Localized Brain Activation Related to the Strength of Auditory Learning in a Parrot

Eda-Fujiwara, Hiroko; Imagawa, Takuya; Matsushita, Makoto; Matsuda, Yasushi; Takeuchi, Hisanao; Satoh, Ryohei; Watanabe, Akïharu; Zandbergen, Matthijs A.; Manabe, Kazuchika; Kawashima, Takashi; Bolhuis, Johan J.

doi:10.1371/journal.pone.0038803

Cited by 13 publications

(18 citation statements)

References 74 publications

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“…For example, immediate-early gene (IEG) auditory responses (i.e. ZENK induction in NCM in response to auditory playbacks) yield varying results depending on species: no differences between NCM subregions are reported in in adult male European starlings 81 or adult male budgerigars 82 , whereas higher dNCM ZENK compared to vNCM has been reported in both adult female white-crowned sparrows 83 and both sexes of adult black-capped chickadees 84, but see 85 . In contrast, extracellular recordings in the NCM of adult starlings find stronger experience-dependent changes in firing rates in ventral vs dorsal NCM 86 , which were suggested to be attributed to a noted enhanced thalamic input from Field L to ventral NCM (Vates et al 1996).…”

Section: Discussionmentioning

confidence: 99%

Neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation in developing songbirds

Vahaba

Hecsh

Remage‐Healey

2020

Sci Rep

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Birdsong learning, like human speech, depends on the early memorization of auditory models, yet how initial auditory experiences are formed and consolidated is unclear. In songbirds, a putative cortical locus is the caudomedial nidopallium (NCM), and one mechanism to facilitate auditory consolidation is 17β-estradiol (E2), which is associated with human speech-language development, and is abundant in both NCM and human temporal cortex. Circulating and NCM E2 levels are dynamic during learning, suggesting E2's involvement in encoding recent auditory experiences. Therefore, we tested this hypothesis in juvenile male songbirds using a comprehensive assessment of neuroanatomy, behavior, and neurophysiology. First, we found that brain aromatase expression, and thus the capacity to synthesize neuroestrogens, remains high in the auditory cortex throughout development. Further, while systemic estrogen synthesis blockade suppressed juvenile song production, neither systemic nor unilateral E2 synthesis inhibition in NCM disrupted eventual song imitation. Surprisingly, early life neuroestrogen synthesis blockade in NCM enhanced the neural representations of both the birds' own song and the tutor song in NCM and a downstream sensorimotor region, HVC, respectively. Taken together, these findings indicate that E2 plays a multifaceted role during development, and that, contrary to prediction, tutor song memorization is unimpaired by unilateral estrogen synthesis blockade in the auditory cortex. While many animals use sounds to communicate with one another (vocal communication), the ability to learn to vocally communicate is relatively rare 1. In vocal learning animals, such as humans and songbirds, vocal learning occurs across two main phases: an auditory memorization ('sensory') phase, followed by a sensorimotor phase ('babbling' , error correction/feedback) 2,3. While much is known about sensorimotor learning, the mechanisms that guide the formation and consolidation of auditory memories early in life are less clear. One brain region likely involved in storing auditory memories in songbirds is the caudomedial nidopallium (NCM) 4. NCM, comparable to mammalian secondary auditory cortex, is required for accurate song learning. Blocking ERK-signaling or mTOR bilaterally in NCM during tutoring leads to poor song imitation 5,6. Tutoring naïve juvenile songbirds leads to an increased proportion of tutor-song-selective neurons in NCM 7. Further, bilateral NCM lesions abolish innate preference for tutor song in adults 8 , but see 9,10. Thus, NCM contains a putative tutor 'engram'; however, the neuromodulatory mechanisms that shape this auditory memory formation and consolidation remain unknown. Consolidating recent experience in other contexts and systems require presynaptic signaling molecules ('neuromodulators'), such as brain-derived estrogens 11. The predominant estrogen 17β-estradiol (E2) is a candidate neuromodulator required for auditory memory consolidation, as is evident in a similar role in adult hippocampal-dependent cognit...

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Section: Discussionmentioning

confidence: 99%

Neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation in developing songbirds

Vahaba

Hecsh

Remage‐Healey

2020

Sci Rep

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“…In addition, neuronal activation in the caudomedial pallium of the experimental birds correlated significantly and positively with the percentage of correct responses in the discrimination task. These results suggest that in a parrot, the NCM and the CMM are involved in auditory learning and memory, as they are in songbirds (Eda-Fujiwara et al, 2012).…”

Section: The Caudomedial Pallium and Tutor Song Memory: The Ncmmentioning

confidence: 68%

“…Eda-Fujiwara et al (2012) investigated the neural mechanisms of auditory discrimination learning in the budgerigar (Melopsittacus undulatus), a parrot. Like other parrots, budgerigars can learn to produce human words.…”

Section: The Caudomedial Pallium and Tutor Song Memory: The Ncmmentioning

confidence: 99%

Birdsong memory and the brain: In search of the template

Bolhuis

Moorman

2015

Neuroscience & Biobehavioral Reviews

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“…For example, immediate-early gene (IEG) auditory responses (i.e. ZENK induction in NCM in response to auditory playbacks) yield varying results depending on species: no differences between NCM subregions are reported in in adult male European starlings (Gentner et al, 2004) or adult male budgerigars (Eda-Fujiwara et al, 2012), whereas higher dNCM ZENK compared to vNCM has been reported in both adult female white-crowned sparrows (Sanford et al, 2010) and both sexes of adult black-capped chickadees (Phillmore et al, 2003; but see Avey et al, 2014). In contrast, extracellular recordings in the NCM of adult starlings find stronger experience-dependent changes in firing rates in ventral vs dorsal NCM (Thompson and Gentner, 2010), which were suggested to be attributed to a noted enhanced thalamic input from Field L to ventral NCM (Vates et al 1996).…”

Section: Developmental and Regional Shifts In Neuronal Cell Density Imentioning

confidence: 99%

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

Hecsh

Remage‐Healey

2019

Preprint

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Birdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are formed and consolidated. In both adults and developing songbirds, there is strong evidence suggesting the caudomedial nidopallium (NCM), a higher order auditory forebrain area, is the site of auditory memory consolidation. However, the mechanisms that facilitate this consolidation are poorly understood. One likely mechanism is 17β-estradiol (E2), which is associated with speech-language development and disorders in humans, and is abundant in both mammalian temporal cortex and songbird NCM. Circulating E2 is also elevated during the auditory memory phase, and in NCM immediately after song learning sessions, suggesting it functions to encode recent auditory experience. Therefore, we tested a role for E2 production in auditory memory consolidation during development using a comprehensive set of investigations to ask this question at the level of neuroanatomy, neurophysiology, and behavior. Our results demonstrate that while systemic estrogen synthesis blockade regulates juvenile song production, inhibiting E2 synthesis locally within NCM does not adversely affect song learning outcomes. Surprisingly, early life E2 manipulations in NCM modify the neural representations of birds' own song and the model tutor song in both NCM and a downstream sensorimotor nucleus (HVC). Further, we show that the capacity to synthesize neuroestrogens remains high throughout development alongside substantial changes in NCM cell density across age. Taken together, these findings suggest that E2 plays a multifaceted role during development, and demonstrate that contrary to prediction, unilateral post-training estrogen synthesis blockade in the auditory cortex does not negatively impact vocal learning. Acute downregulation of neuroestrogens are therefore likely permissive for juvenile auditory memorization, while neuroestrogen synthesis influences communication production and representation in adulthood. AntibodiesAntibodies and dilutions for aromatase and parvalbumin were identical to those used in Ikeda et al. (2017). Briefly, we used a polyclonal anti-aromatase primary antibody raised in rabbit (1:2,000; a generous gift from Dr. Colin Saldanha), and a monoclonal anti-parvalbumin primary antibody raised in mouse (1:10,000; Millipore MAB1572; RRID: AB_2174013). Secondary antibodies included goat antirabbit Alexa 488 (1:500; Thermo Fisher Scientific Inc.), and goat anti-mouse Alexa 647 (1:100; Thermo Fisher Scientific Inc.). ProcedureBrain sections were first manually washed 3 x in 0.1 M PB, followed by 3 x 15-minute washes in 0.1 M PB on a plate shaker, followed by a 2-hour incubation at room temperature with 10% normal goat serum (Vector) in 0.3 % PBT. Tissue was then transferred to a 10% normal goat...

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Localized Brain Activation Related to the Strength of Auditory Learning in a Parrot

Cited by 13 publications

References 74 publications

Neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation in developing songbirds

Neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation in developing songbirds

Birdsong memory and the brain: In search of the template

Blocking neuroestrogen synthesis modifies neural representations of learned song without altering vocal imitation accuracy in developing songbirds

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