A cafeína como agente modulador do ciclo atividade-repouso e memória em saguis (Callithrix jacchus)

Caffeine is the most consumed psychostimulant, with effects on attention, memory, and arousal. But when this substance is ingested near to bedtime there is a decrease on sleep, interfering on mnemonic processes. So, our ain was to investigate how the caffeine ingested near to sleep onset acts on sleep and memory in marmosets. We used 16 adult marmosets, single housed, in a 12:12h light-dark cycle. For registering locomotor activity were used two kinds of sensors. The gyroscope sensor registers activity each 30 sec and detects motion with good accuracy. Because of this we used this sensor for detecting nocturnal activity. The second sensor was based on infrared and accumulates activity each 5 min and it’s not able to detect nocturnal activity, just diurnal activity. We also used camera for registering Rest phase of one marmoset. For the cognitive task, the animals needed to learn a rewarded context (CR) when compared to a non-rewarded context CNR). This experiment comprises 5 phases: 1) Two days of habituation to apparatus; 2)Training for 8 days; 3) oral administration of caffeine (10 mg/kg) or placebo administration ±1h before sleep onset, for 8 days, with marmosets receiving placebo or caffeine; 4) retraining to apparatus and after that, placebo administration (placebo group-GP), or caffeine administration (with continuous group-GC and acute groupGA); 5) Test, for evaluating learning to CR. The sessions were filmed and each one had 8 min of duration. At 7 am started the habituation, training and test sessions, and at 3:15 pm started retraining. The results for gyroscope sensor showed that there was coincidence of 68,57% with nocturnal register of the cameras. Then, the gyroscope sensors detected nocturnal activity for all experimental groups Moreover, when compared sensor gyroscope with sensor based on infrared, was observed that both sensor presented similarity on patterns of activity curve. When we observed the effects of caffeine on Activity-Rest Cycle in GP, GA and GC, is possible to see that that gyroscope sensors and based on infrared presented only intra group differences. As behavioral results, the marmosets learned to discriminate CR when compared to CNR. Moreover, GP presented deficits on memory recall during the test, and GA increased the memory recall, when both were compared to GP. We concluded that the marmosets were able to learning the cognitive task and that the caffeine ingested near to sleep onset acts modulating memory in these animals. Moreover the gyroscope sensor can be used as alternative tool for investigating nocturnal activity. Then, the utilization of this non-invasive device allows marmosets exhibit their behavior within the laboratory conditions as natural as possible.

Caracterização citoarquitetônica e por imunoistoquímica para tirosina-hidroxilase da substância negra, área tegmentar ventral e zona retrorubral do Sagui (Callithrix jacchus)

It is known that the catecholamine group is constituted by dopamine, noradrenaline and adrenaline, in which the synthesis is regulated by an enzyme named tyrosine hydroxylase. Thus, 3-hydroxytyramine/dopamine (DA) is a precursor of the noradrenaline and adrenaline synthesis and acts as a neurotransmitter in the central nervous system. The three main nuclei, named the retrorubral field (A8 group), the substantia nigra pars compacta (A9 group) and the ventral tegmental area (A10 group), are arranged in the die-mesencephalic portion and are involved in three complexes circuitries - the mesostriatal, mesolimbic and mesocortical pathways. These pathways are related to behavioral manifestations, motricity, learning, reward and pathologies such as Parkinson’s Disease and Schizophrenia. Thus, the aim of this study was to perform de morphological analysis of the A8, A9 and A10 nuclei of the common marmoset (Callithrix jacchus). The marmoset is a neotropical primate, whose morphological and functional characteristics supports the suitability of use of this animal in biomedical research. Coronal sections of the marmoset brain were submitted to cytoarchitectonic characterization and TH-immunohistochemistry. Based on the morphology of the neurons, it was possible to subdivide the A10 group in seven regions: interfascicular nucleus, raphe rostral linear nucleus and raphe caudal linear nucleus, in the middle line; paranigral and parainterfascicular nucleus, in the middle zone; rostral portion of the ventral tegmental area nucleus and parabrachial pigmented nucleus, located in the dorsolateral portion of the mesencephalic tegmentum. A9 group was divided into four regions: substantia nigra compacta dorsal and ventral tiers; substantia nigra compacta lateral and medial clusters. No subdivisions were founded into A8 group. These results revealed that A8, A9 and A10 are phylogenetically conserved between species, but it’s necessary to expand the studies about this compartmentalization, investigating its occurrence in other primate species or investigating its functional relevance.

Mapeamento das projeções retinianas para o sistema óptico acessório, colículo superior e complexo pré-tectal do sagui (callithrix jacchus)

The accessory optical system, the pretectal complex, and superior colliculus are important control centers in a variety of eye movement, being extremely necessary for image formation, consequently to visual perception. The accessory optical system is constituted by the nuclei: dorsal terminal nucleus, lateral terminal nucleus, medial terminal nucleus and interstitial nucleus of the posterior superior fasciculus. From a functional point of view they contribute to the image stabilization, participating in the visuomotor activity where all system cells respond to slow eye movements and visual stimuli, which is important for the proper functioning of other visual systems. The pretectal complex comprises a group of nuclei situated in mesodiencephalic transition, they are: anterior pretectal nucleus, posterior pretectal nucleus, medial pretectal nucleus, olivary pretectal nucleus and the nucleus of the optic tract, all retinal projection recipients and functionally are related to the route of the pupillary light reflex and the optokinetic nystagmus. The superior colliculus is an important subcortical visual station formed by layers and has an important functional role in the control of eye movements and head in response to multisensory stimuli. Our aim was to make a mapping of retinal projections that focus on accessory optical system, the nuclei of pretectal complex and the superior colliculus, searching mainly for pretectal complex, better delineation of these structures through the anterograde tracing with the B subunit of cholera toxin (CTb) followed by immunohistochemistry and characterized (measured diameter) synaptic buttons present on the fibers / terminals of the nucleus complex pré-tectal. In our results accessory optical system, including a region which appears to be medial terminal nucleus and superior colliculus, were strongly marked by fibers / terminals immunoreactive CTb as well as pretectal complex in the nucleus: optic tract, olivary pretectal nucleus, anterior pretectal nucleus and posterior pretectal nucleus. According to the characterization of the buttons it was possible to make a better definition of these nucleus.

Mecanismos de sincronia social no ritmo circadiano de atividade durante a coabitação em casais de saguis (Callithrix jacchus)

In marmosets, it was observed that the synchrony among circadian activity profiles of animals that cohabite in family groups is stronger than those of the same sex and age of different families. Inside the group, it is stronger between the younger ones than between them and their parents. However, the mechanisms involved in the social synchrony are unknown. With the aim to investigate the synchronization mechanisms involved in the synchrony between the circadian activity profiles during cohabitation in pairs of marmosets, the motor activity was continuously registered by the use of actmeters on three dyads. The pairs were maintained in two different conditions of illumination: light-dark cycle LD 12:12 (LD cohabitation I – 21 days), and thereafter in LL (~350 lux). Under LL, the pairs were submitted to four experimental situations: 1. Cohabitation (LLJ I – 24 days), 2. Removal of one member of the pair to another room with similar conditions (LLS I – 20 days), 3. Reintroduction of the separated member in the cage of the first situation (LLJ II – 30 days) and 4. Removal of a member from each pair to another experimental room (LLS II – 7 days), to evaluate the mechanisms of synchronization. Ultimately, the members of each pair were reintroduced in the cage and were kept in LD cycle 12:12 (LDJ II – 11 days). The rhythms of pairs free-ran in LL, with identical periods between the members of each pair during the two stages of cohabitation. In the stages in which the animals were separated, only the rhythms of two females free-ran in the first stage and of three animals in the second one. In those conditions, the rhythms of animals of each pair showed different endogenous periods. Besides, during cohabitation in LD and LL, the members of each pair showed a stable phase relationship in the beginning of the active phase, while in the stages in which the animals were separated it was noticed a breaking in the stability in the phase relationships between the circadian activity profiles, with an increase in the difference in the phase angles between them. During cohabitation, at the transition between LD and LL, all animals showed free-running rhythms anticipating progressively the beginning and the end of the active phase in a phase similar to the previous condition, showing signs of entrainment to the previous LD. While in the posterior stages this was observed in only three animals between: LLT I and LLS I, and LLT II and LLS II, evidencing signs of entrainment to social cues between the members of each pair. On the other hand, one animal delayed progressively between LLT I and LLS I, three animals delayed between LLS I and LLT II, and three animals between LLT II and LLS II, perhaps by entrainment to the animals maintained outdoors in the colony. Similar process was observed in four animals between LLS II and LDT II, indicating entrainment to LD. In the transition between LLS I and LLT II, signs of masking was observed in the rhythm of a female in response to the male and in another pair in the rhythm of the male in regard to that of the female. The general and maximum correlations in the circadian activity profiles were stronger during cohabitation in LD and LL than in the absence of social contact in LL, evidencing the social effect. The cohabiting pairs had higher values of the maximum correlation in LD and LL than when the profiles were correlated to animals of different cages, with same or different sexes. Similar results were observed in the general correlation. Therefore, it is suggested that cohabitation induces a strong synchrony between circadian activity profiles in marmosets, which involves entrainment and masking. Nevertheless, additional studies are necessary to evaluate the effect of social cues on the synchronization of the circadian rhythm in pairs of marmosets in the absence of external social cues in order to confirm this hypothesis.

Modulaçao do estresse social sobre parâmetros fisiológicos, comportamentais, cognitivos e plasticidade neuronal em saguis (Callithrix jacchus) juvenis: um modelo psiquiátrico e cognitivo

Nos períodos críticos de plasticidade neural ocorre uma maior permissividade do sistema nervoso ao ambiente, por isto, a ação do estresse sobre o individuo e suas repercussões sobre áreas responsáveis pelo controle dos sistemas de resposta ao estresse e por funções cognitivas complexas vem recebendo bastante atenção. A utilização de modelos experimentais translacionais tem sido imprescindível na elucidação destes mecanismos e das patologias associadas. Diante disto, este trabalho investigou os efeitos do estresse social sobre parâmetros fisiológicos, comportamentais, cognitivos e sobre a neurogênese no córtex pré-frontal (CPF) durante um período crítico de plasticidade cerebral, a fase juvenil, em machos de Callithrix jacchus. Durante cinco meses, 5 animais foram acompanhados em suas famílias (GF) e 5 animais foram isolados socialmente por 4 meses (GI), após um mês em observação em ambiente familiar (fase basal- FB). Ao final do 5º mês foram aplicados 2 testes de memória de trabalho (MT) nos animais GF e GI. Em seguida, 3 animais de cada grupo foram sacrificados para análise do fator de neurogênese BDNF ( Brain Derived Neurotrophic Factor) por imunofluorescência no CPF (sub-regiões orbitofrontal e lateral). Os animais do GF não variaram significativamente o cortisol ao longo do estudo, enquanto o GI elevou o cortisol e comportamentos indicadores de ansiedade (CA) na primeira semana do isolamento. Em seguida, o GI apresentou uma redução no cortisol, nos CA, no peso corporal e um aumento de comportamentos estereotipados e da anedonia, alterações tipicamente depressivas em primatas não-humanos. Ao final, o GI apresentaram níveis de cortisol menores que em FB. Ambos os grupos apresentaram dificuldades em realizar e aprender as tarefas cognitivas e a presença de BDNF no córtex pré-frontal foi independente do grupo (GF ou GI), porém correlacionou-se com os níveis de cortisol presentes na ultima semana do estudo, e os animais com presença de BDNF no CPF lateral e orbitofrontal apresentaram maiores níveis de cortisol. Estes resultados contribuem no processo de validação do sagui como um bom modelo psiquiátrico translacional e aponta para possibilidade de estudos sobre transtornos depressivos na juventude e suas repercussões posteriores. Além disto, os resultados observados para as tarefas cognitivas levou-nos a fazer uma releitura dos protocolos utilizados em estudos de memoria de trabalho com animais adultos desta espécie, com a finalidade de aprimora-los facilitando a aprendizagem em animais juvenis, naives e em situações de estresse. Ademais, evidenciou-se pela primeira vez a relação do estresse, cortisol e níveis de BDNF, em animais juvenis desta espécie, com a fim de contribuir com sua utilização como modelo animal neurocognitivo.

Caracterização do ritmo circadiano de atividade e repouso em saguis idosos (Callithrix Jacchus)

Advanced age may become a limiting factor for the maintenance of rhythms in organisms, reducing the capacity of generation and synchronization of biological rhythms. In this study, the influence of aging on the expression of endogenous periodicity and synchronization (photic and social) of the circadian activity rhythm (CAR) was evaluated in a diurnal primate, the marmoset (Callithrix jacchus). This study had two approaches: one with longitudinal design, performed with a male marmoset in two different phases: adult (three years) and older (9 y.o.) (study 1) and the second, a transversal approach, with 6 old (♂: 9.7 ± 2.0 y.o.) and 11 adults animals (♂: 4.2 ± 0.8 y.o.) (study 2). The evaluation of the photic synchronization involved two conditions in LD (natural and artificial illuminations). In study 1, the animal was subjected to the following stages: LD (12:12 ~ 350: ~ 2 lx), LL (~ 350 lx) and LD resynchronization. In the second study, the animals were initially evaluated in natural LD, and then the same sequence stages of study 1. During the LL stage in study 2, the vocalizations of conspecifics kept in natural LD on the outside of the colony were considered temporal cue to the social synchronization. The record of the activity was performed automatically at intervals of five minutes through infrared sensor and actimeters, in studies 1 and 2, respectively. In general, the aged showed a more fragmented activity pattern (> IV < H and > PSD, ANOVA, p < 0.05), lower levels of activity (ANOVA, p < 0.05) and shorter duration of active phase (ANOVA, p < 0.05) in LD conditions, when compared to adults. In natural LD, the aged presented phase delay pronounced for onset and offset of active phase (ANOVA, p < 0.05), while the adults had the active phase more adjusted to light phase. Under artificial LD, there was phase advance and greater adjustment of onset and offset of activity in relation to the LD in the aged (ANOVA, p < 0.05). In LL, there was a positive correlation between age and the endogenous period () in the first 20 days (Spearman correlation, p < 0.05), with prolonged  held in two aged animals. In this condition, most adults showed free-running period of the circadian activity rhythm with  < 24 h for the first 30 days and later on relative coordination mediated by auditory cues. In study 2, the cross-correlation analysis between the activity profiles of the animals in LL with control animals kept under natural LD, found that there was less social synchronization in the aged. With the resubmission to the LD, the resynchronization rate was slower in the aged (t-test; p < 0.05) and in just one aged animal there was a loss of resynchronization capability. According to the data set, it is suggested that the aging in marmosets may be related to: 1) lower amplitude and greater fragmentation of the activity, accompanied to phase delay with extension of period, caused by changes in a photic input, in the generation and behavioral expression of the CAR; 2) lower capacity of the circadian activity rhythm to photic synchronization, that can become more robust in artificial lighting conditions, possibly due to the higher light intensities at the beginning of the active phase due to the abrupt transitions between the light and dark phases; and 3) smaller capacity of non-photic synchronization for auditory cues from conspecifics, possibly due to reducing sensory inputs and responsiveness of the circadian oscillators to auditory cues, what can make the aged marmoset most vulnerable, as these social cues may act as an important supporting factor for the photic synchronization.

Caracterização do ritmo circadiano de atividade e repouso em saguis idosos (Callithrix Jacchus)

Advanced age may become a limiting factor for the maintenance of rhythms in organisms, reducing the capacity of generation and synchronization of biological rhythms. In this study, the influence of aging on the expression of endogenous periodicity and synchronization (photic and social) of the circadian activity rhythm (CAR) was evaluated in a diurnal primate, the marmoset (Callithrix jacchus). This study had two approaches: one with longitudinal design, performed with a male marmoset in two different phases: adult (three years) and older (9 y.o.) (study 1) and the second, a transversal approach, with 6 old (♂: 9.7 ± 2.0 y.o.) and 11 adults animals (♂: 4.2 ± 0.8 y.o.) (study 2). The evaluation of the photic synchronization involved two conditions in LD (natural and artificial illuminations). In study 1, the animal was subjected to the following stages: LD (12:12 ~ 350: ~ 2 lx), LL (~ 350 lx) and LD resynchronization. In the second study, the animals were initially evaluated in natural LD, and then the same sequence stages of study 1. During the LL stage in study 2, the vocalizations of conspecifics kept in natural LD on the outside of the colony were considered temporal cue to the social synchronization. The record of the activity was performed automatically at intervals of five minutes through infrared sensor and actimeters, in studies 1 and 2, respectively. In general, the aged showed a more fragmented activity pattern (> IV < H and > PSD, ANOVA, p < 0.05), lower levels of activity (ANOVA, p < 0.05) and shorter duration of active phase (ANOVA, p < 0.05) in LD conditions, when compared to adults. In natural LD, the aged presented phase delay pronounced for onset and offset of active phase (ANOVA, p < 0.05), while the adults had the active phase more adjusted to light phase. Under artificial LD, there was phase advance and greater adjustment of onset and offset of activity in relation to the LD in the aged (ANOVA, p < 0.05). In LL, there was a positive correlation between age and the endogenous period () in the first 20 days (Spearman correlation, p < 0.05), with prolonged  held in two aged animals. In this condition, most adults showed free-running period of the circadian activity rhythm with  < 24 h for the first 30 days and later on relative coordination mediated by auditory cues. In study 2, the cross-correlation analysis between the activity profiles of the animals in LL with control animals kept under natural LD, found that there was less social synchronization in the aged. With the resubmission to the LD, the resynchronization rate was slower in the aged (t-test; p < 0.05) and in just one aged animal there was a loss of resynchronization capability. According to the data set, it is suggested that the aging in marmosets may be related to: 1) lower amplitude and greater fragmentation of the activity, accompanied to phase delay with extension of period, caused by changes in a photic input, in the generation and behavioral expression of the CAR; 2) lower capacity of the circadian activity rhythm to photic synchronization, that can become more robust in artificial lighting conditions, possibly due to the higher light intensities at the beginning of the active phase due to the abrupt transitions between the light and dark phases; and 3) smaller capacity of non-photic synchronization for auditory cues from conspecifics, possibly due to reducing sensory inputs and responsiveness of the circadian oscillators to auditory cues, what can make the aged marmoset most vulnerable, as these social cues may act as an important supporting factor for the photic synchronization.

New developmental stages for common marmosets (Callithrix jacchus) using mass and age variables obtained by K-means algorithm and self-organizing maps (SOM)

LEÃO, Adriano de Castro; DÓRIA NETO, Adrião Duarte; SOUSA, Maria Bernardete Cordeiro de. New developmental stages for common marmosets (Callithrix jacchus) using mass and age variables obtained by K-means algorithm and self-organizing maps (SOM). Computers in Biology and Medicine, v. 39, p. 853-859, 2009

Fecal androgen levels in common marmoset (Callithrix jacchus) males living in captive family groups

In captive common marmoset groups, the reproductive inhibition observed in subordinate female seems to be a result of olfactory, visual and behavioral cues from the dominant female. However, few studies have examined the relationship among adult males living in the same social group. These studies have shown that reproductive failure among peer males seems to be based on hormonal and behavioral mechanisms. New insights on sexual strategies in primates have been shown using fecal steroids, but so far no information is available for common marmoset males. In the present study, we evaluated the influence of light-dark cycle, age and reproductive condition on the profile of fecal androgens in males living in the same family group. Feces were collected from six fathers and six sons for androgen determination during the light phase of the 24-h cycle for eight days randomly distributed over a 4-week period. Androgen levels were determined by enzyme immunoassay technique. Adult sons showed higher androgen levels (166.97 ± 22.95 ng/g) than fathers (80.69 ± 44.38 ng/g) and juveniles (49.06 ± 23.15 ng/g; P < 0.05). No diurnal variation (P > 0.05) in fecal androgen profile was observed in adults or juveniles. No indication of androgen-mediated social competition between fathers and adult sons was demonstrable. These results provide basic information on fecal androgen profile useful to investigate the socioendocrinology of free-ranging common marmoset males and verify that, in contrast to daughters, the reproductive suppression of sons is not based on physiological inhibition of their gonads

Início da função gonadal no sagui comum (Callithrix jacchus): diferenças entre gêneros

Os primatas não humanos, como Callithrix jacchus vêm sendo utilizados com maior frequência em pesquisa biomédica e, recentemente, nosso laboratório propôs uma nova classificação para monitorar com mais detalhes as modificações comportamentais e hormonais relacionadas ao desenvolvimento. O presente trabalho monitorou os níveis de hormônios gonadais de 4 machos e 6 fêmeas de C. jacchus durante as fases juvenil I e II e subadulta (dos 5 aos 15 meses). Os resultados apontaram que os níveis de progesterona nas fêmeas e andrógenas nos machos foram estatisticamente mais elevados nos estágios juvenil II e subadulto, respectivamente, em relação ao estágio juvenil I. Estes achados indicam que, de acordo com a nova classificação, foi possível observar que o funcionamento gonadal se instala mais cedo nas fêmeas

Histopathology findings in common marmosets (Callithrix jacchus Linnaeus, 1758) with chronic weight loss associated with bile tract obstruction by infestation with Platynosomum (Loos, 1907)

Chronic weight loss in marmosets is often associated with wasting marmoset syndrome (WMS), an important disease that occurs in callitrichid colonies around the world. Even though its etiology is very difficult to determine, particular variables, such as weight loss, diarrhea and alopecia, associated or not with infestation in the pancreatic ducts with Trichospirura leptossoma (Nematoda: Thelazioidea), seem to be linked with the syndrome. This study investigated the histopathology of the lungs, duodenum, liver, gallbladder, extrahepatic bile ducts and pancreatic ducts of six common marmosets (Callithrix jacchus) suffering from severe non-diarrheic weight loss. Three individuals died naturally and the other three were euthanized. Microscopic findings showed the presence of adult flukes (Platynosomum) in the liver. These flukes, which provoke common infection in cats, were also observed inside the gallbladder as well as in the intra and extrahepatic bile ducts in common marmosets. Portal fibrosis was observed in two animals, which developed chronic fibrosing hepatopathy (biliary pattern, grade 3). The disease progresses without diarrhea and without pancreatic lesions or infestation. With the rogression, the animals presented with ascending cholangitis, cholestasis and portal fibrosis, sometimes culminating in secondary biliary cirrhosis. Therefore, this nfirmity, associated with chronic weight loss in common marmosets, could be another tiological factor linked with WMS

Testicular volume and reproductive status of Wild Callithrix jacchus

ARAÚJO, Arrilton ; SOUSA, Maria Bernardete Cordeiro . Testicular volume and reproductive status of Wild Callithrix jacchus. International Journal of Primatology, v.29, p.1355–1364, 2008. DOI 10.1007/s10764-008-9291-4

Efeito do parceiro social sobre a resposta comportamental ao ambiente novo em sagüi comum (Callithrix jacchus)

Algumas pesquisas demonstram que a presença de um parceiro social durante uma situação de risco modula a resposta ao estresse, atenuando seus efeitos negativos. Neste estudo, 8 díades de machos e 8 de fêmeas de sagüi comum (Callithrix jacchus) foram expostos a um ambiente novo, sozinhos e acompanhados de um parceiro de mesmo sexo e idade. Quando submetidos a um ambiente novo em companhia de um animal de mesmo sexo, os machos apresentaram um perfil mais filiativo enquanto as fêmeas foram mais competitivas entre si. Os resultados mostram que a resposta comportamental é sexualmente dimórfica, e que machos e fêmeas utilizam diferentes estratégias quando confrontados com situações desafiadoras no ambiente natural Abstract Some researches demonstrate that the presence of a social partner during a challenging situation modulates the stress response, decreasing its negative effects. In this study common marmoset (Callithrix jacchus) males and females were exposed to a new environment, alone or in companion of a social partner of the same sex and age. When submitted to new environment in companion of a same-sex social partner males showed more affiliation whereas females performed agonistic behaviors. The results show that behavioral response is sexually dimorphic and that males and females used different strategies when facing challenging situations in natural conditions

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infant’s birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both

The Pair-Bond Formation and Its Role in the Stimulation of Reproductive Function in Female Common Marmosets (Callithrix jacchus)

SILVA, H.P.A.; SOUSA, M.B.C. The pair-bond formation and its role in the stimulation of reproductive function in female common marmosets (collithrix Jacchus). International Journal of Primatology, v, 18, n.3, p.387-400, 1997.