Dopamine regulation of human speech and bird song: a critical review

Abstract

To understand the neural basis of human speech control, extensive research has been done using a variety of methodologies in a range of experimental models. Nevertheless, several critical questions about learned vocal motor control still remain open. One of them is the mechanism(s) by which neurotransmitters, such as dopamine, modulate speech and song production. In this review, we bring together the two fields of investigations of dopamine action on voice control in humans and songbirds, who share similar behavioral and neural mechanisms for speech and song production. While human studies investigating the role of dopamine in speech control are limited to reports in neurological patients, research on dopaminergic modulation of bird song control has recently expanded our views on how this system might be organized. We discuss the parallels between bird song and human speech from the perspective of dopaminergic control as well as outline important differences between these species.

Figure 1

Comparative anatomy of human (A) and songbird (B) brain organization with the emphasis on the basal ganglia structures. Ac - accumbens; B - nucleus basalis; Cd -caudate nucleus; CDL - dorsal lateral corticoid area; E - ectostriatum; GP - globus pallidus (i - internal segment; e - external segment); HA - hyperstriatum accessorium; Hp - hippocampus; HV - hyperstriatum ventrale; HVC – HVC nucleus; IHA - interstitial hyperstriatum accessorium; L2 - field L2; LMAN – lateral magnocellular nucleus of anterior nidopallium; OB - olfactory bulb; Pt - putamen; RA – robust nucleus of arcopallium; SN – substantia nigra; STN – subthalamic nucleus. Modified and reprinted by permission from Macmillan Publishers Ltd: Jarvis et al., Nature Reviews Neuroscience, 2005.

Figure 2

Block diagrams of basal ganglia networks related to control of production of human speech (A) and bird singing (B). Individual brain regions are represented in each block; red arrows indicate excitatory (glutamatergic) projections; black arrows indicate inhibitory (GABAergic projections); green arrows indicate dopaminergic input. In (A), the projection from the LMC to the nucleus ambiguus has been described in humans only. In (B), the vocal pallidum is represented within Area X; the subthalamic nucleus and substantia nigra pars reticulata are not considered integral components of bird song system. LMAN – lateral magnocellular nucleus of anterior nidopallium; MMAN – medial magnocellular nucleus of anterior nidopallium; RA – robust nucleus of arcopallium; aDLM – anterior part of the dorsal lateral nucleus of mediodorsal thalamus; DIP -dorsointermedius posterior nucleus of the thalamus.

Figure 3

Projections of the LMC to and from the basal ganglia. (A) depicts a lateral view of the rhesus monkey brain with the regions indicating the laryngeal motor cortex (encircled L for larynx); (B) shows projections from the LMC to the putamen and caudate nucleus in the rhesus monkey; (C) shows projections from the limbic striatum, substantia nigra, and ventral tegmental area to the LMC in the rhesus monkey; (D) depicts LMC in humans with multi-color dots indicating the peaks of activation as described in functional MRI studies of voice and speech production; (E) depicts connections between the LMC and basal ganglia in humans with red showing the strongest connectivity and blue showing the weakest connectivity between the brain regions. Cd – caudate nucleus; Pt – putamen; SI – substantia innominata: SN – substantia nigra; VTA – ventral tegmental area. Modified and reprinted with permissions from Elsevier, SAGE Publications Ltd, and the Journal of Neuroscience. Simonyan and Jurgens, 2003, 2005; Simonyan et al., 2005; Simonyan and Horwitz, 2011.

Figure 4

Dopamine release to the songbird striatum during singing. Photograph of the sagittal section of the songbird brain showing the placement of the microdialysis probe track in Area X of the striatum. The bar graph depicts the extracellular dopamine levels in Area X during undirected and directed singing without and with dopamine reuptake transporter blocker, nomifensine. Reprinted with permission from publisher. Modified and reprinted with permission from the Journal of Neuroscience, Sasaki et al., 2006.