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Rosario J. Marrero-Quevedo 2. Juan Manuel Bethencourth-Perez 2. Maternal cocaine abuse during pregnancy is associated to neglect, abuse, and mother-child bond disruption, which directly affects infant development; therefore, various neurobehavioral problems of children of drug-dependent parents could be attributed to inadequate maternal behavior or prenatal exposure to drugs. Thus, the aim of this research was to analyze the effects of chronic cocaine administration during pregnancy on postpartum maternal behavior. After delivery, for 15 minutes a day, during 20 days, the frequency of occurrence of 16 behavioral patterns of maternal behavior was individually recorded, using an ethogram. Cocaine slightly affected maternal behavior frequency, although it may have affected other parameters, such as latency, duration, and sequence of this behavior. Key words: Pospartum maternal behavior; cocaine; proximal indexes; motor activity and self-maintenance. Maternal Behavior MB is of vital importance in human being development and the development of other altricial species such as humans, rodents, some carnivorous and some omnivorous, as they are born underdeveloped to survive on their own. Thus, the earliest interpersonal relationship begin at birth, where mothers provide them the care necessary to survive and mature Alsina-Llanes, Brun and Olazabal, ; Wickham et al. Thereby, emotional responses are also regulated, thus favoring adequate growth and cognitive development attention, memory, learning, etc. Kristal, This abuse has a high long term negative impact on mothers, children, families and society in general. Children of mothers addicted to cocaine, present numerous alterations to their emotion, cognition, motor skills, and behavior, such as anxiety, depression, stress response complications, emotional regulation difficulties, instability, irritability, attentional deficit, oppo sitional defiant disorder, lability, anorexia and drug abuse vulnerability Ackerman, Riggins and Black, ; Bennett, Bendersky and Lewis, ; Coleman et al. The interactions are unrewarding and cause more stress, additio nally, mothers receive poor or null postnatal care Kippin, Campbell, Ploense, Knight and Bagley, Oxytocin and dopamine systems are those that mainly mediate the filial, maternal, and social behavior, reward or reinforcement and reactivity to stress Johns et al, Hence, cocaine abuse may be influencing the decrease of the maternal sensibility to their children's signals and thereby reducing maternal activity. Additionally, the main neural circuits of parental behavior in humans are the limbic- hypothalamics: the amygdala, the insula, the hypothalamus, the ventral tegmental area, the striatum, and the medial prefrontal cortex. These circuits are altered by drug abuse Johns et al, and result damaging mainly the prefrontal cortex, the orbital cortex and the anterior cingulate, involved in filial behavior and hyperreactivity to stress Strathearn and Mayes, Thus, the baby is exposed from conception to the mother's physiological and behavioral imbalance, produced by the drug, and enhanced by her dysfunctional environment. Nevertheless, the animal models with rodents would allow to isolate the different variables and to know the impact hierarchy of the distinct factors involved, which facilitates an efective approach to this problematic. Prior to birth it pertains to the preparation of the environ ment for the arrival of the ofspring, and the postpartum, triggered by endocrine and chemosensory signals such as smell, movement, and cry of the ofspring Champagne et al. Various behavioral patterns of the mother have been identified in the postpartum, such as nest building, arching her back to give warmth and facilitate breastfeeding, licking, maternal grooming, and pup retrieval to return them to the nest, eating and drinking for the mother's self-maintenance and that of the offspring, self-grooming to eliminate possible noxious elements for the ofspring, locomotion or displacement, and rest Alsina-Llanes, Brun and Olazabal, ; Angoa-Perez and Kuhn, ; Champagne et al. Variations in these behaviors, have repercussions for individual diferences that the ofspring show in their behavior and are linked to the responses of the hypothala-mic- pituitary- adrenal HPA axis, which is the main axis to respond to stress Caldji, Diorio and Meaney, Mice that during infancy have poor licking from their mother are more fearful and beget more fearful ofspring and with more reactivity to stress Champagne et al. In this way, it can be seen that greater maternal contact reduces fear and anxiety reactions in ofspring Hertenstein et al. MB is interdependent with the environment, environmen tal adversity such as food shortage, predators' presence, etc. Mothers in adverse circumstances take more time in pup retrieval; and pup licking and grooming decrease; these effects last to the 3rd generation transge-nerational efects , even in the absence of any posterior stress Champagne and Meaney, ; Champagne et al. Primates and rodents subjected to high maternal deprivation are fearful, anxious, hold inappropriate social behavior, are high aggressive and have raised vulnerability to the abuse of substances such as ethanol Sinha, ; morphine Jaworski, Francis, Brommer, Morgan and Kuhar, and various drugs which are used to reduce anxiety Kippin, Cambell, Ploense, Knight and Bagley, ; Sinha, , additionally to numerous cognitive problems such as attention deficit, slow learning between others Champagne et al. Cocaine injures MB, reduces maternal aggression: they are more submissive, attack less and threaten more. The mothers subjected to this doses used more time in self-grooming, in environmental sniffing, in rearing and they stayed more time away from the nest Johns et al. Williams and Johns , in their review, found that cocaine altered the beginning of MB, depending on the doses and the administration regimen chronic, acute or intermit tent , and its effect was seen in the first postpartum days. The various results found with similar cocaine doses can be explain by the methodological variations such as drug administration routes, gestation time, as well as the species of mice used. Those results prevented knowledge of the impact of cocaine used during pregnancy to maternal behavior in mice. The administration was subcutaneous s. After birth, all the mothers stayed with their offspring until weaning, at 21 days. Materials and instruments. Cocaine was donated by the 'Universidad Nacional de Colombia' \[National University of Colombia\] pharmaceutic analyses lab. Ethogram ofpostpartum maternal behavior, adapted from Silverman This ethogram includes 16 behavioral patterns of postpartum maternal behavior, classified by proximal behaviors that implicate contact with the offspring, motor activity which includes animal movements to roam and recognize its space and self-maintenance associated to the mother's survival:. Proximal Behaviors. Breastfeeding: the mother lays on her side or on top of her offspring to breastfeed them. Nest repair: includes: nest building, in which the female presents a temporary and spatial organization of her territory, where she accumulates sawdust in a quadrant of the box forming the nest; nest moving, which consists in moving the location; cleaning nest, the mother eats the feces or throw them out of the nest with her back or front legs. Pup retrieval: the mother returns her pups to the nest holding them with her teeth by the neck, each time that any pup gets away from it. Maternal grooming: the mother cleans the pups' bodies with her tongue or legs. Warmth for offspring: the mother provides warmth to her pups by covering them with her body. Anogenital licking: the mother licks the abdominal, anal, genital, and urinary areas to stimulate the pup defecation and urination. Pups' body sniffing: the female tracks with her nose her pups' bodies. Motor behaviors. Self-grooming: the female cleans her body with her tongue or her back or front legs. Environmental sniffing: the female sniffs the environment making head movements. Rearing: the female assumes a vertical position raising her front legs and holding herself on her back legs. Locomotion: the female moves across the cage floor. Climbing: the female walks clinging to the mesh tops of the cages with her legs. Self-maintenance behaviors. Drink: the female laps from the spout. Eat: the female consumes food from the feeder. Rest: the female reposes with her eyes closed and remains still. Sleep: the female lies coiled up with her eyes closed. On the eighth gestation day they were weight in order to randomly assign seven females to each group to the subcutaneous s. These substances were injected during the remaining 14 days ofgestation G8-G21 , in various places on the back of the neck to avoid necrotic skin lesions. The frequency of each behavioral index was recorded every 5 seconds, to get a full 15 minutes, on a modified ethogram based on the one created by Silverman In accordance to said regulations, the animals were raised only for research, the minimum number of mice required to get scientifically approved results was used. The procedures of cocaine administration were performed by trained personnel and taking strict precaution to reduce pain and prevent mistreatment. The frequency of the diverse maternal behavior MB indexes postpartum were recorded every 5 seconds, for 15 consecutive minutes, during the 20 postpartum maternal behavior days. All the statistical analysis were done using SSPS version The results of the MB frequency comparisons will be presented, beginning with proximal behaviors, following with motor behaviors, and ending with self-maintenance behaviors. The preliminary analysis of proximal behavioral pat terns of MB frequency, such as anogenital licking, pups' body sniffing, and offspring carrying, had a low frequency of occurrence during the 20 days, so they were removed from the analysis. Table 1 summarizes the MANOVA results, F values, degrees of freedom, and the p value of the 13 behavioral patterns, in the 20 observations performed of the MB in the four day groups , , and The main effects caused by chronic cocaine administration are represented with the initials CCA. Table 1 MANOVA results for the thirteen behavioral patterns ofpostpartum maternal behavior in 20 consecutive observations and the 4 day groups. When main effects were not found, the 20 observations of each behavioral pattern were grouped by 4, leaving 5 observations in each group, and they were analyzed using the repeated-measures MANOVA see table 1. Figure 1 Nest repair, breastfeeding, enviromental sniffing and self-grooming. Table 2 Repeated-measures ANOVA results to proximal behaviors: nest repair, breastfeeding, maternal grooming and warmth for offspring in 4 groupings. Since the degrees of freedom df are similar to the indexes presented, they are described in the first column. Table 3 Repeated-measures ANOVA of motor behaviors: environmental sniffing, self-grooming, locomotion, rearing and climbing in 4 groupings. Since the degrees of freedom df are similar to the presented indexes, they are described in the first column. Table 4 Repeated-measures ANOVA results of the self-maintenance behaviors: rest, sleep, drink and eat, in the four groupings. It did not affect the proximal behaviors frequency of occurrence, that are the ones directed to the offspring, or the motor activity classified as displacements or movements as either the self-maintenance ones, that are the ones directly involved with the mother's survival. Aside from this high range of behavioral patterns, that in the present study integrates the postpartum MB, the MB had the possibility of occurrence, as was assessed, due to the fact that it was observed during 20 consecutive days until weaning that occurred on day In addition, in general terms, there is a lack of studies assessing cocaine use during gestation and the consequences to MB Nephew and Febo, ; since the great majority are focused on the effects in the neurodevelopment of the ofspring of these mothers. This is because maternal behavior is too strong and resistant to numerous external factors, in this case to cocaine, due to the great importance that has on the survival of the species. It is probable that cocaine in the both tested doses, does not alter the frequency of occurrence of these behavioral patterns, though it could disturb the molecular aspects of the behavior, such as latency, sequence, duration or the various characteristics of this pattern. Such would be the case of the milk provision when breastfeeding, the depth, shape and location of the nest inside the home-box, the retrieval velocity or the latency of pup retrieval, and the minimum distance needed for the mother to react retrieving them to the nest, or in the maternal licking difference between the pups and the pups body parts that she prefers to lick, such as head, body, genitals or abdomen Champagne et al. Another possibility would be that when cocaine admi nistration is suspended after birth, maternal behavior does not alter because the effects weaken in direct correlation to drug suspension Johns et al. Nonewithstanding, seems like cocaine administration during the last 14 days of the 21 days of gestation, does not affect the frequency of occurrence of maternal behavior. The present study focuses on the analysis of MB defined by a series of muscular patterns that shows a spatial-temporal process, and through them, access to the efects of cocaine; however, the fact of not having included neurochemical, electrophysiological correlations, does not allow a clear explanation for the lack of cocaine effects in the frequency of the diverse indexes of MB. As well as neither consents to explain why the modulate brain areas and the hormones that inflects in maternal behavior were not affected by the two cocaine doses tested. So it emphasizes in the results based on similar studies where you can compare the effects of determined doses, administration routes and cocaine administration periods during gestation. It is worthwhile to highlight that the present study, in addition to having a wide range of behavioral patterns that formed the MB, only analyzed the frequency of occurrence every 5 seconds, which were finally totalized in 15 minutes. It would be convenient in future researches to include the latency, duration and sequence study of each one of these behavioral patterns, in order to notice small changes produce by cocaine during gestation. As postpartum maternal behavior was analyzed in diferent phases, from beginning, to maintenance, to decli ne, which happens at weaning Carrera-Guermeur, ; Champagne et al. And motor behaviors such as environmental sniffing and self-grooming, increased while locomotion, rearing and climbing did not change. Self-maintenance behaviors were stable throughout the observations, possibly due to their importance to both mother and ofspring survival, at least in the first days Champagne et al. As no cocaine effects were found, the variations that this study shows are normal in MB, in the phases of beginning, maintenance and decline. Both the numerous indexes of MB assessed in the present study 16 behavioral patterns , as the observation period 20 consecutive days were the two factors that prevented the comparison with other studies that had value the effects of cocaine administration in MB. Most of these researches are restricted to the analyses of determined indexes such as pup retrieval, breastfeeding, nest building to mention a few, and only during the first postpartum days Nephew and Febo, Cocaine may possibly alter other characteristics of behavioral indexes, as occurrence of latency, duration or sequence of the diverse behavioral patterns. Ackerman, J. A review of the effects of prenatal cocaine exposure among school-aged children. Pediatrics , , Adinoff, B. Altered neural cholinergic receptor systems in cocaine-addicted subjects. Neuropsychopharmacology , 35 , Alsina-Llanes, M. Developmental Psychobiology , 57 , Angoa-Perez, M. Neuronal serotonin in the regulation of maternal behavior in rodents. Neurotransmitter , 2, Bennett, D. Preadolescent health risk behavior as a function of prenatal cocaine exposure and gender. Caffrey, M. Cocaine-associated odor cue re-exposure increases blood oxygenation level dependent signal in memory and reward regions of the maternal rat brain. Drug and Alcohol Dependence , , Caldji, C. Variations in maternal care in infancy regulate the development of stress reactivity. Biology Psychiatry , 48 , Carrera-Guermeur, O. Champagne, F. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behavioral Neuroscien ce , , Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Chaplin, T. M, Visconti, K. Prenatal cocaine exposure differentially affects stress responses in girls and boys: Associations with future substance use. Development and Psychopathology , 18 , Colado, M. Drogas de abuso Capitulo En: P. Lorenzo, A. Buenos Aires: Edit. Coleman, L. Adolescent binge ethanol treatment alters adult brain regional volumes, cortical extracellular matrix protein and behavioral flexibility. Pharmacology, Biochemistry and Behavior , , Dow-Edwards, D. The effects of prenatal cocaine, post-weaning housing and sex on conditioned place preference in adolescent rats. Psychopharmacology , , Eiden, R. Maternal cocaine use and mother-infant interactions: direct and moderated associations. Neurotoxicology and Teratology , 33 , Eyler, F. Executive functioning at ages 5 and 7 years in children with prenatal cocaine exposure. Devop-mental Neuroscience , 31 , Febo, M. Development of cocaine sensitization before pregnancy affects subsequent maternal retrieval of pups and prefrontal cortical activity during nursing. Neuroscience , , Frye, C. Early postnatal stimulation alters pregnance neurosteroids in the hippocampus. Hancock, S. Early maternal separation increases symptoms of activity-based anorexia in male and female rats. Hertenstein, M. The communicative functions of touch in humans and non-humans primates and rats. A review and synthesis of empirical research. Genetic, Social and General Psychology Monographs , , Hess, C. Prenatal cocaine exposure alters maternal retrieval behavior in mice. Behavioral Genetics , 32 , Jaworski, J. Effects of early maternal separation on ethanol intake, GABA receptors and metabolizing enzymes in adult rats. Johns, J. Cocaine treatment and prenatal environment interact to disrupt intergenerational maternal behavior in rats. Behavioral Neuroscience , , Effects of chronic and acute cocaine treatment on the onset of maternal behavior and aggression in Sprague-Dawley rats. Effects of short- and long-term withdrawal from gestational cocaine treatment on maternal be havior and aggression in sprague-dawley rats. Development Neurosciences , 19 , Kinsley, C. Cocaine alters the onset and maintenance of maternal behavior in lactating rats. Phar macology Biochemistry and Behavior , 47 , Kippin, T. In Perinatal Programming of Neurodevelopment pp. New York: Springer. Kristal, M. The biopsychology of maternal behavior in nonhuman mammals. Lambert, B. Developmental and behavioral consequences of prenatal cocaine exposure: a re view. Journal of Perinatology , 32 , Lester, B. Neurobehavioral disinhibition predicts initiation of substance use in children with prenatal cocaine exposure. Drug Alcohol Dependence , , Third pathophysiology of prenatal cocaine exposure. Developmental Neuroscience , 31, Lippard, E. Early postpartum pup preference is altered by gestational cocaine treatment: Associations with infant cues and oxytocin expression in the MPOA. Behavioural Brain Research , , Lucantonio, F. The impact of orbitofrontal dysfunction on cocaine addiction. Nature Neuroscience , 15 , McMurray, M. A rodent model of cocaine's effect on the mother infant dyad. Order No. ProQuest Dissertations and Theses. Ministerio de Salud de Colombia 4 de octubre de Minnes, S. Nelson, C. A dose-response study of chronic cocaine on maternal behavior in rats. Neurotoxicology and Teratology , 20 , Nephew, B. Effects of cocaine on maternal behavior and neurochemistry. Current Neuropharmacology , 10 , Office of Applied Studies Olive, M. W Stimulation of endorphin neurotransmission in the nucleus accumbens by ethanol, cocaine, and amphetamine. The Journal of Neuroscience , 21 , Pereira, M. En Perinatal Programming of Neurodevelopment pp. Cocaine impairs maternal nest building in pregnant rats. Pharmacology Biochemist Behavior , 58 , Richardson, G. Neurotoxicology and Teratology , 40 , Arginine vasopressin gene expression changes within the nucleus accumbens during environment elicited cocaine-conditioned response in rats. Neuropharmacology , 58 1 Silverman, M. New York: Lancet. Sinha, R. Chronic stress, drug use and vulnerability to addiction. Annals of the New York Academy of Sciences , , Stamatakis, A. Rat dams exposed repeatedly to a daily brief separation from the pups exhibit increased maternal behavior, decreased anxiety and altered levels of receptors for estrogens ERa, ERP , oxytocin and serotonin 5-HT1A in their brain. Psychoneuroendocrinology , 52 , Strathearn, L. Cocaine addiction in mothers: potential effects on maternal care and infant development. Annals of the New York Academic Sciences. Szyf, M. Nongenetic inheritance and transgenerational epigenetics. Trends in Molecular Medicine , 21 , Toth, M. Mechanisms of non-genetic inheritance and psychiatric disorders. Neuropsychopharmacology , 40 , Wang, Z. Maternal behavior is impaired in female mice lacking type 3-adenylylcyclase. Neuropsy-chopharmacology , 36 , Wickham, M. Maternal depressive symptoms during childhood and risky adolescent health behaviors. Williams, S. Prenatal and gestational cocaine exposure: Effects on the oxytocin system and social behavior with implications for addiction. Prenatal cocaine disrupts serotonin signaling-dependent behaviors: Implications for sex differences, early stress and prenatal SSRI exposure. Current Neuropharmacology , 9, DOI: This is an open-access article distributed under the terms of the Creative Commons Attribution License. Services on Demand Journal. Abstract Maternal cocaine abuse during pregnancy is associated to neglect, abuse, and mother-child bond disruption, which directly affects infant development; therefore, various neurobehavioral problems of children of drug-dependent parents could be attributed to inadequate maternal behavior or prenatal exposure to drugs. Data Analysis The frequency of the diverse maternal behavior MB indexes postpartum were recorded every 5 seconds, for 15 consecutive minutes, during the 20 postpartum maternal behavior days. RESULTS The results of the MB frequency comparisons will be presented, beginning with proximal behaviors, following with motor behaviors, and ending with self-maintenance behaviors. How to cite this article.
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