Bidirectional scaling of vocal variability by an avian cortico-basal ganglia circuit

Heston, Jonathan B.; Simon, József; Day, Nancy F.; Coleman, Melissa J.; White, Stephanie A.

doi:10.14814/phy2.13638

Cited by 13 publications

(13 citation statements)

References 43 publications

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“…We also found that OR modulation in LMAN and Area X appear to have contrasting effects on the spectral properties of song (Heston et al, 2018). In an earlier study, blocking ORs in Area X led to significant decreases in FM, AM and pitch goodness, and a significant increase in pitch, whereas Wiener entropy and mean frequency of motifs was not affected (Kumar et al, 2019).…”

Section: Changes In or Modulation In Lman Lead To Alterations In The supporting

confidence: 57%

Blocking Opioid Receptors in a Songbird Cortical Region Modulates the Acoustic Features and Levels of Female-Directed Singing

et al. 2020

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The organization of the anterior forebrain pathway (AFP) of songbirds important for context-dependent singing is similar to that of cortical basal ganglia loops (CBG) in mammals, which underlie motor behaviors including vocalization. Since different components of the AFP express high levels of µ-opioid receptors (µ-ORs) as do CBG loops, songbirds act as model systems to study the role of opioid modulation on vocalization and the motivation to sing. The AFP in songbirds includes the cortical/pallial region LMAN (lateral magnocellular nucleus of the anterior nidopallium) which projects to Area X, a nucleus of the avian basal ganglia. In the present study, microdialysis was used to infuse different doses of the opioid antagonist naloxone in LMAN of adult male zebra finches. Whereas all doses of naloxone led to significant decreases in the number of FD (female-directed) songs, only 100 and 200 ng/ml of naloxone affected their acoustic properties. The decrease in FD song was not accompanied by changes in levels of attention toward females or those of neurotransmitters (dopamine, glutamate, and GABA) in LMAN. An earlier study had shown that similar manipulations in Area X did not lead to alterations in the number of FD songs but had significantly greater effects on their acoustic properties. Taken together, our results suggest that there are reciprocal effects of OR modulation on cortical and basal ganglia components of the AFP in songbirds.

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Section: Changes In or Modulation In Lman Lead To Alterations In The supporting

confidence: 57%

Blocking Opioid Receptors in a Songbird Cortical Region Modulates the Acoustic Features and Levels of Female-Directed Singing

et al. 2020

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“…Female preference for male song is inversely correlated with song variability (Woolley and Doupe, 2008; Chen et al, 2017; Heston et al, 2018). To determine if increased variability of FD song induced by FoxP2 overexpression was perceived by conspecifics, and thus of potential ethological relevance, we tested whether female zebra finches altered their behavior in response to more stereotyped (AAV-FoxP2 PRE FD) or variable (AAV-FoxP2 POST FD) songs.…”

Section: Resultsmentioning

confidence: 99%

Beyond Critical Period Learning: Striatal FoxP2 Affects the Active Maintenance of Learned Vocalizations in Adulthood

Day

Hobbs

Heston

2019

eNeuro

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In humans, mutations in the transcription factor forkhead box P2 (FOXP2) result in language disorders associated with altered striatal structure. Like speech, birdsong is learned through social interactions during maturational critical periods, and it relies on auditory feedback during initial learning and on-going maintenance. Hearing loss causes learned vocalizations to deteriorate in adult humans and songbirds. In the adult songbird brain, most FoxP2-enriched regions (e.g., cortex, thalamus) show a static expression level, but in the striatal song control nucleus, area X, FoxP2 is regulated by singing and social context: when juveniles and adults sing alone, its levels drop, and songs are more variable. When males sing to females, FoxP2 levels remain high, and songs are relatively stable: this “on-line” regulation implicates FoxP2 in ongoing vocal processes, but its role in the auditory-based maintenance of learned vocalization has not been examined. To test this, we overexpressed FoxP2 in both hearing and deafened adult zebra finches and assessed effects on song sung alone versus songs directed to females. In intact birds singing alone, no changes were detected between songs of males expressing FoxP2 or a GFP construct in area X, consistent with the marked stability of mature song in this species. In contrast, songs of males overexpressing FoxP2 became more variable and were less preferable to females, unlike responses to songs of GFP-expressing control males. In deafened birds, song deteriorated more rapidly following FoxP2 overexpression relative to GFP controls. Together, these experiments suggest that behavior-driven FoxP2 expression and auditory feedback interact to precisely maintain learned vocalizations.

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“…The zebra finch (Taeniopygia guttata) provides an excellent avian system to understand the neural mechanisms of pair bonding. In addition to the formation of monogamous pairs, their courtship behavior is well described (Zann, 1994(Zann, , 1996, much of the circuitry involved in social behaviors is known (O'Connell and Hofmann, 2011b;Prior and Soma, 2015;Wild and Botelho, 2015) and the system is becoming more accessible to specific neural manipulations (Heston et al, 2018;Murugan et al, 2013;Xiao et al, 2018;Yazaki-Sugiyama et al, 2015). Additionally, previous studies in zebra finches have identified that partner preference is dependent on many neurotransmitters and other signaling molecules, including oxytocin (Klatt and Goodson, 2013;Pedersen and Tomaszycki, 2012), vasopressin (Goodson et al, 2004), cortisol (LaPlante et al, 2014, hormones (Prior and Soma, 2015) and dopamine (Adkins-Regan, 2009;Banerjee et al, 2013;Goodson et al, 2009;Iwasaki et al, 2014;Tokarev et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

D2 dopamine receptor activation induces female preference for male song in the monogamous zebra finch

Day

Saxon

Robbins

et al. 2019

Journal of Experimental Biology

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The evolutionary conservation of neural mechanisms for forming and maintaining pair bonds is unclear. Oxytocin, vasopressin and dopamine (DA) transmitter systems have been shown to be important in pair-bond formation and maintenance in several vertebrate species. We examined the role of dopamine in formation of song preference in zebra finches, a monogamous bird. Male courtship song is an honest signal of sexual fitness; thus, we measured female song preference to evaluate the role of DA in mate selection and pairbond formation, using an operant conditioning paradigm. We found that DA acting through the D2 receptor, but not the D1 receptor, can induce a song preference in unpaired female finches and that blocking the D2 receptor abolished song preference in paired females. These results suggest that similar neural mechanisms for pair-bond formation are evolutionarily conserved in rodents and birds.

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Bidirectional scaling of vocal variability by an avian cortico-basal ganglia circuit

Cited by 13 publications

References 43 publications

Blocking Opioid Receptors in a Songbird Cortical Region Modulates the Acoustic Features and Levels of Female-Directed Singing

Blocking Opioid Receptors in a Songbird Cortical Region Modulates the Acoustic Features and Levels of Female-Directed Singing

Beyond Critical Period Learning: Striatal FoxP2 Affects the Active Maintenance of Learned Vocalizations in Adulthood

D2 dopamine receptor activation induces female preference for male song in the monogamous zebra finch

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