Experience-dependent auditory cortical map plasticity across the lifespan Open Access

Shepard, Kathryn Nancy (2014)

Permanent URL: https://etd.library.emory.edu/concern/etds/ws859g11z?locale=en


Throughout our lives, the sounds that we engage with sculpt our auditory responses. This is particularly true in auditory cortex (AC), where salient acoustic experiences can reorganize the distributions of response properties that are mapped across its surface. Though such "map plasticity" has been studied across sensory systems since the 1960s, the processes leading to its emergence are still not fully understood. This dissertation constitutes an effort to better understand the circumstances that promote map plasticity in the AC. I first examine the physiological environment that permits map plasticity during development, when mere exposure to a stimulus can be enough to drive map plasticity. While the mechanisms that render the developing AC so sensitive to its acoustic environment are incompletely understood, studies in the visual system have suggested that the neuromodulator norepinephrine (NE) may be involved. Further, recent work in the AC has connected NE to map plasticity in adult animals. The first aim of this dissertation links these two bodies of research by asking whether NE is required for map plasticity during the critical period for frequency tuning in AC development. Using the dopamine β-hydroxylase knockout mouse, which cannot produce NE, I show that NE is required for the map plasticity that follows from sound exposure during development. The second aim concerns map plasticity in adulthood. In adulthood, it is accepted that map plasticity only follows from behavioral engagement with sounds; this is generally explored through the use of laboratory conditioning paradigms in which a sound is reinforced with a reward or punishment. Here, I ask whether map plasticity occurs when a sound is made behaviorally relevant through natural experience (specifically, motherhood) rather than laboratory conditioning. In contrast to expectations based on previous work, I found that map plasticity does not occur among maternal females for any feature of their pups' ultrasonic vocalizations (USVs). Rather, more subtle plasticity in USV response magnitude emerges that may serve to suppress background neural activity when pups are calling. Taken together, this work advances our understanding of AC plasticity by establishing physiological and behavioral prerequisites for map plasticity in development and adulthood, respectively.

Table of Contents

1 Introduction 1

1.1 The anatomy of the AC 3

1.1.1 Intrinsic organization of the AC 3

1.1.2 Core versus non-core AC 5

1.1.3 The mouse AC 7

1.2 Experience-dependent map plasticity in AC 9

1.2.1 Map plasticity and auditory memory 10

1.2.2 Map plasticity during the developmental critical period in AC 14

1.2.3 Developmental versus adulthood map plasticity 17

1.3 Neuromodulation of map plasticity 19

1.3.1 Acetylcholine 191.3.2 Dopamine 211.3.3 Serotonin 211.3.4 Norepinephrine 221.3.5 Unanswered questions regarding the neuromodulation of AC plasticity 23

1.4 Summary and objectives 23

2 Norepinephrine and developmental plasticity in the auditory cortical map 25

2.1 Introduction 25

2.2 Method 27

2.3 Results 31

2.3.1 Comparable peripheral auditory responses in NE-deficient and -competent mice 31

2.3.2 Comparable baseline AC physiology in NE-deficient and competent mice 33

2.3.3 Critical period plasticity is impeded by NE deficiency 36

2.4 Discussion 38

2.4.1 NE loss affects AC organization in sound-exposed, but not baseline groups 38

2.4.2 Achieving NE deficiency using genetic versus neurotoxic lesions 40

2.4.3 Possible targets of NE 44

2.4.4 Summary 47

3 Tonotopic map plasticity in the maternal adult 48

3.1 Introduction 48

3.2 Method 51

3.3 Results 53

3.3.1 AC organization in CBA/CaJ mice 54

3.3.2 Tonotopic map in AC is stable throughout motherhood 61

3.3.3 Maternal suppression of ultrasound responses in core sites representing a lateral frequency band 63

3.4 Discussion 673.4.1 Gross organization of the CBA/CaJ mouse AC 67

3.4.2 Absence of map plasticity for ultrasounds in the maternal AC 69

3.4.3 Relationship to prior work 72

3.4.4 Summary 73

4 Plasticity for pup USV responses in the maternal adult 75

4.1 Introduction 75

4.2 Method 78

4.3 Results 79

4.3.1 Auditory cortical map of USV responses is stable across motherhood 79

4.3.2 Different vocalization exemplars evoke markedly different response profiles 82

4.3.3 The maternal A2 loses sensitivity to acoustic differences in pup USV exemplars 85

4.4 Discussion 89

4.4.1 Absence of plasticity in map of USV responses 90

4.4.2 USV processing in core versus non-core AC 91

4.4.3 A2 in auditory categorization 94

4.4.4 Summary 96

5 Conclusion 97

5.1 The mouse model of AC plasticity 97

5.2 Future use of mapping in AC research 99

5.3 The physiological relevance of map plasticity 101

5.4 NE in AC plasticity during adulthood 103

Appendix A - Common methods 106

A.1 Surgery and electrophysiological recording 106

A.2 Data processing 109

A.3 Recording site classification 110

References 113

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