Interactions with littermates are an important component of the early environment of altricial ma... more Interactions with littermates are an important component of the early environment of altricial mammals, frequently with major consequence for individual development, growth and survival. Early differences in starting mass within litters are often predictive of individual differences in behaviour and development, although to what extent such differences are independent of (epi)genetic factors is not always clear. In our study on domestic rabbits, Oryctolagus cuniculus, we created experimentally mixed litters consisting of either heavier or lighter pups obtained from different litters at birth and raised by foster mothers. We hypothesized that pups' body mass relative to their new littermates would determine the nature of their social interactions with consequences for their early growth, largely independent of their absolute or relative body mass in their litters of origin. As predicted, pups with a higher starting mass on postnatal day 1 compared to members of their new litter consistently had more neighbours in the litter huddle, thus reflecting their more central position. In turn, pups with more neighbours had relatively higher body temperatures, greater milk intake and a higher milk conversion ratio, resulting in relatively greater growth during the first critical postnatal week. Relative body mass in the litter of origin or absolute body mass had no notable effect, indicating that the observed developmental patterns were truly driven by pups' body mass relative to their current littermates rather than being a consequence of (epi)genetic effects potentially associated with their birth mass. In conclusion, our study underlines the importance of interactions among siblings in shaping individual differences in early growth and development largely independent of genetic factors.
Anatomical descriptions of the genitofemoral nerve (GFn) innervating the lower pelvic area are co... more Anatomical descriptions of the genitofemoral nerve (GFn) innervating the lower pelvic area are contradictory. Here we re-examine its origin and innervation by its various branches of principal target organs in the male rat. Using gross dissection, electrophysiological techniques and retrograde tracing of motoneurones with horseradish peroxidase, we confirm that the GFn originates from lumbar spinal nerves 1 and 2, and that at the level of the common iliac artery it divides into a lateral femoral and a medial genital branch. In contrast to previous studies, we report that the genital and not the femoral branch innervates the abdominal–inguinal skin, and not only the genital but also the femoral branch innervates the cremaster muscle (Cm) surrounding the testes. Motoneurones innervating the Cm proper are located in the ventral nucleus of L1 and L2, and those innervating the muscular transition region of the rostral Cm are located in the ventral nucleus in L1 and the ventrolateral nucleus in L2. The GFn may contribute to male reproductive performance by transmitting cutaneous information during copulation and, via contraction of the Cm to promote ejaculation, the protective displacement of the testes into the abdominal cavity during fighting and as a sperm-protecting thermoregulatory measure.
This article is part of a Special Issue &quot... more This article is part of a Special Issue "Parental Care". Jay Rosenblatt effectively promoted research on rabbit maternal behavior through his interaction with colleagues in Mexico. Here we review the activities of pregnant and lactating rabbits (Oryctolagus cuniculus), their neuro-hormonal regulation, and the synchronization of behavior between mother and kits. Changing concentrations of estradiol, progesterone, and prolactin throughout gestation regulate nest-building (digging, straw-carrying, fur-pulling) and prime the mother's brain to respond to the newborn. Nursing is the only mother-young contact throughout lactation. It happens once/day, inside the nest, with ca. 24h periodicity, and lasts around 3min. Periodicity and duration of nursing depend on a threshold of suckling as procedures reducing the amount of nipple stimulation interfere with the temporal aspects of nursing, though not with the doe's maternal motivation. Synchronization between mother and kits, critical for nursing, relies on: a) the production of pheromonal cues which guide the young to the mother's nipples for suckling; b) an endogenous circadian rhythm of anticipatory activity in the young, present since birth. Milk intake entrains the kits' locomotor behavior, corticosterone secretion, and the activity of several brain structures. Sibling interactions within the huddle, largely determined by body mass at birth, are important for: a) maintaining body temperature; b) ensuring normal neuromotor and social development. Suckling maintains nursing behavior past the period of abundant milk production but abrupt and efficient weaning occurs in concurrently pregnant-lactating does by unknown factors. female rabbits have evolved a reproductive strategy largely dissociating maternal care from maternal presence, whose multifactorial regulation warrants future investigations.
Journal of Clinical and Experimental Neuropsychology, Nov 8, 2017
In this study we evaluated a recently developed test, the Ball Search Field Task (BSFT) as a neur... more In this study we evaluated a recently developed test, the Ball Search Field Task (BSFT) as a neuropsychological tool for measuring cognitive and behavioral performance of individuals with disorders such as attention-deficit/hyperactivity disorder (ADHD), which are frequently accompanied by cognitive deficits and a lack of behavioral inhibition. The task provides a complementary method of assessment that attempts ecological validity by drawing on challenges faced in real-world situations. In this task, energetic costs and gross sensorimotor feedback are involved, as participants are required to search for targets in a large open area. We compared performance on the BSFT in a clinical sample of children and adolescents with a diagnosis of ADHD with their scores on two widely used neuropsychological tools, the Tower of London (ToLo) and the Behavior Rating Inventory of Executive Function (BRIEF). We found no correlations between scores on the BRIEF and those on either the BSFT or ToLo. However, we found moderate correlations between rule violations on ToLo and several BSFT variables, suggesting the capacity of these tests to detect common aspects of executive dysfunction. These findings, although modest, encourage further study of tasks like the BSFT, which may help assess cognitive dysfunction found in neurodevelopmental disorders such as ADHD in ecologically valid situations.
Individual differences in behavior (“personality”) are of considerable interest to behavioral bio... more Individual differences in behavior (“personality”) are of considerable interest to behavioral biologists. Important questions include how early in life such differences emerge, what factors influence their emergence, and whether they remain stable across development and into adult life. Given the demanding nature of longitudinal studies, there is a lack of information regarding these questions in mammals. Our aim in this study was to investigate the development of individual differences in chin‐marking behavior (chinning) in the domestic rabbit, a notable part of this species’ system of chemical communication, and to relate this to individual differences in growth and behavior among littermates during the early postnatal period. We tested repeatedly the frequency of chinning movements from weaning to sexual maturity in 63 chinchilla‐strain rabbits (35 females, 28 males) from 14 litters. Within litters, we found significant consistencies over time in this behavior, that is, in both sexes inter‐individual differences among litter siblings in the frequency of chinning movements remained stable across the postweaning period until sexual maturity. Unexpectedly, however, we found no significant associations with the morphological, physiological, or behavioral variables known to form a well‐correlated early developmental complex in this species. We tentatively conclude that in the rabbit, individual differences in the frequency of chinning have little relation to other previously studied aspects of individual developmental trajectories. The origin and functional significance of individual differences in chinning frequency, whether in reproductive or other social contexts is largely unknown and requires further investigation.
ABSTRACT The rabbit Sylvilagus cunicularius is endemic to Mexico and is one of the largest, most ... more ABSTRACT The rabbit Sylvilagus cunicularius is endemic to Mexico and is one of the largest, most widespread, but little studied of the country’s 10 rabbit species. As part of a project investigating its reproductive biology, we describe here for the first time the nursery burrow, vital for the survival of the altricial young. During the breeding seasons of 2008–2012, we collected data from 25 nursery burrows and 22 nests constructed by eight females (three wild caught and five captive bred) kept in enclosures within their natural habitat in the Malinche National Park in the central Mexican state of Tlaxcala. Although not a burrow-living species, several days before parturition, females dug a nursery burrow in which they constructed a nest. These burrows were short, shallow tunnels with a median length of 23 cm, typically located beneath grass tussocks or shrubs, and ending in a nest chamber a median 17 cm beneath the surface. Nests consisted of dry grass, fragments of woody plants, pine needles, and alfalfa hay and oat straw provided as supplementary food, fur pulled from the mother’s body, and her fecal pellets. Females nursed their young at the burrow entrance, and until the young were approximately 12 days old, they closed the entrance after each visit in such a way as to make it very difficult for humans to locate. Surprisingly, these nursery burrows were more similar to those of the European rabbit Oryctolagus cuniculus and the pygmy rabbit Brachylagus idahoensis than to other Sylvilagus species studied to date. As almost 50 % of burrows did not result in emergent young, present work is directed to determining what characterizes successful burrows.
Little information is available on the participation of the perineal striated muscles in female r... more Little information is available on the participation of the perineal striated muscles in female reproductive processes. Here, we describe the gross anatomy and innervation of two striated perineal muscles in the female rabbit, the bulbospongiosus (BSM) and ischiocavernosus (ISM), and analyze their reflex electromyographic (EMG) activity in response to stimulation of the perigenital skin and vaginal tract. Twenty-four mature chinchilla-breed
In mammals, body mass at birth is an important predictor of early postnatal growth and survival. ... more In mammals, body mass at birth is an important predictor of early postnatal growth and survival. Within litters, heavier young are more successful in competing for limited resources and show higher rates of growth and survival than their lighter sibs. In the present study, we investigated the contribution of two aspects of the intrauterine environment to within-litter differences in birth mass, growth and survival in the rabbit (Oryctolagus cuniculus): implantation site along the uterine horns and number of adjacent male fetuses. We used unilaterally ovariectomized mothers in order to infer relative sites of implantation from the birth order of pups from the single functional uterine horn. Pups from the extremities of the horn were significantly heavier at birth and weaning than their siblings from more central positions and had a higher probability of survival. The effect on body mass was still apparent 3 weeks after weaning in pups that had occupied positions at the ovarian end of the horn. The number of adjacent male fetuses did not affect individuals' growth or survival, and there were no differences between females and males. There were also no significant interactions between the different variables considered, indicating that the effects of implantation site on individuals' birth mass, growth and survival relative to littermates were independent of number of male neighbors, sex or litter size. Our study clearly demonstrates that in the rabbit, the site of implantation along the uterine horns is a major contributor to individual differences among littermates in early postnatal growth and survival.
Many aspects of an animal&amp... more Many aspects of an animal's early development might potentially contribute to long-term individual differences in physiology and behavior. Here we asked whether differences among littermates of the domestic rabbit in the position in the litter huddle that they occupy during the early nest period might contribute to the development of distinct behavioral and physiological phenotypes. In each of 12 litters we determined the pup occupying the most peripheral, the most central, and an intermediate position in the huddle during the first postnatal week. We then tested the responses of these same individuals as nestlings, juveniles and young adults when confronted by a range of age-appropriate environmental challenges. Two behavioral tests appeared particularly discriminatory in identifying differences associated with early position in the huddle; latency of pre-weaning pups to jump down from a shelf, and the response of young adults to the fearful screams of a conspecific. In both cases animals that had occupied the periphery of the huddle showed behavioral responses indicative of a more proactive behavioral style than their "intermediate" or "central" littermates. We conclude that while consistent long-term differences in behavioral style associated with early position in the litter huddle exist in rabbits, future work is needed to confirm the causal nature of this association, to identify underlying mechanisms, and to refine methods of behavioral and physiological testing across the life span.
Despite the importance of the rabbit (Oryctolagus cuniculus) in reproductive research, no compreh... more Despite the importance of the rabbit (Oryctolagus cuniculus) in reproductive research, no comprehensive account of the anatomical organization of the female reproductive tract is presently available. Based on gross dissection and on the electrical stimulation of striated muscles in 10 domestic female rabbits, it was the aim of this study to help fill this gap by describing the origin, insertion, and general action of muscles associated with the vaginal tract and with associated scent glands. Compared with the better-studied rat or cat, the long vaginal tract of the rabbit is characterized by a well-developed and complex musculature. The bulbospongiosus, ischiocavernosus, constrictor vestibuli, and constrictor vulvae muscles, poorly developed or absent in the female rat or cat, were particularly conspicuous. Scent glands, including the newly identified preputial glands, were also a distinctive feature. These structures may represent specializations underlying the rapid copulation, rapid parturition, and well-developed chemical communication characteristic of the reproductive efficiency of the rabbit.
Interactions with littermates are an important component of the early environment of altricial ma... more Interactions with littermates are an important component of the early environment of altricial mammals, frequently with major consequence for individual development, growth and survival. Early differences in starting mass within litters are often predictive of individual differences in behaviour and development, although to what extent such differences are independent of (epi)genetic factors is not always clear. In our study on domestic rabbits, Oryctolagus cuniculus, we created experimentally mixed litters consisting of either heavier or lighter pups obtained from different litters at birth and raised by foster mothers. We hypothesized that pups' body mass relative to their new littermates would determine the nature of their social interactions with consequences for their early growth, largely independent of their absolute or relative body mass in their litters of origin. As predicted, pups with a higher starting mass on postnatal day 1 compared to members of their new litter consistently had more neighbours in the litter huddle, thus reflecting their more central position. In turn, pups with more neighbours had relatively higher body temperatures, greater milk intake and a higher milk conversion ratio, resulting in relatively greater growth during the first critical postnatal week. Relative body mass in the litter of origin or absolute body mass had no notable effect, indicating that the observed developmental patterns were truly driven by pups' body mass relative to their current littermates rather than being a consequence of (epi)genetic effects potentially associated with their birth mass. In conclusion, our study underlines the importance of interactions among siblings in shaping individual differences in early growth and development largely independent of genetic factors.
Anatomical descriptions of the genitofemoral nerve (GFn) innervating the lower pelvic area are co... more Anatomical descriptions of the genitofemoral nerve (GFn) innervating the lower pelvic area are contradictory. Here we re-examine its origin and innervation by its various branches of principal target organs in the male rat. Using gross dissection, electrophysiological techniques and retrograde tracing of motoneurones with horseradish peroxidase, we confirm that the GFn originates from lumbar spinal nerves 1 and 2, and that at the level of the common iliac artery it divides into a lateral femoral and a medial genital branch. In contrast to previous studies, we report that the genital and not the femoral branch innervates the abdominal–inguinal skin, and not only the genital but also the femoral branch innervates the cremaster muscle (Cm) surrounding the testes. Motoneurones innervating the Cm proper are located in the ventral nucleus of L1 and L2, and those innervating the muscular transition region of the rostral Cm are located in the ventral nucleus in L1 and the ventrolateral nucleus in L2. The GFn may contribute to male reproductive performance by transmitting cutaneous information during copulation and, via contraction of the Cm to promote ejaculation, the protective displacement of the testes into the abdominal cavity during fighting and as a sperm-protecting thermoregulatory measure.
This article is part of a Special Issue &quot... more This article is part of a Special Issue "Parental Care". Jay Rosenblatt effectively promoted research on rabbit maternal behavior through his interaction with colleagues in Mexico. Here we review the activities of pregnant and lactating rabbits (Oryctolagus cuniculus), their neuro-hormonal regulation, and the synchronization of behavior between mother and kits. Changing concentrations of estradiol, progesterone, and prolactin throughout gestation regulate nest-building (digging, straw-carrying, fur-pulling) and prime the mother's brain to respond to the newborn. Nursing is the only mother-young contact throughout lactation. It happens once/day, inside the nest, with ca. 24h periodicity, and lasts around 3min. Periodicity and duration of nursing depend on a threshold of suckling as procedures reducing the amount of nipple stimulation interfere with the temporal aspects of nursing, though not with the doe's maternal motivation. Synchronization between mother and kits, critical for nursing, relies on: a) the production of pheromonal cues which guide the young to the mother's nipples for suckling; b) an endogenous circadian rhythm of anticipatory activity in the young, present since birth. Milk intake entrains the kits' locomotor behavior, corticosterone secretion, and the activity of several brain structures. Sibling interactions within the huddle, largely determined by body mass at birth, are important for: a) maintaining body temperature; b) ensuring normal neuromotor and social development. Suckling maintains nursing behavior past the period of abundant milk production but abrupt and efficient weaning occurs in concurrently pregnant-lactating does by unknown factors. female rabbits have evolved a reproductive strategy largely dissociating maternal care from maternal presence, whose multifactorial regulation warrants future investigations.
Journal of Clinical and Experimental Neuropsychology, Nov 8, 2017
In this study we evaluated a recently developed test, the Ball Search Field Task (BSFT) as a neur... more In this study we evaluated a recently developed test, the Ball Search Field Task (BSFT) as a neuropsychological tool for measuring cognitive and behavioral performance of individuals with disorders such as attention-deficit/hyperactivity disorder (ADHD), which are frequently accompanied by cognitive deficits and a lack of behavioral inhibition. The task provides a complementary method of assessment that attempts ecological validity by drawing on challenges faced in real-world situations. In this task, energetic costs and gross sensorimotor feedback are involved, as participants are required to search for targets in a large open area. We compared performance on the BSFT in a clinical sample of children and adolescents with a diagnosis of ADHD with their scores on two widely used neuropsychological tools, the Tower of London (ToLo) and the Behavior Rating Inventory of Executive Function (BRIEF). We found no correlations between scores on the BRIEF and those on either the BSFT or ToLo. However, we found moderate correlations between rule violations on ToLo and several BSFT variables, suggesting the capacity of these tests to detect common aspects of executive dysfunction. These findings, although modest, encourage further study of tasks like the BSFT, which may help assess cognitive dysfunction found in neurodevelopmental disorders such as ADHD in ecologically valid situations.
Individual differences in behavior (“personality”) are of considerable interest to behavioral bio... more Individual differences in behavior (“personality”) are of considerable interest to behavioral biologists. Important questions include how early in life such differences emerge, what factors influence their emergence, and whether they remain stable across development and into adult life. Given the demanding nature of longitudinal studies, there is a lack of information regarding these questions in mammals. Our aim in this study was to investigate the development of individual differences in chin‐marking behavior (chinning) in the domestic rabbit, a notable part of this species’ system of chemical communication, and to relate this to individual differences in growth and behavior among littermates during the early postnatal period. We tested repeatedly the frequency of chinning movements from weaning to sexual maturity in 63 chinchilla‐strain rabbits (35 females, 28 males) from 14 litters. Within litters, we found significant consistencies over time in this behavior, that is, in both sexes inter‐individual differences among litter siblings in the frequency of chinning movements remained stable across the postweaning period until sexual maturity. Unexpectedly, however, we found no significant associations with the morphological, physiological, or behavioral variables known to form a well‐correlated early developmental complex in this species. We tentatively conclude that in the rabbit, individual differences in the frequency of chinning have little relation to other previously studied aspects of individual developmental trajectories. The origin and functional significance of individual differences in chinning frequency, whether in reproductive or other social contexts is largely unknown and requires further investigation.
ABSTRACT The rabbit Sylvilagus cunicularius is endemic to Mexico and is one of the largest, most ... more ABSTRACT The rabbit Sylvilagus cunicularius is endemic to Mexico and is one of the largest, most widespread, but little studied of the country’s 10 rabbit species. As part of a project investigating its reproductive biology, we describe here for the first time the nursery burrow, vital for the survival of the altricial young. During the breeding seasons of 2008–2012, we collected data from 25 nursery burrows and 22 nests constructed by eight females (three wild caught and five captive bred) kept in enclosures within their natural habitat in the Malinche National Park in the central Mexican state of Tlaxcala. Although not a burrow-living species, several days before parturition, females dug a nursery burrow in which they constructed a nest. These burrows were short, shallow tunnels with a median length of 23 cm, typically located beneath grass tussocks or shrubs, and ending in a nest chamber a median 17 cm beneath the surface. Nests consisted of dry grass, fragments of woody plants, pine needles, and alfalfa hay and oat straw provided as supplementary food, fur pulled from the mother’s body, and her fecal pellets. Females nursed their young at the burrow entrance, and until the young were approximately 12 days old, they closed the entrance after each visit in such a way as to make it very difficult for humans to locate. Surprisingly, these nursery burrows were more similar to those of the European rabbit Oryctolagus cuniculus and the pygmy rabbit Brachylagus idahoensis than to other Sylvilagus species studied to date. As almost 50 % of burrows did not result in emergent young, present work is directed to determining what characterizes successful burrows.
Little information is available on the participation of the perineal striated muscles in female r... more Little information is available on the participation of the perineal striated muscles in female reproductive processes. Here, we describe the gross anatomy and innervation of two striated perineal muscles in the female rabbit, the bulbospongiosus (BSM) and ischiocavernosus (ISM), and analyze their reflex electromyographic (EMG) activity in response to stimulation of the perigenital skin and vaginal tract. Twenty-four mature chinchilla-breed
In mammals, body mass at birth is an important predictor of early postnatal growth and survival. ... more In mammals, body mass at birth is an important predictor of early postnatal growth and survival. Within litters, heavier young are more successful in competing for limited resources and show higher rates of growth and survival than their lighter sibs. In the present study, we investigated the contribution of two aspects of the intrauterine environment to within-litter differences in birth mass, growth and survival in the rabbit (Oryctolagus cuniculus): implantation site along the uterine horns and number of adjacent male fetuses. We used unilaterally ovariectomized mothers in order to infer relative sites of implantation from the birth order of pups from the single functional uterine horn. Pups from the extremities of the horn were significantly heavier at birth and weaning than their siblings from more central positions and had a higher probability of survival. The effect on body mass was still apparent 3 weeks after weaning in pups that had occupied positions at the ovarian end of the horn. The number of adjacent male fetuses did not affect individuals' growth or survival, and there were no differences between females and males. There were also no significant interactions between the different variables considered, indicating that the effects of implantation site on individuals' birth mass, growth and survival relative to littermates were independent of number of male neighbors, sex or litter size. Our study clearly demonstrates that in the rabbit, the site of implantation along the uterine horns is a major contributor to individual differences among littermates in early postnatal growth and survival.
Many aspects of an animal&amp... more Many aspects of an animal's early development might potentially contribute to long-term individual differences in physiology and behavior. Here we asked whether differences among littermates of the domestic rabbit in the position in the litter huddle that they occupy during the early nest period might contribute to the development of distinct behavioral and physiological phenotypes. In each of 12 litters we determined the pup occupying the most peripheral, the most central, and an intermediate position in the huddle during the first postnatal week. We then tested the responses of these same individuals as nestlings, juveniles and young adults when confronted by a range of age-appropriate environmental challenges. Two behavioral tests appeared particularly discriminatory in identifying differences associated with early position in the huddle; latency of pre-weaning pups to jump down from a shelf, and the response of young adults to the fearful screams of a conspecific. In both cases animals that had occupied the periphery of the huddle showed behavioral responses indicative of a more proactive behavioral style than their "intermediate" or "central" littermates. We conclude that while consistent long-term differences in behavioral style associated with early position in the litter huddle exist in rabbits, future work is needed to confirm the causal nature of this association, to identify underlying mechanisms, and to refine methods of behavioral and physiological testing across the life span.
Despite the importance of the rabbit (Oryctolagus cuniculus) in reproductive research, no compreh... more Despite the importance of the rabbit (Oryctolagus cuniculus) in reproductive research, no comprehensive account of the anatomical organization of the female reproductive tract is presently available. Based on gross dissection and on the electrical stimulation of striated muscles in 10 domestic female rabbits, it was the aim of this study to help fill this gap by describing the origin, insertion, and general action of muscles associated with the vaginal tract and with associated scent glands. Compared with the better-studied rat or cat, the long vaginal tract of the rabbit is characterized by a well-developed and complex musculature. The bulbospongiosus, ischiocavernosus, constrictor vestibuli, and constrictor vulvae muscles, poorly developed or absent in the female rat or cat, were particularly conspicuous. Scent glands, including the newly identified preputial glands, were also a distinctive feature. These structures may represent specializations underlying the rapid copulation, rapid parturition, and well-developed chemical communication characteristic of the reproductive efficiency of the rabbit.
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Papers by Robyn Hudson