Cerebellothalamic and thalamostriatal projections in a songbird, the Bengalese Finch Open Access

Abstract

Like a child learning to speak, songbirds learn their songs as juveniles from adult tutors. They then perfect their song by practicing it thousands of times during development. This behavior makes songbirds an excellent model system through which neuroscientists can understand how the brain learns and produces a motor skill that resembles speech. Birdsong is under the control of a network of nuclei in the songbird brain known as the song system. To what extent is the song system like motor systems in the mammalian brain? Many studies have shown how a thalamocortical-basal ganglia loop in the song system known as the Anterior Forebrain Pathway (AFP) contributes to learning song and adaptively maintaining it in adulthood. In mammals, the basal ganglia receive input from the thalamus, including thalamic regions that receive output from the cerebellum. It is unknown whether the basal ganglia nucleus of the song system, Area X, receives thalamic input, or whether such inputs might be used to convey cerebellar outputs to the song system. I first demonstrate that the cerebellum projects to dorsal thalamus in the Bengalese finch, and provide the first detailed description of the cerebellothalamic projections. Then, using a viral vector that specifically labels presynaptic axon terminals, I demonstrate that dorsal thalamus projects to the striatum. To determine the sources and targets of the thalamostriatal system in songbirds, I use tracers to map thalamic regions and immunohistochemistry to identify song system nuclei. I find that DLM and immediately adjacent DTCbN project to Area X. In contrast, more medial and ventral subregions of DTCbN project to striatum outside Area X. These results suggest that in the AFP the basal ganglia integrates feedback from the thalamic region to which it projects as well as input from thalamic regions that receive cerebellar output, much like the mammalian basal ganglia.

Table of Contents

List of Figures and Tables             xiv

List of Abbreviations      xvii

I              Introduction      1

I.1          Songbirds as a model system     2

I.1.A      Parallels between birdsong, speech, and similar motor skills         2

I.1.A.1  Sensorimotor learning  3

I.1.A.2  Social interaction            5

I.2          The song system as a general model of motor systems   6

I.2.A.1  The motor system in mammals 8

I.2.A.2  The song system in songbirds    11

I.2.A.3  The basal ganglia in mammals and songbirds      13

I.2.A.3.a              Mammalian basal ganglia anatomy         14

I.2.A.3.b              Songbird basal ganglia anatomy 15

I.2.A.3.c               Basal ganglia output to motor thalamus 20

I.2.A.3.d              Basal ganglia output to thalamus in the AFP        23

I.2.A.3.e              Basal ganglia function and theoretical models    25

I.2.A.3.f Reinforcement learning in the AFP          32

I.2.A.4  The thalamostriatal system: anatomy, physiology, and theories about computation          34

I.2.A.4.a.1           Anatomy: two types of thalamostriatal projection neurons          34

I.2.A.4.a.2           Anatomy: afferents of the intralaminar nuclei     39

I.2.A.4.a.3           Physiology and function of the thalamostriatal system   41

I.2.A.5  Cerebellum: anatomy, physiology, and theories about computation         43

I.2.A.5.a.1           Cerebellothalamic system: anatomy       46

I.2.A.5.a.2           Cerebellothalamic system: physiology and proposed function     54

I.2.A.5.a.3           Other relevant cerebellar pathways        59

I.2.A.5.a.4           Cerebellar function in speech    61

I.2.A.5.b              Possible interactions between the basal ganglia and cerebellum 63

I.2.A.5.c               Motor control of speech              64

I.2.B      Open question about the song system: does the song system contain a thalamostriatal projection?           68

I.2.B.1.a               Evidence for a thalamostriatal system in birds    69

I.2.C      Open question about the song system: is there a route through thalamus from the cerebellar nuclei to the song system?    76

I.2.D      Non-classical components of the song system    77

I.2.D.1  Descending motor pathways in the avian brain  77

I.2.D.2  Other connections          82

I.2.D.3  Hypothesized evolutionary origins of neural pathways for vocal behavior               83

I.3          Overview of studies in this dissertation 84

II            Methods            86

II.1         Surgery and tissue collection.     86

II.2         Immunohistochemistry 88

II.3         Production and specificity of antisera     89

II.4         Microscopy, digital photography, and image processing. 92

II.5         “Drawings” of signal from lentiviral injections.   93

II.6         Map of dorsal thalamus 94

III           Results 96

III.1       The cerebellar nuclei in Bengalese Finches project to dorsal thalamus     96

III.1.A   CbL projects to dorsal thalamus 96

III.1.B   CbI and CbM also project to dorsal thalamus       100

III.2       Dorsal thalamus in Bengalese Finches projects to Area X 103

III.2.A   DLM and the immediately adjacent DTCbN project to Area X       105

III.2.B   More medial and ventral DTCbN projects to medial striatum outside of Area X    107

IV           Discussion          109

IV.1       Technical considerations, and relation to previous work 110

IV.1.A   Cerebellothalamic projections   110

IV.1.B   Thalamostriatal projections        112

IV.1.C   Disynaptic pathway from CbN to Area X through DTCbN 115

IV.2       Functional implications and future studies           117

IV.2.A   Thalamostriatal projections        117

IV.2.A.1 Microcircuitry of Area X, including thalamostriatal projections: ultrastructural studies      117

IV.2.A.2 Topography and morphology of thalamostriatal projections: single-cell reconstruction studies     119

IV.2.A.3 Cell types in Area X targeted by thalamostriatal projections: immunohistochemical studies           122

IV.2.A.4 Subcortical inputs to dorsal thalamus: retrograde tracer and immunohistochemical studies           125

IV.2.A.5 Efferents of dorsal thalamic subregions: studies with iontophoretic injections of AAV       126

IV.2.A.6 Physiology of thalamostriatal projections             127

IV.2.A.7 Determine nature of information relayed to DLM and DTCbN by subcortical inputs            131

IV.2.B   Cerebellothalamic projections   132

IV.2.B.1 Is the projection from CbN to thalamus glutamatergic? Can immunostain for glutamatergic and GABAergic inputs to dorsal thalamus serve as a proxy for pallidal and cerebellar inputs? A combined tracer and immunohistochemical study.     133

IV.2.B.2 Disynaptic pathways from CbN to the forebrain through thalamus: a study with transsynaptic tracers       134

IV.2.B.3 Specificity of projections of the cerebellar nuclei: tracer studies 135

IV.2.B.4 Does the cerebellum interact with VTA? 137

IV.2.B.5 Disynaptic pathways from CbN to the forebrain through thalamus: physiological studies 139

IV.2.B.6 Does the cerebellum or red nucleus interact with phonatory or respiratory nuclei in the brainstem? Tracer studies 140

IV.2.B.7 Cerebellar involvement with beak movements: behavioral and physiological studies         141

IV.2.B.8 Is the cerebellum involved in sensorimotor learning or in social interaction?         145

IV.2.B.9 Does the cerebellum co-ordinate dancing during song?  147

IV.2.C   Functional considerations and conclusions           149

IV.2.C.1 Cerebellothalamic system           149

IV.2.C.2 Thalamostriatal projections        150

V            Appendices       152

V.1        Introduction      152

V.2        Afferents and efferents of the Bengalese finch cerebellar nuclei 152

V.2.A    Comparison of projections of CbL and CbI to dorsal thalamus      152

V.2.B    SpM sends collaterals to dorsal thalamus             154

V.2.C    CbL projects to several other regions in the midbrain      156

V.2.D    Input from cerebellar folia to CbL             160

V.3        Regions of dorsal thalamus in Bengalese finches 161

V.3.A    DLM as defined by projections from Area X          161

V.3.B    DIP as defined by projections from globus pallidus            163

V.4        Relation of CbL projections to other song system nuclei in dorsal thalamus           165

V.4.A    CbL axon terminals in some cases closely appose thalamic neurons retrogradely labeled by injections in Area X               165

V.4.B    CbL does not project to thalamic song system nucleus DMP         167

V.4.C    CbL does not project to thalamic song system nucleus Uva           169

V.4.D    CbN axon terminals closely appose dendrites and soma of neurons in dorsal thalamus that project to nidopallium       171

V.4.E     Lentiviral vector injections in DIVA labeled HA    173

V.4.F     Discussion of additional anatomical results          174

V.5        Possible cerebellar contributions to song              176

V.5.A    Electrolytic lesions of CbL do not produce gross distortions of song           176

V.5.B    Electrolytic lesions of CbL can have long term effects on acoustic parameters      178

V.5.C    Electrolytic lesions of CbL do not impair the ability to change song in response to aversive reinforcement experiments     179

V.5.D    Discussion of results from electrolytic lesions of CbL        179

V.6        Additional methods       181

V.6.A    Additional stereotactic co-ordinates and tracer injection methods            181

V.6.B    Electroylytic lesions of CbL          182

V.6.C    Histology and estimate of size of CbL lesions       182

V.6.D    Measurement of effect of CbL lesions on acoustic parameters    183

V.6.E     Aversive reinforcement experiments     184

VI           References        187

About this Dissertation

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School	Laney Graduate School
Department	Biological and Biomedical Sciences
Subfield / Discipline	Neuroscience
Degree	Ph.D.
Submission	Dissertation
Language	English
Research Field	Biology, Neuroscience
Keyword	motor learning cerebellum vocalization thalamostriatal basal ganglia songbird
Committee Chair / Thesis Advisor	Sober, Samuel, Emory University
Committee Members	Liu, Robert, Emory University Medina, Javier, Emory University Jaeger, Dieter, Emory University Hess, Ellen, Emory University

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