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

Nicholson, David (Fall 2017)

Permanent URL: https://etd.library.emory.edu/concern/etds/8k71nh08w?locale=en


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


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