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

Abstract

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.

Genetically identified neurons in avian auditory pallium mirror core principles of their mammalian counterparts

“…The viruses and approximate titers used in the present study included: pAAV9-CaMKIIa-hChR2(E123A)-EYFP (titer: 1x10 13 viral genomes/mL; Addgene: 35505); 135 pAAV9-hGAD1-FLAG-NLS-Cre (titer: 1.25x10 12 viral genomes/mL; made in-house; rAAV-GAD-SD/ SA-YTB plasmid generously gifted by Dr David Lyon; see Liu et al 136 for promoter selectivity in mammals), pAAV9-mDlx-ChR2(H134R)-EYFP (titer: 1.5x10 12 viral genomes/mL; made in-house; mDlx viral construct additionally validated in zebra finch nidopallium in previous work 81,82 ), AAV9-hSyn-hChR2(H134R)-eYFP-WPRE-hGH (titer: 3.36x10 12 ; made in-house), AAV9-pCAG-FLEX-tdTomato-WPRE (titer: 1.5x10 12 viral genomes/mL; Addgene: 51503), 137 AAV9-FLEX-rev-ChR2(H134R)-mCherry (titer: 5x10 12 viral genomes/mL; Addgene: 18916), 138 and AAV-FLEX-Arch-GFP (titer: 5x10 12 viral genomes/mL; Addgene: 22222). 139 Immunofluorescence A subset of birds (N = 3; 2 males, 1 female) given injections with viruses targeting both CaMKIIa and GAD1 promoters were transcardially perfused with 4% paraformaldehyde 4-6 weeks following surgery.…”

“…In this study, we characterized CaMKIIa and GAD1 populations using viral constructs with both in vitro and in vivo approaches. We used an mDlx enhancer sequence as an additional, complementary way to access inhibitory populations (previously validated in songbirds; 81,82 migration of mDlx cells from the subventricular zone to pallium is similar to tangential migration of interneurons in mammalian pallium). 21 If avian pallial cell types exhibit similar circuit and computational roles as observed in mammals, then promoters that distinguish mammalian cell types (i.e., CaMKIIa and GAD1) should categorically define viral-driven optogenetic access to broadand narrow-spiking pallial cells in NCM.…”

Adult‐like neural representation of species‐specific songs in the auditory forebrain of zebra finch nestlings

“…Kudo et al. (2020) also report that isolation from tutors also has differential effects on developmental changes in the proportion of burst‐type neurons in NCM of males and females. Perhaps the reason for the lack of evidence for sex differences in NCM is that many studies do not address its role through development.…”

“…Perhaps the developmental mismatch between studies can also be explained by differences in age, stimuli, and anesthetized versus awake recording procedures across studies. Particularly, while we did not test any individuals during the sensitive period of song learning, several studies show changes in NCM properties between ~20–60 dph (Jin & Clayton, 1997; Kudo et al., 2020; Miller‐Sims & Bottjer, 2014; Stripling et al., 2001; Vahaba et al., 2017). This indicates that the sensitive period (including ages tested by Amin et al.…”

Modulation of Theta Phase Synchrony during Syllable Processing as a Function of Interactive Acoustic Experience in Infancy

“…Given that the infant brain is highly plastic and learning experiences induce cortical representational plasticity ( Buonomano and Merzenich 1998 ; Kudo et al. 2020 ), a process that is enhanced by attention ( Ahveninen et al.…”