Localized brain activation specific to auditory memory in a female songbird

Terpstra, Nienke J.; Bolhuis, Johan J.; Riebel, Katharina; Burg, Jorien M.M. van der; Boer-Visser, Ardie M. den

doi:10.1002/cne.20831

Cited by 108 publications

(110 citation statements)

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“…In adult male zebra finches, there was no such difference (Terpstra et al 2004), while in female zebra finches, which do not sing themselves, mean levels of molecular neuronal activation were greater for the father's song than for a novel song (Terpstra et al 2006). The present results indicate that the CMM may also be important while juveniles are learning their song.…”

Section: Discussioncontrasting

confidence: 43%

“…For the CMM, the frame was placed adjacent to the ventricle and the lamina mesopallialis. Distance from the midline was assessed by calculating the number of serial sections and this location was verified using the atlas of Vates et al (1996), an unpublished atlas of the zebra finch brain by A. M. den Boer-Visser (which was also used in previous studies; Terpstra et al 2004Terpstra et al , 2006) and a stereotaxic atlas that is available online (Nixdorf-Bergweiler & Bischof 2007). For three sections containing the HVC, as well as for the RA, the photomicrographs were taken in the centre of the nucleus.…”

Section: Methodsmentioning

confidence: 99%

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Memory in the making: localized brain activation related to song learning in young songbirds

2010

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Songbird males learn to sing their songs from an adult 'tutor' early in life, much like human infants learn to speak. Similar to humans, in the songbird brain there are separate neural substrates for vocal production and for auditory memory. In adult songbirds, the caudal pallium, the avian equivalent of the auditory association cortex, has been proposed to contain the neural substrate of tutor song memory, while the song system is involved in song production as well as sensorimotor learning. If this hypothesis is correct, there should be neuronal activation in the caudal pallium, and not in the song system, while the young bird is hearing the tutor song. We found increased song-induced molecular neuronal activation, measured as the expression of an immediate early gene, in the caudal pallium of juvenile zebra finch males that were in the process of learning to sing their songs. No such activation was found in the song system. Molecular neuronal activation was significantly greater in response to tutor song than to novel song or silence in the medial part of the caudomedial nidopallium (NCM). In the caudomedial mesopallium, there was significantly greater molecular neuronal activation in response to tutor song than to silence. In addition, in the NCM there was a significant positive correlation between spontaneous molecular neuronal activation and the strength of song learning during sleep. These results suggest that the caudal pallium contains the neural substrate for tutor song memory, which is activated during sleep when the young bird is in the process of learning its song. The findings provide insight into the formation of auditory memories that guide vocal production learning, a process fundamental for human speech acquisition.

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Section: Discussioncontrasting

confidence: 43%

Section: Methodsmentioning

confidence: 99%

Memory in the making: localized brain activation related to song learning in young songbirds

2010

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“…It is not considered part of the traditional song system, but its two main components, NCM and CMM 38 , are highly specialized to process complex sounds, especially conspecific birdsongs (for example, see refs. [6][7][8]12,13,39 ). We used a well-established pharmacological inhibitor of ERK activation to achieve a transient, reversible disruption of memory processes in the auditory lobule.…”

Section: Discussionmentioning

confidence: 99%

Functional identification of sensory mechanisms required for developmental song learning

2008

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A young male zebra finch (Taeniopygia guttata) learns to sing by copying the vocalizations of an older tutor in a process that parallels human speech acquisition. Brain pathways that control song production are well defined, but little is known about the sites and mechanisms of tutor song memorization. Here we test the hypothesis that molecular signaling in a sensory brain area outside of the song system is required for developmental song learning. Using controlled tutoring and a pharmacological inhibitor, we transiently suppressed the extracellular signal-regulated kinase signaling pathway in a portion of the auditory forebrain specifically during tutor song exposure. On maturation, treated birds produced poor copies of tutor song, whereas controls copied the tutor song effectively. Thus the foundation of normal song learning, the formation of a sensory memory of tutor song, requires a conserved molecular pathway in a brain area that is distinct from the circuit for song motor control.Young male zebra finches learn to sing from adult tutors during a critical period in juvenile life. Developmental song learning occurs in two phases 1 . First, the young bird creates an auditory memory, or 'template', of his tutor's song. Then the young bird begins to vocalize, and, through a process of sensorimotor error correction, modifies his own song to resemble the tutor template. As an adult, each male zebra finch sings a unique set of unchanging syllables (the bird's own song) that reflects his earlier song exposure.The neural circuitry that controls song production is relatively well understood 2-4 , but it has been much more difficult to find the neuroanatomical and molecular basis for the sensory component of song learning: tutor song memorization. Recent studies suggest that the forebrain auditory lobule 5 , the functional homolog of mammalian primary and secondary auditory cortices, may be important in forming learned song representations. In adult songbirds, immediate-early gene induction and distinct patterns of cellular activity occur in the auditory lobule during song recognition learning 6-9 . Similar measures can be correlated with the fraction of tutor song that is copied 10-13 , implying that a tutor song trace persists in the auditory lobule. The induction of one immediate-early gene, zenk (also known as Egr1, Zif268, , is regulated by the extracellular signal-regulated kinase (ERK) in NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript the zebra finch auditory lobule5 and in other models 14-16 . This connection to ERK, part of a molecular pathway that is integral to memory 14,17 , led us to hypothesize that the ERK cascade in the auditory lobule was necessary for tutor song memorization. We tested this hypothesis using controlled tutor experience and a specific inhibitor of ERK activation 16 , and found that molecular processing in the auditory lobule during tutor exposure is required for accurate tutor song copying. Results Controlled tutoringYoung male zebra finches were soci...

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“…Quantification of Zenk-immunopositive cells was performed for NCM, HVC, and hippocampus as described previously (cf. 13,49,50). Digital photographs were taken using a Leica DFC 4206 camera and the Leica Application Suite program on an Axioskop (Zeiss) with a 20× objective.…”

Section: Methodsmentioning

confidence: 99%

Human-like brain hemispheric dominance in birdsong learning

Moorman

Gobes

Kuijpers

et al. 2012

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

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Unlike nonhuman primates, songbirds learn to vocalize very much like human infants acquire spoken language. In humans, Broca's area in the frontal lobe and Wernicke's area in the temporal lobe are crucially involved in speech production and perception, respectively. Songbirds have analogous brain regions that show a similar neural dissociation between vocal production and auditory perception and memory. In both humans and songbirds, there is evidence for lateralization of neural responsiveness in these brain regions. Human infants already show left-sided dominance in their brain activation when exposed to speech. Moreover, a memoryspecific left-sided dominance in Wernicke's area for speech perception has been demonstrated in 2.5-mo-old babies. It is possible that auditory-vocal learning is associated with hemispheric dominance and that this association arose in songbirds and humans through convergent evolution. Therefore, we investigated whether there is similar song memory-related lateralization in the songbird brain. We exposed male zebra finches to tutor or unfamiliar song. We found left-sided dominance of neuronal activation in a Broca-like brain region (HVC, a letter-based name) of juvenile and adult zebra finch males, independent of the song stimulus presented. In addition, juvenile males showed left-sided dominance for tutor song but not for unfamiliar song in a Wernickelike brain region (the caudomedial nidopallium). Thus, left-sided dominance in the caudomedial nidopallium was specific for the song-learning phase and was memory-related. These findings demonstrate a remarkable neural parallel between birdsong and human spoken language, and they have important consequences for our understanding of the evolution of auditory-vocal learning and its neural mechanisms.left-brain activation | hemispheric specialization | Taeniopygia guttata | language evolution

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Localized brain activation specific to auditory memory in a female songbird

Cited by 108 publications

References 54 publications

Memory in the making: localized brain activation related to song learning in young songbirds

Memory in the making: localized brain activation related to song learning in young songbirds

Functional identification of sensory mechanisms required for developmental song learning

Human-like brain hemispheric dominance in birdsong learning

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