ranges on the basis of associations between response to the tones in each range and reward. All 3 species acquired accurate frequency-range discriminations, but zebra finches acquired the discrimination in fewer trials and to a higher standard than black-capped or mountain chickadees, which did not differ appreciably in the discrimination. Chickadees' relatively poorer accuracy was traced to poorer discrimination of tones in the higher frequency ranges. During transfer tests, the discrimination generalized to novel tones when the training tones were included, but not when they were omitted.

Artificial neural network discrimination of black-capped chickadee (Poecile atricapillus) call notes.

Artificial neural networks were trained to discriminate between two different notes from the "chick-a-dee" call of the black-capped chickadee (Poecile atricapillus). An individual note was represented as a vector of nine summary features taken from note spectrograms. A network was trained to respond to exemplar notes of one type (e.g., A notes) and to fail to respond to exemplar notes of another type (e.g., B notes). After this training, the network was presented novel notes of the two different types, as well as notes of the same two types that had been shifted upwards or downwards in frequency. The strength of the response of the network to each novel and shifted note was recorded. When network responses were plotted as a function of the degree of frequency shift, the results were very similar to those observed in birds that were trained in an analogous task [Charrier et al., J. Comp. Psychol. 119(4), 371-380 (2005)]. The implications of these results to simulating behavioral studies of animal communication are discussed.

Statistical classification of black-capped (Poecile atricapillus) and mountain chickadee (Poecile gambeli) call notes.

Both black-capped (Poecile atricapillus) and mountain chickadees (Poecile gambeli) produce a chick-a-dee call that consists of several distinct note types. In some regions, these 2 species live sympatrically, and it has been shown that 1 species will respond weakly to songs of the other. This suggests that chickadee song, and potentially other of their vocalizations, contains species-specific information. We tested the possibility that call notes were acoustically sufficient for species identification. Black-capped and mountain non-D notes were summarized as a set of 9 features and then analyzed by linear discriminant analysis. Linear discriminant analysis was able to use these notes to identify species with 100% accuracy. We repeated this approach, but with black-capped and mountain D notes that were summarized as a set of 4 features. Linear discriminant analysis was able to use these notes to identify species with 94% accuracy. This demonstrates that any of the note types in these chickadee calls possesses sufficient information for species classification.

Acoustic mechanisms of note-type perception in black-capped chickadee (Poecile atricapillus) calls.

Acoustic communication in black-capped chickadees (Poecile atricapillus) has been studied intensively, the "chick-a-dee" call being among the most well described. This call consists of 4 note types; chickadees perceive these notes as open-ended categories and do so in a continuous manner, with As more similar to Bs and Bs more similar to Cs. Acoustic features contributing to the note-type differentiation are unknown. Recent analyses suggested that certain acoustic features may play a role in note-type classification. Here, the authors tested black-capped chickadees in an operant-conditioning paradigm to determine which features were controlling note-type perception. The results suggest that the note pitch and the frequency modulation in the initial portion of the note control the perception of note types.

Spatial encoding in mountain chickadees: features overshadow geometry.

Encoding the global geometric shape of an enclosed environment is a principal means of orientation in human and non-human animals. Animals spontaneously encode the geometry of an enclosure even when featural information is available. Although features can be used, they typically do not overshadow geometry. However, all previously tested organisms have been reared in human-made environments with salient geometrical cues. Here, we show that wild-caught mountain chickadees (Poecile gambeli) do not spontaneously encode the geometry of an enclosure when salient features are present near the goal. However, chickadees trained without salient features encode geometric information, but this encoding is overshadowed by features.

Effects of songs and calls on ZENK expression in the auditory telencephalon of field- and isolate-reared black capped chickadees.

We examined the effects of hearing two different conspecific vocalizations on expression of the immediate-early gene ZENK in the caudomedial neostriatum (NCM) and the caudomedial portion of the ventral hyperstriatum (cmHV) in male and female black-capped chickadees (Poecile atricapilla). Both the fee-bee song and the chick-a-dee call induced Zenk protein expression in NCM and in cmHV, however, patterns of expression to songs and calls varied across brain region. In the dorsal region of NCM, fee-bee songs induced more Zenk expression than chick-a-dee calls. In ventral NCM and cmHV, Zenk expression did not differ between songs and calls. We found that sex of the listener also affected Zenk expression: there was more robust ZENK response in males than in females. Finally, we compared field- and isolate-reared chickadees and found similar Zenk expression to fee-bee song in each group. These findings indicated that the type of conspecific vocalization, as well as the sex of the listener, appear to modulate IEG expression in the songbird ascending auditory pathway.

Open-ended categorization of chick-a-dee calls by black-capped chickadees (Poecile atricapilla).

The authors trained black-capped chickadees (Poecile atricapilla) in an operant discrimination with exemplars of black-capped and Carolina chick-a-dee calls, with the goal of determining whether the birds memorized the calls of conspecifics and heterospecifics or classified the calls by species. Black-capped calls served as both rewarded (S+) and unrewarded (S-) stimuli (the within-category discrimination), whereas Carolina chick-a-dee calls served as S-s (the between-category discrimination) in the black-capped chick-a-dee call S+ group. The Carolina call S+ group had Carolina calls as S+s and S-s (within-category) and black-capped calls as S-s (between-category). Both groups discriminated between call categories faster than within a call category. In 2 subsequent experiments, both S+ groups showed transfer to novel calls and propagation back to between-category calls. The results favor the hypothesis that the acoustically similar social calls of the 2 species constitute separate open-ended categories.