Mechanisms of call note-type perception in black-capped chickadees (Poecile atricapillus): Peak shift in a note-type continuum.

We report on operant conditioning and artificial neural network (ANN) simulations aimed at further elucidating mechanisms of black-capped chickadee chick-a-dee call note category perception. Specifically, we tested for differences in the speed of acquisition among different discrimination tasks and, in two selected discrimination groups, searched for evidence of peak shift. Earlier, unreported ANN data were instrumental in providing the motivation for the current set of studies with chickadees and are provided here. The ANNs revealed differences in the speed of learning among note-type discrimination groups that is related to the degree of perceptual similarity among the three note types tested (i.e., A, B, and C notes). In many respects, bird and network results were in agreement (i.e., in the observation of peak shift in the same group), but they also differed in important ways (i.e., all discrimination groups showed differences in speed of learning in simulations but not in chickadees). We suggest that the start, peak and end frequency of the chick-a portion of chick-a-dee call notes, which form a graded but overlapping continuum, may drive the peak shift observed. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Song sequence discrimination in the black-capped chickadee (Parus atricapillus).

14 captive black-capped chickadees were presented with normal and altered versions of their species-specific "fee bee" song to determine how note type, number, and sequence affect recognition. Perch changes and vocalizations given in response to playback did not differ reliably as a function of song type, whereas latency to 1st vocalization after playback did. In Exp I, using 2-note songs, Ss vocalized sooner to songs beginning with fee than with bee and to fee bee than to fee fee. In Exp II, Ss were presented with single-note, normal, and 3-note songs each consisting of a single-note type. Habituation slowed responding to altered songs but not to fee bee over 3 test sessions. Results suggest that Ss distinguished (a) single fees and 3-note songs from normal song, (b) single fees from single bees, (c) 2-note songs from 3-note songs, and (d) normal song from altered songs. It is concluded that the internal representation of conspecific song in the chickadee distinguishes between fee and bee notes, contains information about note order, and is sensitive to note number. The pattern of responses is consistent with a model of recognition based on note-by-note integration of individual decisions about song structure. (34 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Black-capped chickadees (Poecile atricapillus) anticipate future outcomes of foraging choices.

In 2 experiments we investigated the cognitive abilities of wild-caught black-capped chickadees (Poecile atricapillus) in future anticipation tasks. Chickadees were sensitive to anticipatory contrast effects over time horizons of 5, 10, and 30 min (Experiment 1). Chickadees also learned the order of events and anticipated that the quality of future foraging outcomes was contingent on current foraging choices. This behavior was demonstrated while foraging in a naturalistic aviary environment with a 30-min delay between the initial choice and the future outcome (Experiment 2). These results support the hypothesis that black-capped chickadees can cognitively travel in time both retrospectively and prospectively using episodic memory. This result shows the occurrence of anticipatory cognition in a noncorvid species of food-storing bird and supports the idea that cognitive time travel may have evolved in nonhuman animals in response to specific ecological selection pressures. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

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. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Neuron Production, Neuron Number, and Structure Size Are Seasonally Stable in the Hippocampus of the Food-Storing Black-Capped Chickadee (Poecile atricapillus).

Neuronal recruitment in the black-capped chickadee (Poecile atricapillus) hippocampus occurs at a higher rate in the fall than at other times of the year. As a means of determining whether this increase in recruitment results from greater neuron production, chickadees were caught in the wild between October and March and injected with the cell-birth marker 5-bromo-2'-deoxyuridine. Two weeks later, birds were killed by overdose, and hippocampal neuron production, apoptosis, neuron number, and hippocampal volume were determined. Chickadees collected in October, November, January, February, and March did not differ in neuron production, apoptosis, hippocampal volume, or neuron number. These findings indicate that increases in neuronal recruitment in the chickadee hippocampus in the fall do not result from increased neuron production, but instead, enhanced survival of new neurons. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Long-Term Memory for Spatial Locations in a Food-Storing Bird (Poecile atricapilla) Requires Activation of NMDA Receptors in the Hippocampal Formation During Learning.

Food-storing birds use a form of long-term memory to recover their hidden food caches that depends on the hippocampal formation (HF). The authors assessed whether food-storing birds' long-term memory for spatial locations requires N-methyl-D-aspartate receptor (NMDA-R)-dependent synaptic plasticity. Black-capped chickadees (Poecile atricapilla) were given bilateral infusions of the NMDA-R antagonist AP5 into the hippocampus, and their memory on a spatial reference memory task was assessed. NMDA-R inactivation during learning prevented formation of long-term spatial memories but did not affect short-term memory and retrieval processes. NMDA-R inactivation immediately following learning did not disrupt long-term memory formation. NMDA-R inactivation disrupted the learning of multiple serially encoded reward locations when a 180-min delay separated successive learning episodes, suggesting that NMDA-R activity has a role in the incorporation of new information into existing long-term memory, as well as in forming unitary long-term memories. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Auditory Categorization of Complex Sounds by Rats (Rattus norvegicus).

Little research has explored the auditory categorization abilities of mammals. To better understand these processes, the authors tested the abilities of rats (Rattus norvegicus) to categorize multidimensional acoustic stimuli by using a classic category-learning task developed by R. N. Shepard, C. I. Hovland, and H. M. Jenkins (1961). Rats proved to be able to categorize 8 complex sounds on the basis of either the direction or rate of frequency modulation but not on the basis of the range of frequency modulation. Rats' categorization abilities were limited but improved slowly and incrementally, suggesting that learning was not facilitated by selective attention to acoustic dimensions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Divided attention, memory, and spatial discrimination in food-storing and nonstoring birds, black-capped chickadees ( Poecile atricapilla) and dark-eyed Juncos ( Junco hyemalis).

Food-storing birds, black-capped chickadees (Poecile atricapilla), and nonstoring birds, dark-eyed juncos (Junco hyemalis), matched color or location on a touch screen. Both species showed a divided attention effect for color but not for location (Experiment 1). Chickadees performed better on location than on color with retention intervals up to 40 s, but juncos did not (Experiment 2). Increasing sample-distractor distance improved performance similarly in both species. Multidimensional scaling revealed that both use a Euclidean metric of spatial similarity (Experiment 3). When choosing between the location and color of a remembered item, food storers choose location more than do nonstorers. These results explain this effect by differences in memory for location relative to color, not division of attention or spatial discrimination ability. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A Gray Seal's (Halichoerus grypus) Responses to Experimenter-Given Pointing and Directional Cues.

A gray seal (Halichoerus grypus) was trained to touch a target on its left or right by responding to pointing signals. The authors then tested whether the seal would be able to generalize spontaneously to altered signals. It responded correctly to center pointing and head turning, center upper body turning, and off-center pointing but not to head turning and eye movements alone. The seal also responded correctly to brief ipsilateral and contralateral points from center and lateral positions. Pointing gestures did not cause the seal to select an object placed centrally behind it. Like many animals in similar studies, this gray seal probably did not understand the referential character of these gestures but rather used signal generalization and experience from initial operant conditioning to solve these tasks. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Pitch perception in chinchillas (Chinchilla laniger): Stimulus generalization using rippled noise.

Rippled noises evoke the perception of pitch in human listeners. Infinitely iterated rippled noise (IIRN) is generated when wideband noise (WBN) is delayed, attenuated, and added to the original WBN through either a positive (+) or a negative (-) feedback loop. The pitch of IIRN[+] is matched to the reciprocal of the delay, whereas the pitch of IIRN[-] for the same delay is an octave lower. Chinchillas (Chinchilla laniger) were trained to discriminate IIRN[+] with a 4-ms delay from IIRN[+] with a 2-ms delay and then tested in a stimulus generalization paradigm with IIRN[+] at delays between 2 and 4 ms. Systematic gradients in behavioral response occurred along the dimension of delay, suggesting that a perceptual dimension corresponding to pitch exists for IIRN[+]. Behavioral responses to IIRN[-] test stimuli were more variable among chinchillas, suggesting that IIRN[-] did not evoke similar pitches relative to IIRN[+]. Systematic gradients in behavioral response were observed when IIRN[-] test stimuli were presented in the context of other IIRN[-] stimuli. Thus, other perceptual cues such as timbre may dominate the pitch cues when IIRN[-] test stimuli are presented in the context of IIRN[+] stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A test of the adaptive specialization hypothesis: Population differences in caching, memory, and the hippocampus in black-capped chickadees (Poecile atricapilla).

To test the hypothesis that accurate cache recovery is more critical for birds that live in harsh conditions where the food supply is limited and unpredictable, the authors compared food caching, memory, and the hippocampus of black-capped chickadees (Poecile atricapilla) from Alaska and Colorado. Under identical laboratory conditions, Alaska chickadees (a) cached significantly more food; (b) were more efficient at cache recovery; (c) performed more accurately on one-trial associative learning tasks in which birds had to rely on spatial memory, but did not differ when tested on a nonspatial version of this task; and (d) had significantly larger hippocampal volumes containing more neurons compared with Colorado chickadees. The results support the hypothesis that these population differences may reflect adaptations to a harsh environment. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Interpreting the effects of image manipulation on picture perception in pigeons (Columba livia) and humans (Homo sapiens).

The effects of picture manipulations on humans' and pigeons' performance were examined in a go/no-go discrimination of two perceptually similar categories, cat and dog faces. Four types of manipulation were used to modify the images. Mosaicization and scrambling were used to produce degraded versions of the training stimuli, while morphing and cell exchange were used to manipulate the relative contribution of positive and negative training stimuli to test stimuli. Mosaicization mainly removes information at high spatial frequencies, whereas scrambling removes information at low spatial frequencies to a greater degree. Morphing leads to complex transformations of the stimuli that are not concentrated at any particular spatial frequency band. Cell exchange preserves high spatial frequency details, but sometimes moves them into the “wrong” stimulus. The four manipulations also introduce high-frequency noise to differing degrees. Responses to test stimuli indicated that high and low spatial frequency information were both sufficient but not necessary to maintain discrimination performance in both species, but there were also species differences in relative sensitivity to higher and lower spatial frequency information. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Enantioselectivity of odor perception in honeybees (Apis mellifera carnica).

The authors tested the ability of 60 free-flying honeybees (Apis mellifera carnica) to discriminate a conditioning odor from an array of 26 simultaneously presented substances. The stimuli included 10 pairs of enantiomers and 6 essential oils. The bees (a) significantly distinguished between 98% of the 540 odor pairs tested, thus showing an excellent overall discrimination performance, and (b) were able to discriminate between the optical isomers of limonene, α-pinene, β-citronellol, menthol, and carvone but failed to distinguish between the (+)- and (–)- forms of α-terpineol, camphor, rose oxide, fenchone, and 2-butanol. The findings support the assumptions that enantioselective molecular odor receptors may exist only for some volatile enantiomers and that insects and mammals may share common principles of odor quality perception, irrespective of their completely differing repertoires of olfactory receptors. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Acoustic interactions in broods of nestling birds (Tachycineta bicolor).

Studies of acoustic interactions in animal groups, such as chorusing insects, anurans, and birds, have been invaluable in showing how cooperation and competition shape signal structure and use. The begging calls of nestling birds are ideal for such studies, because they function both as a cooperative signals of the brood's needs and as competitive signals for parental allocation within the brood. Nonetheless, studies of acoustic interactions among nestlings are rare. Here we review our work on acoustic interactions in nestling tree swallows (Tachycineta bicolor), especially how calls are used in competition for parental feedings. Nestlings attracted parental attention and responded to acoustic interference mainly by increasing call output. However, nestlings also gave more similar calls when they called together and decreased their call bandwidth when exposed to elevated noise. We suggest that these competitive uses of calls might intensify the cooperative brood signal, affecting both parental provisioning and vocal development. Given their tremendous variation across species, begging calls offer promising opportunities for developmental and comparative studies of acoustic signaling. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Sex differences in audiovisual discrimination learning by Bengalese Finches (Lonchura striata var. domestica).

Both visual and auditory information are important for songbirds, especially in developmental and sexual contexts. To investigate bimodal cognition in songbirds, the authors conducted audiovisual discrimination training in Bengalese finches. The authors used two types of stimulus: an artificial stimulus, which is a combination of simple figures and sound, and a biological stimulus, consisting of video images of singing males along with their songs. The authors found that while both sexes predominantly used visual cues in the discrimination tasks, males tended to be more dependent on auditory information for the biological stimulus. Female responses were always dependent on the visual stimulus for both stimulus types. Only males changed their discrimination strategy according to stimulus type. Although males used both visual and auditory cues for the biological stimulus, they responded to the artificial stimulus depending only on visual information, as the females did. These findings suggest a sex difference in innate auditory sensitivity. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Spatial memory of food-storing tits (Parus ater and P. atricapillus): Comparison of storing and nonstoring tasks.

We compared food-storing tits' memory for the locations of items they had stored and of food they had only seen. Experiment 1 showed that after 1.5–2 hrs black-capped chickadees (Parus atricapillus) and coal tits (P. ater) are better at discriminating between sites where they have stored a seed and ones simply visited than at discriminating between sites where they have seen a seed behind a window and ones visited. In Experiment 2, we compared chickadees' accuracy of return after 1.5 hrs to either seeds behind windows or seeds without windows in front of them. The probability of returning to seeds behind windows was lower than that of returning to stored seeds, but stored seeds and seeds without windows were visited with equal probability. In Experiment 3, neither stored seeds nor seeds without windows were forgotten after 26 hrs. The results are consistent with suggestions that memory for stored food is subserved by the same memory system as that for encountered food. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Classical tone-shock conditioning induces zenk expression in the pigeon (Columba livia) hippocampus.

The hippocampus is involved in fear conditioning, although the molecular events underlying this function are still under investigation. The authors analyzed the expression of the Zenk proto-oncogene product within the pigeon (Columba livia) hippocampus after training with a classical aversive conditioning protocol using tone-shock associations. Control groups were trained with shock or tone alone or were only exposed to the experimental chamber and manipulated. Experimental pigeons showed significant increases of Zenk expression in the ventromedial region of the hippocampus, whereas both the experimental and shock groups had increased Zenk expression in the dorsal region. The expression of Zenk in specific neuronal populations within the pigeon hippocampus may be indicative of plasticity-associated aversive classical conditioning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)