Fundamental motor patterns of the mammalian fetus.

Techniques that permit direct observation of fetuses in vivo recently have expanded our understanding of prenatal behavioral development in mammals. Although fetal motor activity seems to lack the dynamic, goal-directed character of postnatal behavior, the dimensions that define behavioral organization after birth are applicable to the movements expressed by fetuses. Fetal activity exhibits temporal, sequential, and spatial organization that emerges between the inception of movement and term. Fetal rodents, for example, exhibit coordinated motor patterns antecedent to postnatal righting, locomotion, suckling, maternal-infant communication and grooming behavior, while other action patterns appear to be functional adaptations to the intrauterine niche. Fetuses also are behaviorally responsive to sensory stimulation and changes in environmental conditions in utero. Expression of these behavioral properties emphasizes continuity between prenatal and postnatal life while implying an adaptive role for behavior before birth.     

Gene expression studies of developing bovine <Emphasis Type="Italic">longissimus</Emphasis>muscle from two different beef cattle breeds

Background  

The muscle fiber number and fiber composition of muscle is largely determined during prenatal development. In order to discover genes that are involved in determining adult muscle phenotypes, we studied the gene expression profile of developing fetal bovine longissimus muscle from animals with two different genetic backgrounds using a bovine cDNA microarray. Fetal longissimus muscle was sampled at 4 stages of myogenesis and muscle maturation: primary myogenesis (d 60), secondary myogenesis (d 135), as well as beginning (d 195) and final stages (birth) of functional differentiation of muscle fibers. All fetuses and newborns (total n = 24) were from Hereford dams and crossed with either Wagyu (high intramuscular fat) or Piedmontese (GDF8 mutant) sires, genotypes that vary markedly in muscle and compositional characteristics later in postnatal life.     

Activity of Acetylcholinesterase in the Motor-Sensory Cortex in Early Ontogenesis of Rats Exposed to Prenatal Hypoxia

Effects of acute prenatal hypoxia (13–14 days of gestation, 3 h, O₂ = 7%) on acetylcholinesterase (AChE, EC 3.1.1.7) activity in homogenates, synaptosomes, and cytosol of the motor-sensory cortex of Wistar rats were studied on the days 1, 5, 10, 19 and 30 after birth. In homogenates of normally developing cortex, the AChE activity did not significantly change with age. Activity of AChE in synaptosomes increased 4 times throughout the entire period of observation, while in the cytosol, 4.3 times to reach maximum at the 19th day. Maximum rise of the AChE activity in synaptosomes was observed at the period from the 5th to the 10th day. Activity of AChE in homogenate and synaptosomes of rats submitted to prenatal hypoxia decreased during the first five days after birth (p < 0.001) but later, starting from the day 10, it increased in all fractions. A statistically significantly higher activity of AChE than in controls was revealed in homogenate of the motor-sensory cortex on day 19 (p < 0.01), while in synaptosomes, on the days 19 and 26 (p < 0.001 and p < 0.05, respectively), and in cytosol, on the days 10, 26, and 30 (p < 0.05, p < 0.05, and p < 0.001). Maximum change in the ratio of AChE activities in cytosol and synaptosomes was found on the day 19 (p < 0.01). At the same period of development, changes in the ratio of AChE activity in synaptosomes and homogenate of the control and hypoxic animals were also observed. Thus, prenatal hypoxia leads to in changes in the activity both of the cytosol and synaptosomal membrane-bound forms of AChE in the motor-sensory cortex of rats, which agrees with our own and literature data on disorder of neuro- and neuritogenesis in the process of formation of CNS and of behavioral reactions in early postnatal ontogenesis under the effect of pathogenic factors at certain days of prenatal ontogenesis.     

Postnatal penile growth concurrent with mini-puberty predicts later sex-typed play behavior: Evidence for neurobehavioral effects of the postnatal androgen surge in typically developing boys

The masculinizing effects of prenatal androgens on human neurobehavioral development are well established. Also, the early postnatal surge of androgens in male infants, or mini-puberty, has been well documented and is known to influence physiological development, including penile growth. However, neurobehavioral effects of androgen exposure during mini-puberty are largely unknown. The main aim of the current study was to evaluate possible neurobehavioral consequences of mini-puberty by relating penile growth in the early postnatal period to subsequent behavior. Using multiple linear regression, we demonstrated that penile growth between birth and three months postnatal, concurrent with mini-puberty, significantly predicted increased masculine/decreased feminine behavior assessed using the Pre-school Activities Inventory (PSAI) in 81 healthy boys at 3 to 4 years of age. When we controlled for other potential influences on masculine/feminine behavior and/or penile growth, including variance in androgen exposure prenatally and body growth postnally, the predictive value of penile growth in the early postnatal period persisted. More specifically, prenatal androgen exposure, reflected in the measurement of anogenital distance (AGD), and early postnatal androgen exposure, reflected in penile growth from birth to 3 months, were significant predictors of increased masculine/decreased feminine behavior, with each accounting for unique variance. Our findings suggest that independent associations of PSAI with AGD at birth and with penile growth during mini-puberty reflect prenatal and early postnatal androgen exposures respectively. Thus, we provide a novel and readily available approach for assessing effects of early androgen exposures, as well as novel evidence that early postnatal aes human neurobehavioral development.     

Growth,development, and parental care in the western tarsier (Tarsius bancanus) in captivity: Evidence for a “slow” life-history and nonmonogamous mating system

I studied reproduction, prenatal and postnatal growth rates, behavioral ontogeny, and parental care in nine captive births to two wild-caught pairs of Tarsius bancanusover a 5-year period. T. bancanusinvariably gives birth to a single infant of approximately 20% maternal body mass after an extremely long gestation period. The fetal growth rate is among the slowest recorded for any mammal and the relative postnatal growth rate to physical maturity is the lowest in a sample of 26 prosimian species examined. These life-history variables, and a slow rate of reproduction, contribute to an extremely low г _max in this and other species of Tarsius.The relative rate of behavioral development, especially foraging and locomotor behaviors, is extremely rapid for a specialized predator. Infants attained nutritional independence at approximately 80 days and perfected hunting skills without apparent help from either parent. Mothers were very protective of their young and kept fathers from having contact with infants through heightened agonism after birth, and thus , there was no evidence of direct paternal care. The data suggest that there is an energetic/dietary basis for slow pre- and postnatal growth rates, but an extremely large neonatal brain size enables the rapid behavioral development and neuromuscular coordination necessary for this specialized predator to attain early nutritional independence. The captive and field data also suggest that extremely restrictive conditions exist for the purported monogamous mating system of T. bancanusand that an alternative mating system is more likely.     

Supraspinal influence on the development of motor behavior in the fetal lamb

To examine the involvement of supraspinal inputs in the maturation of motor activity patterns in the developing fetal lamb, we recorded spontaneous electromyographic activity from spinally innervated muscles at approximately 45, 65, and 95 days gestation (G45, G65, and G95; term = 147 days). At G45, fetal activity occurred in synchronized activity-inactivity cycles of approximately 2 min duration, with the activity phase lasting 22.2 ± 4.8 s and the inactivity phase lasting 95.4 ± 13.3 s (mean ± standard error of the mean, n = 5). At G65 and G95, the organization of activity was clearly different from that at G45 in that it was no longer cyclic, nor was the discharge of different muscles synchronized. By contrast, after spinal cord transection at G62, synchronised cyclic activity occurred in muscles innervated by segmental levels below the transection, both at G65 and G95. At G65 the duration of the activity phase of the cycle was 53.5 ± 6.0 s, while the inactivity phase lasted 171.6 ± 22.1 s; these durations did not alter between G65 and G95. Since spinal cord transection leads to the motor behavior of the G65 fetus reverting to the cyclic pattern characteristic of the G45 fetus, we conclude that supraspinal inputs begin to modulate the output of the spinal pattern generators at some stage between G45 and G65. The observation that spinally transected fetuses generate identical behavior at G65 and G95, both in terms of its cyclic character and the duration of cycles, suggests that spinal circuits undergo little autonomous development overthis period; that is, the altered behavior observed in the developing intact fetus reflects the influence of supra-spinal inputs on the motor circuits of the spinal cord. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 276–288, 1997     

Semi-natural and enclosed groups of Macaca mulatta: a behavioral comparison

Differences in aggression and grooming frequencies between enclosed and semi-natural groups of Macaca mulatta were studied quantitatively. Group composition, group densities and time of day were held constant. Results indicated that semi-natural monkey groups were significantly more aggressive, while enclosed groups exhibited significantly higher grooming frequencies. These results raise the question: Do alterations in behavioral frequencies lead to changes in social behavior patterns and group social organization?     

Patterns of muscle activity during different behaviors in chicks: implications for neural control

The large behavioral repertoire that spans the embryonic and postembryonic stages of development make chicks an ideal system for identifying patterns of muscle activity that are common to different behaviors and those that are behavior-specific. The main goal of this work was to identify the similar and dissimilar aspects of the recruitment patterns and the regulation of muscle activity during three distinct postembryonic behaviors: walking, swimming and airstepping. We identified two synergies that were common to each of these behaviors. The synergies were not disrupted by the absence of FT1 activity in airstepping. Within each synergy the recruitment time, recruitment order and duration of activity were not rigid, but varied according to the context-specific resistance that the leg encountered. Unlike the other muscles, FT2 activity was not recruited as part of the same synergy in each behavior. When weight-bearing contact with the substrate did not occur, as in swimming and airstepping, as well as in walking in chicks with deafferented legs, FT2 activity was not recruited as part of either synergy, but was recruited during the time between them. Although not identical, embryonic motility and hatching motor pattern both show the two synergies described for the postembryonic behaviors. Like the latter behaviors, the synergies tolerated the absence of activity from specific muscles. Thus, we suggest that the CNS produces different behaviors using many of the same muscles by organizing the patterned activity around two common synergies while permitting the different muscles that participate in a synergy to be modified in tandem or on an individual basis. Furthermore, the common synergies are established early during prenatal development in chicks.Abbreviations aIF anterior iliofibularius - CF caudilioflexorius - CNS central nervous system - EMG electromyogram - FT femorotibialis - GL gastrocnemius lateralis - P1 protraction 1 - P2 protraction 2 - pIF posterior iliofibularis - R retraction - SA sartorius - TA tibialis anterior - pIF posterior iliofibularis - ms millisecond     

Choline kinase activity in the developing rat spinal cord: differential development of hemicholinium-3 sensitive and insensitive activity.

Abstract— Choline kinase (ATP:cholinephosphotransferase; EC 2.7.1.32) activity was measured in preparations of lumbar spinal cord from rats ranging in development from 12 days of gestation to 46 days of age. The enzyme activity was measured with a radiochemical assay procedure suitable for whole tissue preparations which are rich in ATP-metabolizing enzymes. Total choline kinase activity was further differentiated into hemicholinium-3 (HC-3) sensitive and HC-3 insensitive components. The specific activity of choline kinase (unhibited) increased 3-fold during the prenatal period and subsequently decreased to relatively low levels by birth. There was no significant change in choline kinase activity throughout the postnatal period. The ontogenetic patterns for the HC-3 sensitive and HC-3 insensitive components of choline kinase activity had transient peaks in activity during the prenatal period; however, these peaks in specific activity for the 2 components were 2–3 days out of phase temporally. HC-3 insensitive activity reached a peak at 18 days of gestation while the HC-3 sensitive activity peaked at 2CL21 days of gestation. In the 10-day-old rat, the apparent choline K_m values were 0.56 and 0.16 MM for the total activity, 0.58 and 0.13 mM for the HC-3 insensitive activity, and 0.47 for the HC-3 sensitive activity.     

Interactive effects of prenatal cocaine and nicotine exposure on maternal toxicity,postnatal development,and behavior in the rat

Two experiments were performed to investigate the interactive effects of prenatal coadministration of cocaine hydrochloride (C) and nicotine tartrate (N). Experiment I was designed to determine doses of C and N that could be coadministered without altering maternal gestational parameters and/or fetal viability. Exposure of Sprague-Dawley rats to combined high-dose C (20 mg/kg) and high-dose N (5.0 mg/kg) on gestation days 8–21 was not more toxic to dam or fetus than that of exposure to C alone. Experiment II investigated pregnancy outcome, postnatal development, and behavior of the offspring following drug exposure to either high-dose cocaine (20 mg/kg: CS), high-dose nicotine (5.0 mg/kg: NS), or both (NC) on gestation days 8–21. N was administered by osmotic minipump and C by sc injection. Saline-injected dams, fitted with saline-filled pumps (SS), and untreated dams, pair-fed (PF) to NC females, served as controls. Alterations in maternal variables were limited to a 10–15% decrease in food consumption in NC and CS groups. Pregnancy outcome and birth statistics were unaffected by prenatal treatment, as was offspring body weight during the first four postnatal weeks. However, the development of surface righting was delayed in CS pups, and only CS offspring were underresponsive to the stimulatory effects of dopamine agonists on activity and stereotypy. Behavioral responses to N challenge were similar in all groups. In addition, only CS offspring showed altered behavioral responses in a spontaneous alternation task. Treatment effects on dopamine D₁ and D₂ binding in the caudate nucleus were not observed. The combination of N and C did not exacerbate any of the behavioral changes seen in CS offspring. These results support the hypothesis that C is a behavioral teratogen in rodents, and suggest that in the present model, nicotine can mitigate some of the consequences ofin utero exposure to cocaine.     

Neural mechanism for generating and switching motor patterns of rhythmic movements of ovipositor valves in the cricket

In adult female crickets (Gryllus bimaculatus), rhythmic movements of ovipositor valves are produced by contractions of a set of ovipositor muscles that mediate egg-laying behavior. Recordings from implanted wire electrodes in the ovipositor muscles of freely moving crickets revealed sequential changes in the temporal pattern of motor activity that corresponded to shifts between behavioral steps: penetration of the ovipositor into a substrate, deposition of eggs, and withdrawal of the ovipositor from the substrate. We aimed in this study to illustrate the neuronal organization producing these motor patterns and the pattern-switching mechanism during the behavioral sequence. Firstly, we obtained intracellular recordings in tethered preparations, and identified 12 types of interneurons that were involved in the rhythmic activity of the ovipositor muscles. These interneurons fell into two classes: ‘initiator interneurons’ in which excitation preceded the rhythmic contractions of ovipositor muscles, and ‘oscillator interneurons’ in which the rhythmic oscillation and spike bursting occurred in sync with the oviposition motor rhythm. One of the oscillator interneurons exhibited different depolarization patterns in the penetration and deposition motor rhythms. It is likely that some of the oscillator interneurons are involved in producing different oviposition motor patterns. Secondly, we analyzed oviposition motor patterns when the mecahnosensory hairs located on the inside surface of the dorsal ovipositor valves were removed. In deafferented preparations, the sequential change from deposition to withdrawal did not occur. Therefore, the switching from deposition pattern to withdrawal pattern is signaled by the hair sensilla that detect the passage of an egg just before it is expelled.     

Life history and locomotion in Cebus capucinus and Alouatta palliata

As an individual matures from birth to adulthood, many factors may influence the positional repertoire. The biological and behavioral changes that accompany a growing individual are expected to influence foraging strategy, social status and interaction, diet, predator avoidance strategies, and ultimately positional behavior as a behavioral link between anatomy and the environment. In this work, positional behavior is considered as an important feature of life history in juvenile and adult white‐faced capuchins (Cebus capucinus) and mantled howling monkeys (Alouatta palliata) inhabiting the same tropical forest in Costa Rica. During growth and development ontogenetic changes in body size, limb proportions, and motor skills are likely to influence locomotion and posture through the arboreal canopy. I collected data on positional behavior, activity, branch size, branch angle, and crown location during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Life history timing and differences in rates of growth did not predictably influence the development of adultlike positional behaviors in Cebus and Alouatta. Young Cebus resembled the adult pattern of positional behavior by 6 months of age while howlers exhibited significant differences in several positional behavior categories through 24 months of age. The positional repertoire of both species revealed similarities in the types of modes used during feed/forage and travel in juveniles and adults. Data presented here suggest that the environment exerts different pressures on growing Cebus and Alouatta that may relate to diet, energy expenditure, foraging skill, and/or social learning. Am J Phys Anthropol, 2009 © 2009 Wiley‐Liss, Inc.     

Clinical implications of the organizational and activational effects of hormones

Debate on the relative contributions of nature and nurture to an individual's gender patterns, sexual orientation and gender identity are reviewed as they appeared to this observer starting from the middle of the last century. Particular attention is given to the organization-activation theory in comparison to what might be called a theory of psychosexual neutrality at birth or rearing consistency theory. The organization-activation theory posits that the nervous system of a developing fetus responds to prenatal androgens so that, at a postnatal time, it will determine how sexual behavior is manifest. How organization-activation was or was not considered among different groups and under which circumstances it is considered is basically understood from the research and comments of different investigators and clinicians. The preponderance of evidence seems to indicate that the theory of organization-activation for the development of sexual behavior is certain for non-human mammals and almost certain for humans. This article also follows up on previous clinical critiques and recommendations and makes some new suggestions.     

Development of glycogen and phospholipid metabolism in fetal and newborn rat lung.

Glucose, a major metabolic substrate for the mammalian fetus, probably makes significant contributions to surface active phospholipid synthesis in adult lung. We examined the developmental patterns of glycogen content, glycogen synthase activity, glycogen phosphorylase activity and glucose oxidation in fetal and newborn rat lung. These patterns were correlated with the development of phosphatidylcholine synthesis, content and the activities of enzymes involved in phosphatidylcholine synthesis. Fetal lung glycogen concentration increased until day 20 of gestation (term is 22 days) after which it declined to low levels. Activity of both glycogen synthase I and total glycogen synthase (I + D) in fetal lung increased late in gestation. Increased lung glycogen concentration preceded changes in enzyme activity. Glycogen phosphorylase a and total glycogen phosphorylase (a + b) activity in fetal lung increased during the period of prenatal glycogen depletion. The activity of the pentose phosphate pathway, as measured by the ratio of CO2 derived from oxidation of C1 and C6 of glucose, declined after birth. Fetal lung total phospholipid, phosphatidycholine and disaturated phosphatidylcholine content increased by 60, 90 and 180%, respectively, between day 19 of gestation and the first postnatal day. Incorporation of choline into phosphatidylcholine and disaturated phosphatidylcholine increased 10-fold during this time. No changes in phosphatidylcholine enzyme activities were noted during gestation, but both choline phosphate cytidylyltransferase and phosphatidate phosphatase activity increased after birth. The possible contributions of carbohydrate derived from fetal lung glycogen to phospholipid synthesis are discussed.     

Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny

Exposure to synthetic glucocorticoids in utero markedly improves survival after preterm birth, but repeated exposures impair fetal and postnatal growth and are associated with evidence of insulin resistance in later life. The insulin-like growth factor (IGF) axis is an important regulator of growth and metabolism before and after birth. We have therefore investigated the effects of repeated maternal betamethasone injections on plasma IGF-I, IGF-II, and IGF-binding proteins (IGFBP) in fetal and postnatal progeny in the sheep. Pregnant sheep carrying male fetuses were injected with saline or betamethasone at 104, 111, and 118 days of gestation (dG, term approximately 150 dG). Plasma samples were collected postmortem from fetuses before (75, 84, 101 dG) or after one (109 dG), two (116 dG), or three (121-122, 132-133, 145-147 dG) doses of saline or betamethasone and from progeny at 42 and 84 days of age. Fetal weight was reduced after two or more maternal betamethasone injections, and this effect persisted to term. Repeated betamethasone exposures reduced plasma IGF-I and total IGFBP in fetuses at 133 dG and progeny at 84 days, and reduced plasma IGFBP-3 at 84 days. Fetal plasma IGF-II tended to increase transiently at 109 dG following the first betamethasone injection. Fetal, placental, and/or postnatal weights correlated positively with concomitant plasma IGF-I, IGF-II, and total IGFBP. We conclude that repeated exposure to synthetic glucocorticoids in utero programs the IGF axis before and after birth, which may contribute to the adverse effects of betamethasone exposure on growth and metabolism.     

Possible involvement of microcystins in the unexplained mass mortalities of Lesser Flamingo (<Emphasis Type="Italic">Phoeniconaias minor</Emphasis> Geoffroy) at Lake Manyara in Tanzania

We examined the effects of food and light on the swimming behavior of nauplii of the cyclopoid Apocyclops royi (Lindberg, 1940) (Copepoda: Cyclopoida) and the calanoid Pseudodiaptomus annandalei Sewell, 1919 (Copepoda: Calanoida). Several behavioral parameters such as swimming patterns, speed, and trajectories exhibited distinct ontogenetic differences between the two species. When algae Isochrysis galbana (Haptophyta: Isochrysidales) were offered as food to the nauplii of A. royi, they showed fast circle swimming behavior, while nauplii of P. annandalei never exhibited such behavior, neither with, nor without algae. The different behavioral patterns between the nauplii of both species suggest they both have different foraging strategies in detecting and capturing food.     

In utero cortisol and testosterone exposure and fear reactivity in infancy

Fetal programming is emerging as a major conceptual model for understanding developmental origins of health and disease, including behavioral outcomes. As part of a larger study of prenatal stress and child development, we examined the association between prenatal hormone exposure and fear reactivity, a temperament dimension that is a predictor of long-term behavioral adjustment. Amniotic fluid was collected from a sample of women undergoing clinically indicated amniocentesis for later analysis of cortisol and testosterone. Children with normal birth outcomes were recalled for follow-up assessment at 17 months, at which time we administered an observational assessment of temperament (lab-TAB; n = 108). Information on pregnancy and obstetric outcome was included as covariates. Results indicated that there was a significant association between prenatal testosterone and observed fear reactivity in boys (r(53) = 0.34, p = 0.01); no significant effect was found in girls (r(54) = − 0.07, ns); the effect remained when obstetric, psychosocial, and parental anxiety were controlled for. There was not a significant association between fetal cortisol exposure and fear reactivity. The prediction from in utero testosterone exposure to fear reactivity in boys extends prior research on prenatal testosterone and may represent an association with a general predisposition to greater arousal and reactivity.     

The Development of Upper Limb Movements: From Fetal to Post-Natal Life

Background

The aim of this longitudinal study was to investigate how the kinematic organization of upper limb movements changes from fetal to post-natal life. By means of off-line kinematical techniques we compared the kinematics of hand-to-mouth and hand-to-eye movements, in the same individuals, during prenatal life and early postnatal life, as well as the kinematics of hand-to-mouth and reaching-toward-object movements in the later age periods.

Methodology/Principal Findings

Movements recorded at the 14^th, 18^th and 22^nd week of gestation were compared with similar movements recorded in an ecological context at 1, 2, 3, 4, 8, and 12 months after birth. The results indicate a similar kinematic organization depending on movement type (i.e., eye, mouth) for the infants at one month and for the fetuses at 22 weeks of gestation. At two and three months such differential motor planning depending on target is lost and no statistical differences emerge. Hand to eye movements were no longer observed after the fourth month of life, therefore we compared kinematics for hand to mouth with hand to object movements. Results of these analyses revealed differences in the performance of hand to mouth and reaching to object movements in the length of the deceleration phase of the movement, depending on target.

Conclusion/Significance

Data are discussed in terms of how the passage from intrauterine to extra-uterine environments modifies motor planning. These results provide novel evidence of how different types of upper extremity movements, those directed towards one’s own face and those directed to external objects, develop.