Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Stripling, Roy; Milewski, Lynn; Kruse, Amy; Clayton, David F.

doi:10.1016/s1074-7427(02)00005-9

Cited by 40 publications

(51 citation statements)

References 33 publications

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“…Video analysis (Fig. 2) confirmed the difference between the novel and habituated groups in their behavioral responses to the song as described in previous studies (8,13).…”

supporting

confidence: 85%

“…Habituation is not simply the loss of all neural responses to the auditory stimulus, as neurons in the auditory forebrain still fire in response to the familiar song (albeit at a somewhat lower rate compared to when the song is first novel) (9-11). These changing neural responses may be related to shifts in how the singer is perceived in the context of territorial and colonial social life (3,12,13).Studies of song response habituation have focused on a single gene, ZENK. However, other genes are likely to be involved as well, as studies in other systems have indicated that experience can affect the expression of many genes in the brain (e.g., refs.…”

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confidence: 99%

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Discrete molecular states in the brain accompany changing responses to a vocal signal

Dong¹,

Replogle

Hasadsri³

et al. 2009

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

100

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New experiences can trigger changes in gene expression in the brain. To understand this phenomenon better, we studied zebra finches hearing playbacks of birdsong. Earlier research had shown that initial playbacks of a novel song transiently increase the ZENK (ZIF-268, EGR1, NGFIA, KROX-24) mRNA in the auditory forebrain, but the response selectively habituates after repetition of the stimulus. Here, using DNA microarray analysis, we show that novel song exposure induces rapid changes in thousands of RNAs, with even more RNAs decreasing than increasing. Habituation training leads to the emergence of a different gene expression profile a day later, accompanied by loss of essentially all of the rapid ''novel'' molecular responses. The novel molecular profile is characterized by increases in genes involved in transcription and RNA processing and decreases in ion channels and putative noncoding RNAs. The ''habituated'' profile is dominated by changes in genes for mitochondrial proteins. A parallel proteomic analysis [2-dimensional difference gel electrophoresis (2D-DIGE) and sequencing by mass spectrometry] also detected changes in mitochondrial proteins, and direct enzyme assay demonstrated changes in both complexes I and IV in the habituated state. Thus a natural experience, in this case hearing the sound of birdsong, can lead to major shifts in energetics and macromolecular metabolism in higher centers in the brain.habituation ͉ microarray ͉ mitochondria ͉ proteomic ͉ songbird T he genome was once regarded as a passive agent in brain function, directing brain development but having little role in the moment-to-moment operation of the mature brain. Through the widespread application of technologies for measuring gene expression in experimental model systems, however, it now appears that changing social conditions, perceptual experience, and behavioral activity can all result in rapid changes in the expression of specific genes in the brain (1, 2). The challenge ahead is to understand the links between gene expression and natural experience, behavior, and cognition.A striking example for study is the phenomenon of song response habituation in songbirds (3). In one of the first demonstrations of brain gene activation in response to a natural experience, Mello and colleagues (4) showed that the sound of another bird singing triggers a transient increase in expression of the ZENK gene EGR1, NGFIA, in an auditory/associative region of the songbird forebrain. This was not simply a sensory or an auditory response, as its magnitude showed clear categorical discrimination (conspecific song Ͼ heterospecific song Ͼ noise Ͼ pure tones). Further research showed that the same song stimulus would either activate ZENK expression or not, depending on the recent history of exposure to the stimulus and its context. After the stimulus was repeated for a few hours the ZENK RNA declined back to its initial starting level (5, 6). Subsequent presentations no longer elicited a response, but presentation of a different song (6) or even of ...

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“…Video analysis (Fig. 2) confirmed the difference between the novel and habituated groups in their behavioral responses to the song as described in previous studies (8,13).…”

supporting

confidence: 85%

mentioning

confidence: 99%

Discrete molecular states in the brain accompany changing responses to a vocal signal

Dong¹,

Replogle

Hasadsri³

et al. 2009

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

100

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show abstract

“…Right: Mean and SD of reaction times for birds trained on 30 dB songs. (Stripling et al 2003), or displays (Nowicki et al 2002;O'Lochlen and Beecher 1999) in response to song presentation, have also been successfully used to gauge mate recognition and song familiarity, but it is often difficult to determine the difference between incorrect and absent responses. Techniques such as multi-dimensional scaling (e.g., Dooling et al 1987) have also provided insight into what acoustic parameters birds use to group or classify calls; however, this approach requires the experimenter to parameterize the differences between the stimuli being classified.…”

Section: Discussionmentioning

confidence: 99%

“…How does the brain achieve these two tasks? One model (Cadieu et al 2007;Serre et al 2007;Sugrue et al 2005) is that it transforms the stimulus to emphasize the most important differences, then classifies these representations according to some set of rules.…”

Section: Introductionmentioning

confidence: 99%

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Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

Nagel

McLendon

Doupe

2010

Journal of Neurophysiology

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Nagel KI, McLendon HM, Doupe AJ. Differential influence of frequency, timing, and intensity cues in a complex acoustic categorization task. J Neurophysiol 104: 1426 -1437, 2010. First published July 7, 2010 doi:10.1152/jn.00028.2010. Songbirds, which, like humans, learn complex vocalizations, provide an excellent model for the study of acoustic pattern recognition. Here we examined the role of three basic acoustic parameters in an ethologically relevant categorization task. Female zebra finches were first trained to classify songs as belonging to one of two males and then asked whether they could generalize this knowledge to songs systematically altered with respect to frequency, timing, or intensity. Birds' performance on song categorization fell off rapidly when songs were altered in frequency or intensity, but they generalized well to songs that were changed in duration by Ͼ25%. Birds were not deaf to timing changes, however; they detected these tempo alterations when asked to discriminate between the same song played back at two different speeds. In addition, when birds were retrained with songs at many intensities, they could correctly categorize songs over a wide range of volumes. Thus although they can detect all these cues, birds attend less to tempo than to frequency or intensity cues during song categorization. These results are unexpected for several reasons: zebra finches normally encounter a wide range of song volumes but most failed to generalize across volumes in this task; males produce only slight variations in tempo, but females generalized widely over changes in song duration; and all three acoustic parameters are critical for auditory neurons. Thus behavioral data place surprising constraints on the relationship between previous experience, behavioral task, neural responses, and perception. We discuss implications for models of auditory pattern recognition.

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Molecular Neurobiology of Bird Song

Clayton¹

2007

Handbook of Neurochemistry and Molecular Neurobiology

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Rapidly learned song-discrimination without behavioral reinforcement in adult male zebra finches (Taeniopygia guttata)

Cited by 40 publications

References 33 publications

Discrete molecular states in the brain accompany changing responses to a vocal signal

Discrete molecular states in the brain accompany changing responses to a vocal signal

Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

Molecular Neurobiology of Bird Song

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