Distributed recognition of natural songs by European starlings

Individual vocal recognition behaviors in songbirds provide an excellent framework for the investigation of comparative psychological and neurobiological mechanisms that support the perception and cognition of complex acoustic communication signals. To this end, the complex songs of European starlings have been studied extensively. Yet, several basic parameters of starling individual vocal recognition have not been assessed. Here we investigate the temporal extent of song information acquired by starlings during vocal recognition learning. We trained two groups of starlings using standard operant conditioning techniques to recognize several songs from two conspecific male singers. In the first experiment we tested their ability to maintain accurate recognition when presented with (1) random sequences of 1–12 motifs (stereotyped song components) drawn from the training songs, and (2) 0.1–12-s excerpts of continuous song drawn from the training songs. We found that song recognition improved monotonically as more vocal material is provided. In the second experiment, we systematically substituted continuous, varying length regions of white noise for portions of the training songs and again examined recognition accuracy. Recognition remained above chance levels for all noise substitutions tested (up to 91% of the training stimulus) although all but the smallest substitutions led to some decrement in song recognition. Overall, above chance recognition could be obtained with surprisingly few motifs, short excerpts of song, and in the absence of large portions of the training songs. These results suggest that starlings acquire a representation of song during individual vocal recognition learning that is robust to perturbations and distributed broadly over large portions of these complex acoustic sequences.     

Sequential learning and rule abstraction in Bengalese finches

The Bengalese finch (Lonchura striata var. domestica) is a species of songbird. Males sing courtship songs with complex note-to-note transition rules, while females discriminate these songs when choosing their mate. The present study uses serial reaction time (RT) to examine the characteristics of the Bengalese finches’ sequential behaviours beyond song production. The birds were trained to produce the sequence with an “A–B–A” structure. After the RT to each key position was determined to be stable, we tested the acquisition of the trained sequential response by presenting novel and random three-term sequences (random test). We also examined whether they could abstract the embedded rule in the trained sequence and apply it to the novel test sequence (abstract test). Additionally, we examined rule abstraction through example training by increasing the number of examples in baseline training from 1 to 5. When considered as (gender) groups, training with 5 examples resulted in no statistically significant differences in the abstract tests, while statistically significant differences were observed in the random tests, suggesting that the male birds learned the trained sequences and transferred the abstract structure they had learned during the training trials. Individual data indicated that males, as opposed to females, were likely to learn the motor pattern of the sequence. The results are consistent with observations that males learn to produce songs with complex sequential rules, whereas females do not.     

Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury.

Adult male zebra finches (Taeniopygia guttata), as closed-ended learners, normally crystallize their songs at 90 days of age, and the song remains fixed throughout life (Price, 1979). We show that injuring the tracheosyringeal nerve(s) (each of which innervates the ipsilateral half of the syrinx, the avian vocal organ) results in a short-term deficit in the syllables forming adult male song; this deficit disappears after ts nerve regeneration. However, when adult males were followed for a period of several weeks after unilateral tracheosyringeal nerve injury, long-term changes occurred in the temporal patterning of song. Syllables were deleted, remaining portions of the song were linked, and new syllables were added. Syllables with call-like morphology were less likely to be deleted from and more likely to be added to the song. Deletions were most often contiguous chunks of syllables. Changes in the temporal patterning of song occurred during specific periods following nerve injury, were completed within 100 days after nerve transection, and were not dependent upon regeneration of the ts nerve. The resulting newly formed song patterns were stable, remaining unchanged up to 1 year later. The ability of adult male zebra finches to make specific types of changes to crystallized song indicates that some form of vocal plasticity remains even after song learning is completed, though this plasticity may be restricted to a subset of song characteristics. The limitations on the types of changes that are possible may reflect how song is centrally organized.     

Learning to pause: Fidelity of and biases in the developmental acquisition of gaps in the communicative signals of a songbird

The temporal organization of sounds used in social contexts can provide information about signal function and evoke varying responses in listeners (receivers). For example, music is a universal and learned human behavior that is characterized by different rhythms and tempos that can evoke disparate responses in listeners. Similarly, birdsong is a social behavior in songbirds that is learned during critical periods in development and used to evoke physiological and behavioral responses in receivers. Recent investigations have begun to reveal the breadth of universal patterns in birdsong and their similarities to common patterns in speech and music, but relatively little is known about the degree to which biological predispositions and developmental experiences interact to shape the temporal patterning of birdsong. Here, we investigated how biological predispositions modulate the acquisition and production of an important temporal feature of birdsong, namely the duration of silent pauses (“gaps”) between vocal elements (“syllables”). Through analyses of semi-naturally raised and experimentally tutored zebra finches, we observed that juvenile zebra finches imitate the durations of the silent gaps in their tutor's song. Further, when juveniles were experimentally tutored with stimuli containing a wide range of gap durations, we observed biases in the prevalence and stereotypy of gap durations. Together, these studies demonstrate how biological predispositions and developmental experiences differently affect distinct temporal features of birdsong and highlight similarities in developmental plasticity across birdsong, speech, and music.

Research Highlights

• The temporal organization of learned acoustic patterns can be similar across human cultures and across species, suggesting biological predispositions in acquisition.
• We studied how biological predispositions and developmental experiences affect an important temporal feature of birdsong, namely the duration of silent intervals between vocal elements (“gaps”).
• Semi-naturally and experimentally tutored zebra finches imitated the durations of gaps in their tutor's song and displayed some biases in the learning and production of gap durations and in gap variability.
• These findings in the zebra finch provide parallels with the acquisition of temporal features of speech and music in humans.

     

Pavlovian conditioning and rule learning

The experiment reviewed here was an attempt to show that two differential Pavlovian conditioning designs, namely positive and negative patterning, can best be understood as rule learning. First, it is shown that positive patterning is equivalent to the logical rule of conjunction (AND) and that negative patterning is equivalent to the logical rule of exclusive disjunction (XOR). It is assumed that in order to learn both kinds of discrimination subjects learn to use the according rule. If this is the case, the observed differentiation should be independent of the number of reinforcements for each individual stimulus. Second, subjects should be able to transfer the rule to new stimuli. Forty human subjects were randomly divided into four groups (N=10 each). Two factors were manipulated independently between subjects: (1) positive vs negative patterning, and (2) 2 vs 4 pairs of trained stimuli. Second interval skin conductance responses were measured. During initial acquisition positive as well as negative patterning occurred independently of number of pairs of trained stimuli (with total amount of training kept constant). Furthermore, AND as well as XOR could be transfered to new stimuli.     

The profile of abstract rule learning in infancy: Meta‐analytic and experimental evidence

Everyone agrees that infants possess general mechanisms for learning about the world, but the existence and operation of more specialized mechanisms is controversial. One mechanism—rule learning—has been proposed as potentially specific to speech, based on findings that 7‐month‐olds can learn abstract repetition rules from spoken syllables (e.g. ABB patterns: wo‐fe‐fe, ga‐tu‐tu…) but not from closely matched stimuli, such as tones. Subsequent work has shown that learning of abstract patterns is not simply specific to speech. However, we still lack a parsimonious explanation to tie together the diverse, messy, and occasionally contradictory findings in that literature. We took two routes to creating a new profile of rule learning: meta‐analysis of 20 prior reports on infants’ learning of abstract repetition rules (including 1,318 infants in 63 experiments total), and an experiment on learning of such rules from a natural, non‐speech communicative signal. These complementary approaches revealed that infants were most likely to learn abstract patterns from meaningful stimuli. We argue that the ability to detect and generalize simple patterns supports learning across domains in infancy but chiefly when the signal is meaningfully relevant to infants’ experience with sounds, objects, language, and people.     

Perceptual organization of auditory temporal patterns in European starlings (Sturnus vulgaris)

The perception of continuously repeating auditory patterns by European starlings was explored in seven experiments. In Experiment 1, 4 starlings learned to discriminate between two continuously repeating, eight-element, auditory patterns. Each eight-element pattern was constructed from different temporal organizations of two elements differing in timbre. In Experiments 2–7, the repeating patterns were transformed in ways designed to identify the starlings’ perceptual organization of the patterns. In Experiment 2, the starlings identified patterns beginning with novel starting points. In Experiment 3, discrimination performance was adversely affected by reorganizing the elements in the patterns. In Experiments 4 and 5, the pattern elements were altered. In Experiment 4, the patterns were constructed from two novel elements. In Experiment 5, the temporal location of the two pattern elements was reversed. The transformations of the patterns in Experiments 4 and 5 affected discrimination performance for some, but not all, of the starlings. In Experiments 6 and 7, replacing either of the two elements with silent intervals had no effect on discrimination performance. The results of these experiments identify basic grouping principles that starlings use when they perceive auditory patterns.     

Information from multiple modalities helps 5‐month‐olds learn abstract rules

By 7 months of age, infants are able to learn rules based on the abstract relationships between stimuli ( Marcus et al ., 1999 ), but they are better able to do so when exposed to speech than to some other classes of stimuli. In the current experiments we ask whether multimodal stimulus information will aid younger infants in identifying abstract rules. We habituated 5‐month‐olds to simple abstract patterns (ABA or ABB) instantiated in coordinated looming visual shapes and speech sounds (Experiment 1), shapes alone (Experiment 2), and speech sounds accompanied by uninformative but coordinated shapes (Experiment 3). Infants showed evidence of rule learning only in the presence of the informative multimodal cues. We hypothesize that the additional evidence present in these multimodal displays was responsible for the success of younger infants in learning rules, congruent with both a Bayesian account and with the Intersensory Redundancy Hypothesis.     

Spontaneous generalization of abstract multimodal patterns in young domestic chicks

From the early stages of life, learning the regularities associated with specific objects is crucial for making sense of experiences. Through filial imprinting, young precocial birds quickly learn the features of their social partners by mere exposure. It is not clear though to what extent chicks can extract abstract patterns of the visual and acoustic stimuli present in the imprinting object, and how they combine them. To investigate this issue, we exposed chicks (Gallus gallus) to three days of visual and acoustic imprinting, using either patterns with two identical items or patterns with two different items, presented visually, acoustically or in both modalities. Next, chicks were given a choice between the familiar and the unfamiliar pattern, present in either the multimodal, visual or acoustic modality. The responses to the novel stimuli were affected by their imprinting experience, and the effect was stronger for chicks imprinted with multimodal patterns than for the other groups. Interestingly, males and females adopted a different strategy, with males more attracted by unfamiliar patterns and females more attracted by familiar patterns. Our data show that chicks can generalize abstract patterns by mere exposure through filial imprinting and that multimodal stimulation is more effective than unimodal stimulation for pattern learning.     

The effect of motion on tactile and visual temporal order judgments

Four experiments were conducted, three with tactile stimuli and one with visual stimuli, in which subjects made temporal order judgments (TOJs). The tactile stimuli were patterns that moved laterally across the fingerpads. The subject's task was to judge which finger received the pattern first. Even though the movement was irrelevant to the task, the subjects' TOJs were greatly affected by the direction of movement of the patterns. Accuracy in judging temporal order was enhanced when the patterns moved in a direction that was consistent with the temporal order of presentation--for example, when the movement on each fingerpad was from right to left and the temporally leading site of stimulation was to the right of the temporally trailing site of stimulation. When movement was inconsistent with the temporal order of presentation, accuracy was considerably reduced, often well below chance.The bias in TOJs was unaffected by training or by presenting the stimuli to fingers on opposite hands. In a fourth experiment, subjects judged the temporal order of visual stimuli that, like the tactile stimuli, moved in a direction that was either consistent or inconsistent with the TOJ. The results were similar to those obtained with tactile stimuli. It is suggested that the bias may be affected by attentional mechanisms and by apparent motion generated between the two sites on the skin.     

Probing the Time Course of Nonlinear Discriminations during Human Electrodermal Conditioning

Animal-based theories of Pavlovian conditioning propose that patterning discriminations are solved using unique cues or immediate configuring. Recent studies with humans, however, provided evidence that in positive and negative patterning two different rules are utilized. The present experiment was designed to provide further support for this proposal by tracking the time course of the allocation of cognitive resources. One group was trained in a positive patterning schedule (A−, B−, AB+) and a second in a negative patterning schedule (A+, B+, AB−). Electrodermal responses and secondary task probe reaction time were measured. In negative patterning, reaction times were slower during reinforced stimuli than during nonreinforced stimuli at both probe positions while there were no differences in positive patterning. These results support the assumption that negative patterning is solved using a rule that is more complex and requires more resources than does the rule employed to solve positive patterning.     

Robustness of the rule-learning effect in 7-month-old infants: A close,multicenter replication of Marcus et al. (1999)

We conducted a close replication of the seminal work by Marcus and colleagues from 1999, which showed that after a brief auditory exposure phase, 7-month-old infants were able to learn and generalize a rule to novel syllables not previously present in the exposure phase. This work became the foundation for the theoretical framework by which we assume that infants are able to learn abstract representations and generalize linguistic rules. While some extensions on the original work have shown evidence of rule learning, the outcomes are mixed, and an exact replication of Marcus et al.'s study has thus far not been reported. A recent meta-analysis by Rabagliati and colleagues brings to light that the rule-learning effect depends on stimulus type (e.g., meaningfulness, speech vs. nonspeech) and is not as robust as often assumed. In light of the theoretical importance of the issue at stake, it is appropriate and necessary to assess the replicability and robustness of Marcus et al.'s findings. Here we have undertaken a replication across four labs with a large sample of 7-month-old infants (N = 96), using the same exposure patterns (ABA and ABB), methodology (Headturn Preference Paradigm), and original stimuli. As in the original study, we tested the hypothesis that infants are able to learn abstract “algebraic” rules and apply them to novel input. Our results did not replicate the original findings: infants showed no difference in looking time between test patterns consistent or inconsistent with the familiarization pattern they were exposed to.     

Configural olfactory learning in honeybees: negative and positive patterning discrimination

In an appetitive context, honeybees (Apis mellifera) learn to associate odors with a reward of sucrose solution. If an odor is presented immediately before the sucrose, an elemental association is formed that enables the odor to release the proboscis extension response (PER). Olfactory conditioning of PER was used to study whether, beyond elemental associations, honeybees are able to process configural associations. Bees were trained in a positive and anegative patterning discrimination problem. In the first problem, single odorants were nonreinforced whereas the compound was reinforced. In the second problem, single odorants were reinforced whereas the compound was nonreinforced. We studied whether bees can solve these problems and whether the ratio between the number of presentations of the reinforced stimuli and the number of presentations of the nonreinforced stimuli affects discrimination. Honeybees differentiated reinforced and nonreinforced stimuli in positive and negative patterning discriminations. They thus can process configural associations. The variation of the ratio of reinforced to nonreinforced stimuli modulated the amount of differentiation. The assignment of singular codes to complex odor blends could be implemented at the neural level: When bees are stimulated with odor mixtures, the activation patterns evoked at the primary olfactory neuropile, the antennal lobe, may be combinations of the single odorant responses that are not necessarily fully additive.     

Free-flying honeybees extrapolate relational size rules to sort successively visited artificial flowers in a realistic foraging situation

Learning and applying relational concepts to solve novel tasks is considered an indicator of cognitive-like ability. It requires the abstraction of relational concepts to different objects independent to the physical nature of the individual objects. Recent research has revealed the honeybee’s ability to rapidly learn and manipulate relations between visual stimuli such as ‘same/different’, ‘above/below’, or ‘larger/smaller’ despite having a miniature-sized brain. While honeybees can solve problems using rule-based relative size comparison, it remains unresolved as to whether bees can apply size rules when stimuli are encountered successively, which requires reliance on working memory for stimuli comparison. Additionally, the potential ability of bees to extrapolate acquired information to novel sizes beyond training sets remains to be investigated. We tested whether individual free-flying honeybees could learn ‘larger/smaller’ size rules when visual stimuli were presented successively, and whether such rules could then be extrapolated to novel stimulus sizes. Honeybees were individually trained to a set of four sizes such that individual elements might be correct, or incorrect, depending upon the alternative stimulus. In a learning test, bees preferred the correct size relation for their respective learning group. Bees were also able to successfully extrapolate the learnt relation during transfer tests by maintaining the correct size relationships when considering either two smaller, or two larger, novel stimulus sizes. This performance demonstrates that an insect operating in a complex environment has sufficient cognitive capacity to learn rules that can be abstracted to novel problems. We discuss the possible learning mechanisms which allow their success.     

The effects of intensity and interval rhythms on the perception of auditory and visual temporal patterns

Repeating temporal patterns were presented in the auditory and visual modalities so that: (a) all elements were of equal intensity and were equally spaced in time (uniform presentation); (b) the intensity of one element was increased (accent presentation); or (c) the interval between two elements was increased (pause presentation). Intensity and interval patterning serve to segment the element sequence into repeating patterns.

For uniform presentation, pattern organization was by pattern structure, with auditory identification being faster. For pause presentation, organization was by the pauses; both auditory and visual identification were twice as fast as for uniform presentation. For auditory accent presentation, organization was by pattern structure and identification was slower than for uniform presentation. In contrast, the organization of visual accent presentation was by accents and identification was faster than for uniform presentation. These results suggest that complex stimuli, in which elements are patterned along more than one sensory dimension, are perceptually unique and therefore their identification rests on the nature of each modality.     

Infants’ representations of same and different in match- and non-match-to-sample

Three experiments investigated the representations that underlie 14-month-old infants’ and adults’ success at match-to-sample (MTS) and non-match-to-sample (NMTS) tasks. In Experiment 1, 14-month-old infants were able to learn rules based on abstract representations of sameness and/or difference. When presented with one of eighteen sample stimuli (A) and a choice between a stimulus that was the same as the sample (A) and a different stimulus (B), infants learned to choose A in MTS and B in NMTS. In Experiments 2 and 3, we began to explore the nature of the representations at play in these paradigms. Experiment 2 confirmed that abstract representations were at play, as infants generalized the MTS and NMTS rules to stimuli unseen during familiarization. Experiment 2 also showed that infants tested in MTS learned to seek the stimulus that was the same as the sample, whereas infants tested in NMTS did not learn to seek the different stimulus, but instead learned to avoid the stimulus that was the same as the sample. Infants appeared to only use an abstract representation of the relation same in these experiments. Experiment 3 showed that adult participants, despite knowing the words “same” and “different”, also relied on representations of sameness in both MTS and NMTS in a paradigm modeled on that of Experiment 2. We conclude with a discussion of how young infants may possibly represent the abstract relation same.     

Direct social contacts override auditory information in the song-learning process in starlings (Sturnus vulgaris)

Social influence on song acquisition was studied in 3 groups of young European starlings raised under different social conditions but with the same auditory experience of adult song. Attentional focusing on preferred partners appears the most likely explanation for differences found in song acquisition in relation to experience, sex, and song categories. Thus, pair-isolated birds learned from each other and not from broadcast live songs, females did not learn from the adult male tutors, and sharing occurred more between socially associated peers. On the contrary, single-isolated birds clearly copied the adult songs that may have been the only source of attention stimulation. Therefore, social preference appears as both a motor for song learning and a potential obstacle for acquisition from nonpreferred partners, including adults.     

Stimulus-dependent flexibility in non-human auditory pitch processing

Songbirds and humans share many parallels in vocal learning and auditory sequence processing. However, the two groups differ notably in their abilities to recognize acoustic sequences shifted in absolute pitch (pitch height). Whereas humans maintain accurate recognition of words or melodies over large pitch height changes, songbirds are comparatively much poorer at recognizing pitch-shifted tone sequences. This apparent disparity may reflect fundamental differences in the neural mechanisms underlying the representation of sound in songbirds. Alternatively, because non-human studies have used sine-tone stimuli almost exclusively, tolerance to pitch height changes in the context of natural signals may be underestimated. Here, we show that European starlings, a species of songbird, can maintain accurate recognition of the songs of other starlings when the pitch of those songs is shifted by as much as ±40%. We observed accurate recognition even for songs pitch-shifted well outside the range of frequencies used during training, and even though much smaller pitch shifts in conspecific songs are easily detected. With similar training using human piano melodies, recognition of the pitch-shifted melodies is very limited. These results demonstrate that non-human pitch processing is more flexible than previously thought and that the flexibility in pitch processing strategy is stimulus dependent.     

From central pattern generator to sensory template in the evolution of birdsong

Central nervous networks, be they a part of the human brain or a group of neurons in a snail, may be designed to produce distinct patterns of movement. Central pattern generators can account for the development and production of normal vocal signals without auditory feedback in non-songbirds. Songbirds need auditory feedback to develop and maintain the normal song of their species. The prerequisite for the use of auditory feedback for the control of song is a set of acoustic criteria or a template to which voice must match. The template method perhaps evolved to free birds from fixed central pattern generators, resulting in the evolution of diverse and complex songs among oscine songbirds. The evolution of human speech may have followed a similar course.     

Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in aplysia

In Aplysia, three distinct phases of memory for sensitization can be dissociated based on their temporal and molecular features. A single training trial induces short-term memory (STM, lasting <30 min), whereas five trials delivered at 15-min intervals induces both intermediate-term memory (ITM, lasting >90 min) and long-term memory (LTM, lasting >24 h). Here, we explore the interaction of amount and pattern of training in establishing ITM and LTM by examining memory for sensitization after different numbers of trials (each trial = one tail shock) and different patterns of training (massed vs. spaced). Under spaced training patterns, two trials produced STM exclusively, whereas four or five trials each produced both ITM and LTM. Three spaced trials failed to induce LTM but did produce an early decaying form of ITM (E-ITM) that was significantly shorter and weaker in magnitude than the late-decaying ITM (L-ITM) observed after four to five trials. In addition, E-ITM was induced after three trials with both massed and spaced patterns of training. However, L-ITM and LTM after four to five trials require spaced training: Four or five massed trials failed to induce LTM and produced only E-ITM. Collectively, our results indicate that in addition to three identified phases of memory for sensitization—STM, ITM, and LTM—a unique temporal profile of memory, E-ITM, is revealed by varying either the amount or pattern of training.