Hemispheric differences in processing of vocalizations depend on early experience

Phan, Mimi L.; Vicario, David S.

doi:10.1073/pnas.0900091107

Cited by 61 publications

(64 citation statements)

References 37 publications

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“…Structures in the songbird forebrain that could be involved in the top-down process include (i) vocal motor structures, e.g., HVC and the lateral magnocellular nucleus of the anterior nidopallium, that contribute to vocal learning (27)(28)(29) and perception of grammatical structures (2, 7) and possibly (ii) the hippocampus, involved in statistical learning in vision (30), but not yet explored in songbirds. In any case, the recognition of nonadjacent patterns occurs primarily in the right hemisphere, which is known to have higher responses to conspecific vocalizations and adapt more rapidly than the left hemisphere (31).…”

Section: Discussionmentioning

confidence: 99%

Statistical learning of recurring sound patterns encodes auditory objects in songbird forebrain

Lü

Vicario

2014

Proc. Natl. Acad. Sci. U.S.A.

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Auditory neurophysiology has demonstrated how basic acoustic features are mapped in the brain, but it is still not clear how multiple sound components are integrated over time and recognized as an object. We investigated the role of statistical learning in encoding the sequential features of complex sounds by recording neuronal responses bilaterally in the auditory forebrain of awake songbirds that were passively exposed to long sound streams. These streams contained sequential regularities, and were similar to streams used in human infants to demonstrate statistical learning for speech sounds. For stimulus patterns with contiguous transitions and with nonadjacent elements, single and multiunit responses reflected neuronal discrimination of the familiar patterns from novel patterns. In addition, discrimination of nonadjacent patterns was stronger in the right hemisphere than in the left, and may reflect an effect of top-down modulation that is lateralized. Responses to recurring patterns showed stimulusspecific adaptation, a sparsening of neural activity that may contribute to encoding invariants in the sound stream and that appears to increase coding efficiency for the familiar stimuli across the population of neurons recorded. As auditory information about the world must be received serially over time, recognition of complex auditory objects may depend on this type of mnemonic process to create and differentiate representations of recently heard sounds.multielectrode | electrophysiology | single-unit | memory | novelty A central question in neuroscience is how a sensory system combines the transduced features of a sensory experience into a unitary object that is recognized and available for further processing. In the field of auditory research, progress has been made on the mechanisms that encode basic acoustic features, but it still not clear how multiple sound components are integrated over time and recognized as a single object. A striking example is that, after only 2 min of passive exposure to a continuous stream of artificial words (nonsense sound sequences), infants extract and distinguish these "words" from other sequences based on the transition probability between syllables; this provides an explanation of how actual words may be initially recognized by infants, even though obvious boundaries (e.g., interword pauses) are absent in natural speech (1). Further work with similar passive exposure paradigms showed that human adults and infants could also learn to distinguish consistent but nonadjacent patterns (2, 3), and were thus able to learn invariant relationships despite variable intervening sounds. These experiments demonstrate that the brain can form a record of the recurring patterns in an ongoing stimulus stream. This occurs spontaneously in the absence of reinforcement or of any cues to what should be learned, and is referred to as statistical learning. The ability to extract invariant patterns through passive exposure is not unique to the speech/language system, because behavioral studies with...

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Section: Discussionmentioning

confidence: 99%

Statistical learning of recurring sound patterns encodes auditory objects in songbird forebrain

Lü

Vicario

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…Neurons in the MLd as well as each of the auditory forebrain regions have been shown to respond selectively to CVs, particularly the “auditory association” areas CM and NCM. Moreover, hemispheric specialization has also been observed in the NCM, where CVs evoke larger overall responses in the right hemisphere (e.g., Phan and Vicario, 2010). The songbird brain has additional highly specialized circuitry enabling song production, including the sensory/motor nucleus HVC, which exhibits selectivity for the bird’s own song over other conspecific songs (e.g., Lehongre and Del Negro, 2011; Margoliash, 1986).…”

Section: Neural Representation Of Conspecific Vocalizationsmentioning

confidence: 89%

“…Phan and Vicario (2010) recently investigated the role of auditory experience in shaping hemispheric specialization for CV processing in zebra finches. The auditory environment of the developing finches was manipulated in two ways: a first set of birds was divided into two groups that either received song exposure (“tutored”) or were deprived of normal song during development (“untutored”); a second set of birds was surgically devocalized, rendering them incapable of producing audible vocalizations, and then similarly divided into tutored and untutored groups.…”

Section: The Effects Of Experience In Shaping Neural Responses To mentioning

confidence: 99%

“…There are several differences between the neural substrates of birdsong and the representation of CVs in humans and other mammals that call for caution when drawing inferences about representation of CVs in the mammalian brain from the birdsong literature, such as sex differences (Hauber et al, 2007; Maul et al, 2010; Phan and Vicario, 2010), hormonal influences (Del Negro et al, 2005; Fusani and Gahr, 2006; Tremere and Pinaud, 2011), and differences between songs and other communication vocalizations. However, it is clear in these bird species that significant brain resources are devoted to perception of these sounds, and that experience with the CVs including self-vocalizations plays a significant role in elevating these sounds above others.…”

Section: The Effects Of Experience In Shaping Neural Responses To mentioning

confidence: 99%

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Processing of communication sounds: Contributions of learning, memory, and experience

2013

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Abundant evidence from both field and lab studies has established that conspecific vocalizations (CVs) are of critical ecological significance for a wide variety of species, including humans, nonhuman primates, rodents, and other mammals and birds. Correspondingly, a number of experiments have demonstrated behavioral processing advantages for CVs, such as in discrimination and memory tasks. Further, a wide range of experiments have described brain regions in many species that appear to be specialized for processing CVs. For example, several neural regions have been described in both mammals and birds wherein greater neural responses are elicited by CVs than by comparison stimuli such as heterospecific vocalizations, nonvocal complex sounds, and artificial stimuli. These observations raise the question of whether these regions reflect domain-specific neural mechanisms dedicated to processing CVs, or alternatively, if these regions reflect domain-general neural mechanisms for representing complex sounds of learned significance. Inasmuch as CVs can be viewed as complex combinations of basic spectrotemporal features, the plausibility of the latter position is supported by a large body of literature describing modulated cortical and subcortical representation of a variety of acoustic features that have been experimentally associated with stimuli of natural behavioral significance (such as food rewards). Herein, we review a relatively small body of existing literature describing the roles of experience, learning, and memory in the emergence of species-typical neural representations of CVs and auditory system plasticity. In both songbirds and mammals, manipulations of auditory experience as well as specific learning paradigms are shown to modulate neural responses evoked by CVs, either in terms of overall firing rate or temporal firing patterns. In some cases, CV-sensitive neural regions gradually acquire representation of non-CV stimuli with which subjects have training and experience. These results parallel literature in humans describing modulation of responses in face-sensitive neural regions through learning and experience. Thus, although many questions remain, the available evidence is consistent with the notion that CVs may acquire distinct neural representation through domain-general mechanisms for representing complex auditory objects that are of learned importance to the animal.

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“…This is highly unlikely in zebra finches, as males and females have very different plumage characteristics, and while males sing, females do not. Furthermore, animals ofboth sexes havea largememory capacity for the songs they have heard throughout development (Bolhuis, Zijlstra, den Boer-Visser, & Van Der Zee, 2000;London & Clayton, 2008;Phan & Vicario, 2010). Females choose male mates on the basis of song (Tomaszycki & Adkins-Regan, 2005) and males clearly learn to prefer the physical characteristics of the mother and use these to choose mates in adulthood (Burley, 2006;Vos, 1995).…”

Section: Discussionmentioning

confidence: 99%

Same-Sex Partner Preference in Zebra Finches: Pairing Flexibility and Choice

Tomaszycki

Zatirka

2014

Arch Sex Behav

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This study examined flexibility and choice in same-sex pair-bonding behavior in adult zebra finches (Taeniopygia guttata). Zebra finches form life-long monogamous relationships and extra pair behavior is very low, making them an ideal species in which to study same-sex pairing. We examined same-sex behaviors using both semi-naturalistic choice paradigms and skewed sex ratios. In the first experiment, we allowed zebra finches to pair in aviaries with equal sex ratios as part of multiple experiments. On average, 6.4% (N = 78) of unmanipulated pairs were same-sex: all but one was female-female. In a second experiment, we identified pairs from same-sex cages and selected 20 total same-sex pairs (10 of each sex). We then gave pairs a chance to court and pair with members of the opposite sex and observed their behavior for three days. Females did not retain their partner, but most paired with males. In contrast, some males did retain their partner. Similarly, females were more likely to engage in pairing behaviors with males than with their partners or other females whereas males were equally likely to engage in same-sex and opposite-sex pairing behaviors. These findings suggest that same-sex partnerships in zebra finches can be facultative, based on the sex ratio of the group in which they live, but can also be a choice, when opportunities to pair with opposite-sex individuals are possible. Furthermore, it is possible that females are more flexible in this choice of same-sex partnerships than are males.

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Hemispheric differences in processing of vocalizations depend on early experience

Cited by 61 publications

References 37 publications

Statistical learning of recurring sound patterns encodes auditory objects in songbird forebrain

Statistical learning of recurring sound patterns encodes auditory objects in songbird forebrain

Processing of communication sounds: Contributions of learning, memory, and experience

Same-Sex Partner Preference in Zebra Finches: Pairing Flexibility and Choice

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