Inception of memories that guide vocal learning in the songbird

Zhao, Wenchan; García-Oscos, Francisco; Dinh, Daniel; Roberts, Todd F.

doi:10.1126/science.aaw4226

Cited by 45 publications

(41 citation statements)

References 48 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In a combined NIf/HVC model, these NIf ensembles are sufficient to train downstream premotor sequences in HVC. Finally, in light of recent optogenetics results 62 , we model how NIf may play a role specifying the durations of song syllables.…”

mentioning

confidence: 99%

An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

2020

View full text Add to dashboard Cite

How are brain circuits constructed to achieve complex goals? The brains of young songbirds develop motor circuits that achieve the goal of imitating a specific tutor song to which they are exposed. Here, we set out to examine how song-generating circuits may be influenced early in song learning by a cortical region (NIf) at the interface between auditory and motor systems. Single-unit recordings reveal that, during juvenile babbling, NIf neurons burst at syllable onsets, with some neurons exhibiting selectivity for particular emerging syllable types. When juvenile birds listen to their tutor, NIf neurons are also activated at tutor syllable onsets, and are often selective for particular syllable types. We examine a simple computational model in which tutor exposure imprints the correct number of syllable patterns as ensembles in an interconnected NIf network. These ensembles are then reactivated during singing to train a set of syllable sequences in the motor network.

show abstract

mentioning

confidence: 99%

An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

2020

View full text Add to dashboard Cite

show abstract

“…Proportions of NCM firing and burst type neurons changed over the sensory learning period. The NCM has been suggested to be involved in song learning in males, especially as one of the sites for storing tutor song memories (Bolhuis and Gahr, 2006 ; Hahnloser and Kotowicz, 2010 ; Bolhuis and Moorman, 2015 ), while other brain areas in the song system have also been suggested as tutor song memory loci (Mackevicius and Fee, 2018 ; Zhao et al, 2019 ). On the other hand, in females, the NCM is thought to be involved in song discrimination (Tomaszycki and Blaine, 2014 ).…”

Section: Resultsmentioning

confidence: 99%

“…Formed memories of tutor songs are thought to guide later motor song learning in males (Brainard and Doupe, 2002 ; Bolhuis and Gahr, 2006 ; Theunissen and Shaevitz, 2006 ) and also to affect auditory cognitive functions of females in later auditory learning (Chen et al, 2017 ; Diez et al, 2019 ). Accumulating evidence suggests that memories of tutor songs for male juvenile song learning are formed in the caudomedial nidopallium (NCM), which is analogous to the mammalian higher auditory cortex, while other studies have suggested the presence of tutor song memories in the song motor area (Mackevicius and Fee, 2018 ; Zhao et al, 2019 ). A greater number of NCM neurons express the immediate early gene, ZENK, in zebra finches that are exposed to experienced tutor songs than in those that are exposed to novel conspecific songs (Terpstra et al, 2004 ).…”

Section: Introductionmentioning

confidence: 99%

Early Auditory Experience Modifies Neuronal Firing Properties in the Zebra Finch Auditory Cortex

Kudo

Morohashi

Yazaki-Sugiyama

2020

Front. Neural Circuits

View full text Add to dashboard Cite

Songbirds learn to sing much as humans learn to speak. In zebra finches, one of the premier songbird models, males learn to sing for later courtship through a multistep learning process during the developmental period. They first listen to and memorize the song of a tutor (normally their father) during the sensory learning period. Then, in the subsequent sensory-motor learning phase (with large overlap), they match their vocalizations to the memorized tutor song via auditory feedback and develop their own unique songs, which they maintain throughout their lives. Previous studies have suggested that memories of tutor songs are shaped in the caudomedial nidopallium (NCM) of the brain, which is analogous to the mammalian higher auditory cortex. Isolation during development, which extends the sensory learning period in males, alters song preference in adult females, and NCM inactivation decreases song preference. However, the development of neurophysiological properties of neurons in this area and the effect of isolation on these neurons have not yet been explained. Here, we performed whole-cell patch-clamp recording on NCM neurons from juvenile zebra finches during the sensory learning period, 20, 40, or 60 days post-hatching (DPH) and examined their neurophysiological properties. In contrast to previous reports in adult NCM neurons, the majority of NCM neurons of juvenile zebra finches showed spontaneous firing with or without burst firing patterns, and the percentage of neurons that fired increased in the middle of the sensory learning period (40 DPH) and then decreased at the end (60 DPH) in both males and females. We further found that auditory isolation from tutor songs alters developmental changes in the proportions of firing neurons both in males and females, and also changes those of burst neurons differently between males that sing and females that do not. Taken together, these findings suggest that NCM neurons develop their neurophysiological properties depending on auditory experiences during the sensory song learning period, which underlies memory formation for song learning in males and song discrimination in females.

show abstract

“…Juvenile birds can memorize the song of a tutor at any time between 20-60 dph, but they don’t start to practice singing until approximately 35-40 dph (Fig 1a). This developmental progression and the ability to raise birds in groups without a song-tutor – hereby referred to as ‘isolates’ – allowed us to knock down FoxP1 expression prior to behavioral imitation of song, either before or after birds had an opportunity to form a memory of a tutor-song 16 (Fig. 2a: tutoring pre-FP1-KD, referred to as ‘behavioral imitation’ group ( FP1-KD BI ), Fig.2e: tutoring post-FP1-KD, referred to as ‘social experience’ group ( FP1-KD SE )).…”

Section: Knockdown Of Foxp1 In Hvc Blocks Learning From Social Experimentioning

confidence: 99%

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

García-Oscos

Koch

Pancholi

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Autism spectrum disorders (ASD) are characterized by impaired learning of culturally transmitted behaviors like 10 social skills, speech, and language 1-3 . These behaviors are learned by copying parents and other social models during 11 development, a two-stage process that involves forming memories of appropriate behaviors during social 12 experiences and then using those memories to guide imitation. How ASD-linked genes impair these often-13 intertwined aspects of learning is not known, thereby limiting our understanding of the developmental progression 14 of ASD and the targeting of therapeutic interventions. Here we show that these aspects of learning are dissociable 15 and that the ASD-linked gene FoxP1 selectively impairs learning from social experience, but not behavioral imitation. 16 Haploinsufficiency of FOXP1 in humans causes FOXP1 syndrome, a neurodevelopmental disorder typified by severe 17 disruptions in speech and language development, and other ASD-associated symptoms 4,5 . We tested how 18 knockdown of FoxP1 (FP1-KD) affects the cultural transmission of vocal behaviors in zebra finches, a songbird that 19 learns by memorizing and vocally copying the song of an adult 'song-tutor'. We find that FP1-KD blocks song learning20 in juvenile birds by selectively impairing their ability to encode a memory during social experiences with a song-21 tutor. These learning deficits are linked to disruptions in experience-driven structural and functional plasticity. 22However, if birds are exposed to tutor-song prior to FP1-KD, their ability to imitate that song during development is 23 unaffected. Thus, FP1-KD impairs cultural transmission of vocalizations by disrupting the ability to form appropriate 24 vocal memories, yet spares the ability to use previously acquired memories to guide vocal learning. This indicates 25 that learning from social experience may be particularly vulnerable in FOXP1 syndrome. 26 27 28Humans and other animals learn many of their complex and socially oriented behaviors by imitating more experienced 29 individuals in their environment. For example, development of spoken language is rooted in a child's ability to imitate 30 the speech patterns of their parent(s) and other adults 6-8 . This cultural transmission of behavior is impaired in many 31 neurodevelopmental disorders, most notably ASD 1-3 . However, how ASD risk genes impact behavioral imitation is still 32 not known. We sought to examine this issue by testing the role of FoxP1 in the cultural transmission of song between 33 adult and juvenile zebra finches ( Fig. 1a-d, Extended Data Fig. 1). 34 35 2 FOXP1 (forkhead-box protein 1) is one of the top ASD-associated genes, and its haploinsufficiency causes specific 36 language impairment and intellectual disability in children 5 . FoxP1 is expressed in many of the same areas of the pallium 37 and basal ganglia in mammals and songbirds 9-11 . In zebra finches, FoxP1 expression is enriched in many brain regions 38 that are known to be important for song learning [10][11][12] (Fig. ...

show abstract

Inception of memories that guide vocal learning in the songbird

Cited by 45 publications

References 48 publications

An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

Early Auditory Experience Modifies Neuronal Firing Properties in the Zebra Finch Auditory Cortex

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

Contact Info

Product

Resources

About