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Sleep and sensorimotor integration during early vocal learning in a songbird.

Shank SS, Margoliash D - Nature (2008)

Bottom Line: Here we show that, in juvenile zebra finches, playback during the day of an adult 'tutor' song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep.Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling.Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Chicago, Chicago, Illinois 60637, USA.

ABSTRACT
Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours. During sleep, brain regions are reactivated, and specific patterns of neural activity are replayed, consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning. Song development in juvenile zebra finches (Taeniopygia guttata) is characterized by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons in the robust nucleus of the arcopallium (RA) carries information about daytime singing. Here we show that, in juvenile zebra finches, playback during the day of an adult 'tutor' song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep. The night-time neuronal changes preceded tutor-song-induced changes in singing, first observed the following day. Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling. Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning. We hypothesize that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, adaptive changes driven by replay of sensory information at night and by evaluation of sensory feedback during the day interact to produce the complex circadian patterns seen early in vocal development.

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RA sleep activity in absence of auditory feedback (WN or muted). a, ISI distributions prior to tutor song exposure, averaged across two muted birds and four birds raised in WN (lower black line), and averaged (for comparison) across 13 birds with normal feedback (upper black line). b, WN and muted birds fail to show tutor song-specific ISI distributions after song exposure. Lower red line: mean post-exposure distribution from muted and WN birds (5/6 birds heard Song 1). Upper red line: mean distribution from intact Song 1 birds (same as in Fig. 2c,). c, Bursting returns when feedback is restored. WN birds (n=4) both pre-exposure (black line) and post-exposure but in WN (lower red line) show suppression of bursting; bursting recovers after WN is turned off (upper red line). Compare with distribution for intact Song 1 birds (middle red line). d, Profound suppression of bursting for all cells in a WN bird. The second night following withdrawal of WN, bursting appears. White lines represent daytime. e, Recording of singing in presence of 100 dB WN without and with noise cancellation (left and right, respectively). Right, bold yellow lines mark vocalisations.
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Figure 3: RA sleep activity in absence of auditory feedback (WN or muted). a, ISI distributions prior to tutor song exposure, averaged across two muted birds and four birds raised in WN (lower black line), and averaged (for comparison) across 13 birds with normal feedback (upper black line). b, WN and muted birds fail to show tutor song-specific ISI distributions after song exposure. Lower red line: mean post-exposure distribution from muted and WN birds (5/6 birds heard Song 1). Upper red line: mean distribution from intact Song 1 birds (same as in Fig. 2c,). c, Bursting returns when feedback is restored. WN birds (n=4) both pre-exposure (black line) and post-exposure but in WN (lower red line) show suppression of bursting; bursting recovers after WN is turned off (upper red line). Compare with distribution for intact Song 1 birds (middle red line). d, Profound suppression of bursting for all cells in a WN bird. The second night following withdrawal of WN, bursting appears. White lines represent daytime. e, Recording of singing in presence of 100 dB WN without and with noise cancellation (left and right, respectively). Right, bold yellow lines mark vocalisations.

Mentions: Zebra finches begin singing as early as 25 days of age18, so our ≈40 day-old birds had extensive sensorimotor experience prior to neural recordings. To explore the influence of singing and auditory feedback on the structure of RA neuronal bursting, we performed two additional experiments. We prevented singing by surgically muting two birds (a third bird, M2, sang in spite of the surgery), and placed a second group of four birds in a continuous 100 dB white noise (WN) environment to suppress auditory feedback. All seven birds cued tutor song playback, which for WN birds also briefly eliminated the masking noise. A noise cancellation technique allowed us to qualitatively assess the amount of singing in WN (Fig. 3e).


Sleep and sensorimotor integration during early vocal learning in a songbird.

Shank SS, Margoliash D - Nature (2008)

RA sleep activity in absence of auditory feedback (WN or muted). a, ISI distributions prior to tutor song exposure, averaged across two muted birds and four birds raised in WN (lower black line), and averaged (for comparison) across 13 birds with normal feedback (upper black line). b, WN and muted birds fail to show tutor song-specific ISI distributions after song exposure. Lower red line: mean post-exposure distribution from muted and WN birds (5/6 birds heard Song 1). Upper red line: mean distribution from intact Song 1 birds (same as in Fig. 2c,). c, Bursting returns when feedback is restored. WN birds (n=4) both pre-exposure (black line) and post-exposure but in WN (lower red line) show suppression of bursting; bursting recovers after WN is turned off (upper red line). Compare with distribution for intact Song 1 birds (middle red line). d, Profound suppression of bursting for all cells in a WN bird. The second night following withdrawal of WN, bursting appears. White lines represent daytime. e, Recording of singing in presence of 100 dB WN without and with noise cancellation (left and right, respectively). Right, bold yellow lines mark vocalisations.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC2651989&req=5

Figure 3: RA sleep activity in absence of auditory feedback (WN or muted). a, ISI distributions prior to tutor song exposure, averaged across two muted birds and four birds raised in WN (lower black line), and averaged (for comparison) across 13 birds with normal feedback (upper black line). b, WN and muted birds fail to show tutor song-specific ISI distributions after song exposure. Lower red line: mean post-exposure distribution from muted and WN birds (5/6 birds heard Song 1). Upper red line: mean distribution from intact Song 1 birds (same as in Fig. 2c,). c, Bursting returns when feedback is restored. WN birds (n=4) both pre-exposure (black line) and post-exposure but in WN (lower red line) show suppression of bursting; bursting recovers after WN is turned off (upper red line). Compare with distribution for intact Song 1 birds (middle red line). d, Profound suppression of bursting for all cells in a WN bird. The second night following withdrawal of WN, bursting appears. White lines represent daytime. e, Recording of singing in presence of 100 dB WN without and with noise cancellation (left and right, respectively). Right, bold yellow lines mark vocalisations.
Mentions: Zebra finches begin singing as early as 25 days of age18, so our ≈40 day-old birds had extensive sensorimotor experience prior to neural recordings. To explore the influence of singing and auditory feedback on the structure of RA neuronal bursting, we performed two additional experiments. We prevented singing by surgically muting two birds (a third bird, M2, sang in spite of the surgery), and placed a second group of four birds in a continuous 100 dB white noise (WN) environment to suppress auditory feedback. All seven birds cued tutor song playback, which for WN birds also briefly eliminated the masking noise. A noise cancellation technique allowed us to qualitatively assess the amount of singing in WN (Fig. 3e).

Bottom Line: Here we show that, in juvenile zebra finches, playback during the day of an adult 'tutor' song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep.Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling.Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Chicago, Chicago, Illinois 60637, USA.

ABSTRACT
Behavioural studies widely implicate sleep in memory consolidation in the learning of a broad range of behaviours. During sleep, brain regions are reactivated, and specific patterns of neural activity are replayed, consistent with patterns observed in previous waking behaviour. Birdsong learning is a paradigmatic model system for skill learning. Song development in juvenile zebra finches (Taeniopygia guttata) is characterized by sleep-dependent circadian fluctuations in singing behaviour, with immediate post-sleep deterioration in song structure followed by recovery later in the day. In sleeping adult birds, spontaneous bursting activity of forebrain premotor neurons in the robust nucleus of the arcopallium (RA) carries information about daytime singing. Here we show that, in juvenile zebra finches, playback during the day of an adult 'tutor' song induced profound and tutor-song-specific changes in bursting activity of RA neurons during the following night of sleep. The night-time neuronal changes preceded tutor-song-induced changes in singing, first observed the following day. Interruption of auditory feedback greatly reduced sleep bursting and prevented the tutor-song-specific neuronal remodelling. Thus, night-time neuronal activity is shaped by the interaction of the song model (sensory template) and auditory feedback, with changes in night-time activity preceding the onset of practice associated with vocal learning. We hypothesize that night-time bursting induces adaptive changes in premotor networks during sleep as part of vocal learning. By this hypothesis, adaptive changes driven by replay of sensory information at night and by evaluation of sensory feedback during the day interact to produce the complex circadian patterns seen early in vocal development.

Show MeSH
Related in: MedlinePlus