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

Sandeep Kumar,Vasav Arora,Arvind Singh Pundir,Mukta Kumari,Soumya Iyengar,Uzma Din,Atanu Datta,Alok Nath Mohapatra,Sudha Sharma

doi:10.3389/fnins.2020.554094

Abstract

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.

Highlights

The cortico-basal ganglia (CBG) circuitry is known to be involved in many cognitive functions such as motivation, reward-based learning and the execution of motor functions including speech and vocalization (Doupe and Kuhl, 1999; Kao et al, 2005; Van Lancker Sidtis et al, 2006; Ziegler and Ackermann, 2017)
Earlier studies (Nottebohm et al, 1982; Bottjer et al, 1989; Vates and Nottebohm, 1995) had demonstrated that besides projecting to RA, magnocellular neurons in LMAN project to Area X, which is similar to the cortico-striatal pathway (Figure 1A)
Since all three doses of naloxone infused in LMAN led to significant decreases in the number of FD songs, we wanted to study whether this decrease resulted from low levels of the motivation to sing or reduced visual attention toward females

Summary

Introduction

The cortico-basal ganglia (CBG) circuitry is known to be involved in many cognitive functions such as motivation, reward-based learning and the execution of motor functions including speech and vocalization (Doupe and Kuhl, 1999; Kao et al, 2005; Van Lancker Sidtis et al, 2006; Ziegler and Ackermann, 2017). The song control system (SCS, Nottebohm et al, 1976; Figure 1A), a specialized set of neural circuits in songbirds such as zebra finches (Taeniopygia guttata), has been utilized extensively to understand mechanisms underlying vocal learning and vocalization (Simpson and Vicario, 1990; Brainard and Doupe, 2000; Bolhuis et al, 2010) Of these circuits, the anterior forebrain pathway (AFP) has been studied in detail for its role in song learning and context-dependent singing in adulthood (Jarvis et al, 1998; Kao and Brainard, 2006) and is strikingly similar to the mammalian CBG (Farries and Perkel, 2002; Carrillo and Doupe, 2004; Gale et al, 2008; Person et al, 2008; Kumar and Iyengar, 2018). Whereas Area X receives projections from a specific subset of neurons in the pallial nucleus HVC (Nottebohm et al, 1982; Dutar et al, 1998), another set of HVC neurons project to the premotor nucleus RA (robust nucleus of the arcopallium), (Bottjer et al, 1989; Fortune and Margoliash, 1995), forming the vocal motor pathway (VMP) which innervates the syrinx or vocal organ (Nottebohm et al, 1976; Wild, 1993)

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Conclusion