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Prenatal Cocaine: Effects on Neonatal Vocalizations, Cue- Induced Maternal Response, and Brain Development

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Prenatal Cocaine: Effects on Neonatal Vocalizations, Cue- Induced Maternal Response, and Brain Development PRENATAL COCAINE: EFFECTS ON NEONATAL VOCALIZATIONS, CUE- INDUCED MATERNAL RESPONSE, AND BRAIN DEVELOPMENT Elizabeth Thomas Cox A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Curriculum of Neurobiology Chapel Hill 2012 Approved by: Dr. Josephine Johns Dr. Karen Grewen Dr. Clyde Hodge Dr. Carl J. Malanga Dr. John Gilmore Dr. P.S. Zeskind ©2012 Elizabeth Thomas Cox All Right Reserved ii ABSTRACT ELIZABETH T. COX: Prenatal Cocaine: Effects on Neonatal Vocalizations, Cue-induced Maternal Response, and Brain Development (Under the direction of Josephine M. Johns) Cocaine use in women is correlated with child neglect and abuse. Young children prenatally exposed to cocaine are reported to exhibit early signs of neurobehavioral stress and decreased response to caregivers. It is reasonable to suggest that drug-exposed infants seeking comfort from a non-nurturing caretaker might have difficulty responding to their mother/caretaker because of direct neurobehavioral effects following prenatal cocaine exposure (PCE). Animal models of cocaine- induced maternal neglect suggest rodent mothers from both drug-treated and control groups exhibit disrupted offspring-induced maternal behavior towards cocaine-exposed neonates. Results support human studies and suggest cocaine-induced changes in both mother and offspring influence the quality of maternal care and hence developmental outcome of the infant although little is understood about the mechanisms underlying these effects. Work presented here employed parallel translational studies examining behavioral responses of drug-treated mothers, their drug-exposed infants, and neurobiological mechanisms underlying behavioral differences in both human and animal models. Cries were elicited in cocaine-exposed and control human infants at one month of age and subsequently examined for variations in cry acoustics. Mothers returned to lab at three months postpartum and were tested for perceptual response to naturally occurring cries. An animal model of PCE was employed examining if PCE results in similar acoustic variations during the neonatal period and if these differential acoustic properties influence a rodent mother’s preference-like behavior. Additionally, our rodent model was used to explore early brain development in PCE and control rodent offspring during early neonatal and juvenile periods. Findings suggest in human and rodent iii neonates PCE affects early mother-infant interactions in part through changes in infant-produced vocalizations and that gestational cocaine-exposure in human and rodent mothers affects maternal responsiveness to those stimuli. Additionally results suggest variations in neuronal developmental in the Central Amygdala and Ventral Medial Hypothalamus may contribute to variations in vocalizations in juvenile but not infant rodents. These studies provide both translational value, assessment of human and rodent offspring vocalizations and maternal response, and possible mechanisms underlying behavioral effects in offspring. The objectives serve to determine how cocaine affects development in PCE offspring, nurturing behavior in mothers, and long-term offspring developmental outcome. iv To my family and friends who have never wavered in their support and encouragement. The destination would be meaningless without you coming along for the journey. v ACKNOWLEDGMENTS It would be impossible for me to express the gratitude I feel for all the people who have provided support, encouragement, and advice leading up to this moment. I would first like to thank my advisor, mentor, and friend Dr. Josephine Johns. You have provided me with so much support over the past six years (even when I was being headstrong and stubborn). You’ve provided me an amazing environment in which to learn, make mistakes, and succeed and I will forever be grateful. I would also like to thank the entire Johns’ Lab Crew: Sarah Williams, Matthew McMurray, Abigail Jamieson-Drake, Caitlin Zoghby, Pooja Makam, Marlana Radcliffe, and Thomas Jarrett. Specifically, I need to thank Dr. Sarah Williams, Dr. Matthew McMurray, and Abigail Jamieson-Drake. I cannot have imagined surviving the past six years without you three in my life. Sarah and Matt: you have not only been people I look up to and admire (for your scientific contributions and friendly advice) but you have also been my two largest personal motivators. I have been working hard and striving to do my best in a mere attempt to keep up with your brilliance. Princess Abigail, my breath of fresh air in a windowless lab, thank you does not suffice to say how much your friendship has helped me along the way. You’re an amazing person and will undoubtedly succeed at anything you do. This thesis is a product of all three of yours’ mentorship and friendship and I cannot thank you enough. I also want to thank all of my committee members: Drs. Karen Grewen, Clyde Hodge, CJ Malanga, John Gilmore, and Sandy Zeskind for the support and advice at every step along the way. Clyde, I cannot thank you enough for never closing your office door to me and letting me turn to you during my graduate student woes. I was lucky to have you as a mentor and a friend and I only hope one day I can return the favor. vi I next need to thank my mom, dad, sister, and nieces. After studying maternal behavior for the past six years I have a new found respect for everything you have done for me in my life. You’re encouragement, support, and unwavering love has given me the confidence to pursue my dreams. I also need to thank two of the best friends a girl could have: Rebekah McSwain and Britt Patterson. I don’t think I could ever voice how much your friendships have shaped my life. Thank you for being there when I needed you and even more for being there when I thought I didn’t. Lastly and maybe most importantly I need to thank Eli Lippard. You are my best friend and the love of my life. I will spend the rest of my life trying to make you proud and giving you the same level of support that you have provided me over the past six years (although I’m afraid this will be impossible). Having you with me along this journey to laugh with, wipe my tears, and ask “whose butt do I need to kick” is the sole reason why I’m a sane and happy person today. The term grateful or appreciative does not even begin to touch on how I feel and for this reason I won’t try and explain it more. Aside from the individuals mentioned above I also need to acknowledge my financial support of the National Institute of Drug Abuse, through my predoctoral fellowship (F31DA030060), Dr. Johns’ research grant (P01DA022446), and the UNC NIH Neurobiology Curriculum training grant (T32NS007431) without whose funding I would not have been able to follow my interests and complete the work reported here and elsewhere. vii TABLE OF CONTENTS TABLE OF CONTENTS ..................................................................................................... VIII LIST OF TABLES ................................................................................................................... X LIST OF ABBREVIATIONS .............................................................................................. XIII CHAPTER 1. INTRODUCTION ............................................................................................. 1 1.1. GESTATIONAL COCAINE-EXPOSURE AND EFFECTS ON HUMAN MATERNAL BEHAVIOR ...................................................................................................... 1 1.2. IMPACT OF ACOUSTIC CHANGES AND ADULT EMOTIONAL STATE ON ADULT PERCEPTION OF INFANT VOCALIZATIONS………………………..…….2 1.3. PRENATAL DRUG EXPOSURE AND INFANT BEHAVIORAL CHANGES IN HUMANS ........................................................................................................................... 4 1.4. GESTATIONAL COCAINE-EXPOSURE AND EFFECTS ON MATERNAL BEHAVIOR IN ANIMAL MODELS……. ............................................................................. 5 1.5. RODENT MATERNAL RESPONSE: IMPORTANCE OF INFANT BEHAVIOR ................ 6 1.6. NEUROBIOLOGY OF ALTERED CRYING BEHAVIOR ..................................................... 8 1.7. PRENATAL COCAINE’S KNOWN EFFECTS ON BRAIN DEVELOPMENT .................... 9 1.8. VALIDITY OF TRANSLATIONAL VALUE OF RODENT EARLY BRAIN DEVELOPMENT: HUMAN VS. RODENT ......................................................................... 10 1.9. SUMMARY ............................................................................................................................ 11 CHAPTER 2. HUMAN PCE: EFFECTS ON ONE-MONTH OLD INFANT CRIES AND THREE- MONTH POSTPARTUM MATERNAL PERCEPTION OF CRIES .............................................................................. 12 2.1. INTRODUCTION .................................................................................................................. 12 2.2. METHODS ............................................................................................................................. 15 2.3. RESULTS ............................................................................................................................... 22 viii 2.4. DISCUSSION ......................................................................................................................... 38 CHAPTER 3. RODENT PCE: EFFECTS ON RODENT PUP VOCALIZATIONS AND RODENT DAM PREFERENCE BEHAVIOR ....................................
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