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Reproduction of wild-caught and laboratory-born marmoset species used in biomedical research (Saguinus sp, Callithrix jacchus).

Reproductive performances of wild-caught and laboratory-born marmosets maintained in a paired-cage system were summarized. Wild-caught, white-lipped (WL) marmosets (Saguinus fuscicollis, S nigricollis) averaged 2.6 live births per pair per yr compared with 1.6 for cotton-topped (CT) marmosets (S oedipus); S fuscicollis illigeri pairs were the best producers. Of first and second generation laboratory-born animals, crossbred or hybrid WL pairs were the best producers; first generation pairs averaged 2.7 live births per pair per yr, comparable to the production of wild-caught WL pairs. In contrast, laboratory-born Sf illigeri pairs produced only 0.8 live births per pair per yr. No significant differences in reproductive performance were observed between first generation outbred vs inbred and between parent-reared vs hand-reared pairs. Based on limited data, the reproductive capabilities of wild-caught and laboratory-born Callithrix jacchus appeared superior to both WL and CT marmosets. Ten examples of marmoset models in biomedical research were discussed briefly.

Animals

The embryology of the common marmoset (Callithrix jacchus).

Earlier studies have noted the unusual placental anatomy of marmosets and the high frequency of biovular, synchorial twinning. The maintenance of a captive colony of Callithrix jacchus has enabled further studies to be made of embryonic development in this species. Thirty-six embryos from seventeen pregnancies were examined in detail and assigned to horizons on the basis of Streeter's classification of external form and internal structure. The specimens represented tha major part of the embryonic period and, with few exceptions, the structural development of the marmoset closely resembled that of the other primates that have been described. Marmoset embryos of a given horizon were consistently shorter than those of man. The timing of morphogenesis in C. jacchus was different from that observed in man and other primates. There was a considerable delay in early embryogenesis in the marmoset, although subsequent to stage XI, development proceeded at approximately the same rate as other primates. The available evidence suggested that this anomaly was not due to delayed implantation or embryonic diapause but to a generally slower rate of early development. The evolution of synchorial twinning is considered as a possible reason for this mode of development.

Abortion, Induced

Social context affects phee call production by nonreproductive common marmosets (Callithrix jacchus).

Common marmosets produce two variants of their long call (phee call) in different situations. Intergroup calls are produced in territorial situations, and intragroup separation calls are produced by marmosets isolated from group members. Marmoset groups frequently include postpubertal, nonreproductive members; their roles in the spontaneous production of territorial vocalizations is unclear. This study analyzed the production of home cage phee calls by nonreproductive, postpubertal marmosets while they were housed in their natal groups and after pairing with an opposite-sex conspecific. Additionally, the production of the separation phee call variant was assessed in both social conditions. The results indicated that the marmosets rarely produced home cage, or territorial, phee calls while they were natally housed. In contrast, both males and females produced the territorial phee call at a much higher rate as early as 4 days after pairing. Agematched females remaining in their natal groups throughout the study produced home cage phee calls infrequently. Most marmosets produced separation phee calls at a high rate after separation from either their natal group or a partner, suggesting that the makeup of a social group has little effect on an animal's motivation to reunite with conspecifics. These results suggest that the social environment has an important influence on the production of territorial phee calls.

Animals

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus).

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the periovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the periovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets.

Animals

Effects of separation and novelty on distress vocalizations and cortisol in the common marmoset (Callithrix jacchus).

In socially-bonding species, separation from familiar attachment figures is widely known to stimulate a physiological and behavioral stress response. This study investigated the hormonal and vocal responses of adult common marmosets to separation from familiar group members and to 24 hr of cohabitation with an unfamiliar opposite-sex conspecific. All subjects were removed from their home cages and placed into a novel environment for 20 min. In one group, marmosets were exposed to an unfamiliar, opposite-sex partner in the novel environment and remained paired with this partner for the 24 hr test period. In three other groups, marmosets experienced the novel environment alone and subsequently were returned to their original social- or single-housing condition, or kept separate from their social groups for a 24 h period. Blood samples were collected the day before, and at 30 min, 90 min, and at 24 h after separation. Cortisol responses were differentially affected by the length of separation and the presence of unfamiliar conspecifics. Brief separation followed by the return to the social group had minimal effect on plasma cortisol levels. All marmosets produced high levels of separation calls in the novel environment, but there was no apparent relationship between calling and cortisol levels. The lack of a temporal relationship between the production of distress vocalizations and serum cortisol has previously been noted in squirrel monkey and rhesus monkey infant separation studies; the behavioral and physiological responses to separation appear to be similarly dissociated in the marmoset. Further, the characteristics of a separation environment can differentially affect the hormonal response by adult marmosets without differentially affecting their behavioral response.

Animals

Fertilization-promoting peptide in reproductive tissues and semen of the male marmoset (Callithrix jacchus).

Fertilization-promoting peptide (FPP) is present in the prostate gland and semen of some mammals, and has been shown to enhance the fertilizing ability of both epididymal mouse and ejaculated human spermatozoa. The novel peptide may prove of importance for the treatment of some cases of male infertility, and a suitable animal model would be useful to test this hypothesis. To this end, we examined reproductive tissues and semen of the male marmoset for the presence of FPP. Peptides were extracted from seminal plasma, testes, prostate, and bulbourethral glands of intact and castrated male marmosets. The peptides were identified by ion-exchange chromatography followed by radioimmunoassay. The mean concentration of FPP immunoreactivity in semen from intact males was 58.7 nM (SE +/- 9.9 nM, n = 10), and anion-exchange chromatography revealed FPP as the only immunoreactive peptide present. Analysis of tissues revealed that FPP in semen was likely to be derived from the prostate gland, which contained this peptide as the major source of immunoreactivity (10.86 pmol/gland; SE +/- 4.39 pmol/gland, n = 4). Only low concentrations of FPP were detectable in the bulbourethral glands, and the peptide was undetectable in the testis. Surprisingly, FPP was readily detectable in the seminal plasma from one castrated marmoset and was present in the prostate gland from 3 castrates at levels which did not differ significantly from those in intact animals (5.47 pmol/gland, SE +/- 1.64 pmol/gland, n = 3). Plasma testosterone measurements indicated that residual circulatory androgens remained after castration, which may be consistent both with the maintenance of mating behavior and the presence of prostatic FPP. We conclude that FPP is present within the prostate gland and seminal plasma of the marmoset at concentrations consistent with a role in male fertility in this species.

Animals

Interhemispheric connections of visual cortex of owl monkeys (Aotus trivirgatus), marmosets (Callithrix jacchus), and galagos (Galago crassicaudatus).

Interhemispheric connections of visual cortex were studied in owl monkeys, marmosets, and galagos after multiple injections of horseradish peroxidase into one cerebral hemisphere. Areal patterns of connections were revealed in sections of cortex that was flattened and cut parallel to the surface. Results were related to the locations of known visual areas, especially in owl monkeys, in which more visual areas have been established. The connection patterns in owl monkeys and marmosets are very similar, suggesting that the organization of visual cortex differs little in these two New World simians. Galagos have a basically similar pattern, but the connections are more widespread. In all three primates, connections are not restricted to cortex representing the line of decussation of the retina, and even striate cortex has connections displaced from the border. These connections extend up to 2 mm into area 17 in owl monkeys, and they are most extensive in galagos, where they form foci that are coextensive with regions of high cytochrome oxidase activity. Connections are concentrated in the caudal half of area 18, but protrusions of connections cross of the width of the field. The middle temporal visual area (MT) has unevenly distributed connections throughout, with some increase in density along the border. The dorsomedial visual area (DM) of owl monkeys has connections restricted to the rostral border, and a similar region of sparse connections identifies the probable location of DM in marmosets and galagos. Caudal parts of the dorsolateral visual area (DL) of owl monkeys have dense interhemispheric connections. Other visual areas are characterized by unevenly distributed clumps of connections, suggesting that functions are not uniformly distributed, and that semiregular processing modules exist. The results indicate that most extrastriate visual neurons are subject to interhemispheric influences and support the conclusion that callosal connections are functionally heterogeneous.

Animals

Tyrosine hydroxylase-immunoreactive neurons in the nucleus basalis of the common marmoset (Callithrix jacchus).

In the course of characterizing the distribution of putative catecholaminergic neurons in the brain of the common marmoset, we encountered a population of such cells in the basal forebrain. Tyrosine hydroxylase-immunoreactive neurons are abundant within the nucleus basalis magnocellularis throughout its entire rostrocaudal extent, but not in other cholinergic basal forebrain nuclei. Most tyrosine hydroxylase-immunoreactive cells are large and multipolar. Double staining with antibodies to choline acetyltransferase or nerve growth factor receptor confirmed that these tyrosine hydroxylase-immunoreactive neurons are cholinergic, and compose at least 40% of the nucleus basalis cholinergic cells. The presence of a catecholamine-synthesizing enzyme in the neurons that provide the major cholinergic input to the neocortex may have important consequences for cortical function, and may be relevant to the vulnerability of the nucleus basalis in certain neurodegenerative disorders.

1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine

Projections of the lateral terminal accessory optic nucleus of the common marmoset (Callithrix jacchus).

The connections of the lateral terminal nucleus (LTN) of the accessory optic system (AOS) of the marmoset monkey were studied with anterograde 3H-amino acid light autoradiography and horseradish peroxidase retrograde labeling techniques. Results show a first and largest LTN projection to the pretectal and AOS nuclei including the ipsilateral nucleus of the optic tract, dorsal terminal nucleus, and interstitial nucleus of the superior fasciculus (posterior fibers); smaller contralateral projections are to the olivary pretectal nucleus, dorsal terminal nucleus, and LTN. A second, major bundle produces moderate-to-heavy labeling in all ipsilateral, accessory oculomotor nuclei (nucleus of posterior commissure, interstitial nucleus of Cajal, nucleus of Darkschewitsch) and nucleus of Bechterew; some of the fibers are distributed above the caudal oculomotor complex within the supraoculomotor periaqueductal gray. A third projection is ipsilateral to the pontine and mesencephalic reticular formations, nucleus reticularis tegmenti pontis and basilar pontine complex (dorsolateral nucleus only), dorsal parts of the medial terminal accessory optic nucleus, ventral tegmental area of Tsai, and rostral interstitial nucleus of the medial longitudinal fasciculus. Lastly, there are two long descending bundles: (1) one travels within the medial longitudinal fasciculus to terminate in the dorsal cap (ipsilateral >> contralateral) and medial accessory olive (ipsilateral only) of the inferior olivary complex. (2) The second soon splits, sending axons within the ipsilateral and contralateral brachium conjunctivum and is distributed to the superior and medial vestibular nuclei. The present findings are in general agreement with the documented connections of LTN with brainstem oculomotor centers in other species. In addition, there are unique connections in marmoset monkey that may have developed to serve the more complex oculomotor behavior of nonhuman primates.

Animals

Correlations among measures of playfulness and skillfulness in captive common marmosets (Callithrix jacchus jacchus).

Infant sensorimotor and social skills, playfulness, and nonplayful behaviors were measured in common marmosets from 6 to 22 weeks old. Different measures of skill showed a low concordance, implying that skill is a multiple rather than unitary attribute. Significant correlations were found between the amount of social play infants performed from 11 to 13 weeks of age and their performance at 14 weeks in (1) competitive food tests with their mothers, and in (2) their ability to negotiate an obstacle for a food reward. Significant correlations were also found between these skills and nonplayful behaviors, however. Comparable analyses at other ages revealed few significant correlations, suggesting that the association between social play and skills is restricted to the age when infants are rapidly becoming independent of their caregivers both for locomotion and food. Age-specific correlations occurred between changes in levels of skills and both playful and nonplay behaviors. Our results are consistent with the hypothesis that social play promotes the development of skills, but alternative explanations are possible.

Animals

Effects on the behavior of infant common marmosets (Callithrix jacchus) of separation from caregivers and of drug-induced reduction in caregiver responsiveness.

The effects of separating 4-week-old twin marmosets for 8 days from their families are compared with the effects of leaving 4-week-old infants with their families, but reducing the responsiveness of their caregivers for 8 days by administration of the tranquilizer fluphenazine decanoate. Both treatments reduce infant mobility, abolish play, and increase the time that infants spend with each other. During the period after the termination of the treatment, both treatment groups continue to play and move less than controls, and try to climb onto the mothers more frequently. These results are consistent with the hypothesis that the principal factor precipitating disturbed behaviors in infant monkeys subjected to long-term separation is disruption of the infant-caregiver relationship rather than the separation itself. Some post-treatment differences occur between separated and tranquilized groups. Notably, reunion after separation appears to involve a marked readjustment of the behavior of all family members to the return of the infants, whereas withdrawal of the tranquilizer does not.

Animals

The diagnostic usefulness of isocitrate dehydrogenase (ICDH) in the marmoset (Callithrix jacchus).

Marmosets were given either a hepatotoxin, carbon tetrachloride, orally or an i.m. injection of a mytoxin, chlorpromazine. Although muscle damage alone caused small increases in the plasma levels of lactate dehydrogenase, alanine aminotransferase, aspartate aminotransferase and isocitrate dehydrogenase (ICDH), only the isoenzyme analysis of ICDH can differentiate definitely between liver and muscle damage. Only very severe muscle damage can increase the plasma concentration of this enzyme but, in this case, the elevation of plasma creatinine kinase levels helps differentiation. It is recommended that the elevation of ICDH is the most specific indicator of hepatic damage in the marmoset.

Alanine Transaminase

The neuropathology of trimethyltin in the marmoset (Callithrix jacchus) hippocampal formation.

The effects of single and repeated doses of trimethyltin (TMT) treatment on the central nervous system (CNS) of the marmoset were investigated. For the acute-dose experiment adult animals were administered 3 mg/kg of TMT chloride (ip) and were then observed for changes in behavior. Within 24 hr postinjection all animals developed tremors, ataxia, and unresponsiveness. Half of the animals had severe clinical deterioration and died at 2 to 3 days following treatment. Surviving marmosets were sacrificed and the brain was subsequently perfusion-fixed for light microscopic examination. Neuronal degeneration was observed in many cells of the Ammon's horn and fascia dentata of the hippocampus. For the chronic-dose experiment, adult marmosets received (ip) weekly doses of 0.75 mg/kg of TMT chloride for 24 weeks. No evident clinical signs or behavioral changes were observed in any of the treated animals. Histological examination revealed neuropathological changes comparatively similar but less severe than those observed in the acute-treated animals. The differences in toxicity effects between acute and chronic TMT administration are compared and discussed.

Animals

Effects of testosterone propionate upon the sexual and aggressive behavior of adult male marmosets (Callithrix jacchus) castrated as neonates.

In New World monkeys of the family Callitrichidae (marmosets and tamarins), females frequently give birth to dizygotic twins. Twins share a placental circulation throughout fetal development and are hemopoietic chimeras. Despite this, there is no masculinization (freemartinism) in females which develop next to a male co-twin. It has been suggested that the organizing effects of testicular androgen upon sexual differentiation of the brain occur mainly during early postnatal development in male callitrichids, rather than in utero. However, this report demonstrates activation of masculine copulatory behavior by testosterone propionate (TP) administered to adult male marmosets (N = 8) which were castrated in infancy (between Days 1-7). Effects of neonatal castration upon aggressive behavior during pair tests with females (high frequencies of aggression) and intact adult males (low frequencies of aggression) were also reversed by TP treatment in adulthood. While early postnatal androgen secretion plays an important role in behavioral development in marmosets, it appears that a substantial degree of neural sexual differentiation occurs in utero in males of this callitrichid species.

Aggression

Quantitative receptor autoradiography of eight different transmitter-binding sites in the hippocampus of the common marmoset, Callithrix jacchus.

The regional and laminar distributions of eight different transmitter-binding sites were measured in the marmoset hippocampus by means of quantitative in vitro receptor autoradiography. Receptors for 5-HT1, L-glutamate, N-methyl-D-aspartate (NMDA) and GABAA were similarly distributed. The highest concentrations of these receptors were found in the pyramidal layer of CA1 and the molecular layer of the dentate gyrus. The 5-HT2 receptors showed the highest concentrations in the oriens layer of CA2. The highest concentrations of muscarinic M1 receptors were seen in the pyramidal layer of CA1. Muscarinic M2 receptors were most densely concentrated in the pyramidal layers of CA1, CA2 and CA3. The noradrenergic alpha 1 receptors were most densely packed in the radiatum-lacunosum-molecular layer of CA2 and the molecular layer of the dentate gyrus. Statistically significant co-distributions of serotoninergic, glutamatergic and GABAergic receptors point to possible interactions between these receptor systems in the same hippocampal regions and layers. Comparisons of marmoset distribution patterns for GABAA, NMDA, L-glutamate and 5-HT1 receptors with those in human hippocampi and those of other primates showed similarities between them. Clear differences in the patterns of alpha 1, M1, M2 and 5-HT2 receptors could be seen between marmoset and human hippocampi, indicating a high degree of species specificity in a presumably "conservative" brain region. More similarities, however, could be found between marmoset and human hippocampi than between those of rat and human brains, especially in relation to 5-HT1 and GABAA receptors and L-glutamate-binding sites.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals

Intercellular communication between cultured granulosa cells of the marmoset (Callithrix jacchus).

The influence of follicle-stimulating hormone, forskolin, insulin-like growth factor type I, epidermal growth factor, and 12-tetradecanoyl-phorbol-13-acetate on marmoset granulosa cell communication via gap junctions was investigated by morphological means and microinjection of carboxyfluorescein. Gap junctions between neighbouring granulosa cells were present in all groups. The number, but not length, of gap junctions between marmoset granulosa cells increased when the cells had been treated with follicle-stimulating hormone, insulin-like growth factor type I, and follicle-stimulating hormone plus insulin-like growth factor type I. No effect on gap junctions was seen, after exposure of the cells to the other three substances. Carboxyfluorescein and counting of the surrounding labelled cells showed that supplementation with follicle-stimulating hormone, forskolin, insulin-like growth factor type I and epidermal growth factor from the beginning of cultivation led to an increase in stained cells after 48 h. When treatment was started in 48 h cultures the substances reached their maximal activity within 30 min (forskolin and epidermal growth factor) or 3 h (follicle-stimulating hormone and insulin-like growth factor type I). Spreading of the fluorescent dye was inhibited when the medium was supplemented with 12-tetradecanoyl-phorbol-13-acetate. This effect was maximal after 30 min. Additive effects regarding the coupling of the cells were seen by combining of epidermal growth factor with follicle-stimulating hormone, but not with insulin-like growth factor type I or forskolin plus follicle-stimulating hormone.

Animals

A conveyor belt task for assessing visuo-motor coordination in the marmoset (Callithrix jacchus): effects of diazepam, chlorpromazine, pentobarbital and d-amphetamine.

A conveyor belt task for assessing visuo-motor coordination in the marmoset is described. Animals are motivated by apple, a preferred food, under a state of minimal food deprivation. The apparatus used was designed to test animals within their home cages and not restrained in any way, thus avoiding possible confounding factors associated with restraint stress. Stable baseline levels of performance were reached by all animals in a median of 24 sessions. Performance was shown to be differentially sensitive to the effects of four psychoactive drugs. Moderate doses of diazepam, chlorpromazine and pentobarbital disrupted visuo-motor coordination in a dose-related manner. The possibility that disruption of performance observed at higher doses may have resulted from non-specific actions of these drugs such as decreases in feeding motivation were not supported by results from ancillary experiments. Changes in performance characteristic of high dose effects were similar in nature to changes observed when the degree of task difficulty was increased. Doses of d-amphetamine up to and including those reported to produce signs of stereotypy failed to influence performance. The potential of the conveyor belt task for measuring visuo-motor coordination in both primate and rodent species is discussed.

Animals