Regional specialization in pyramidal cell structure in the visual cortex of the galago: An intracellular injection study of striate and extrastriate areas with comparative notes on New World and Old World monkeys

Recent studies have revealed marked differences in the basal dendritic structure of layer III pyramidal cells in the cerebral cortex of adult simian primates. In particular, there is a consistent trend for pyramidal cells of increasing complexity with anterior progression through occipitotemporal cortical visual areas. These differences in pyramidal cell structure, and their systematic nature, are believed to be important for specialized aspects of visual processing within, and between, cortical areas. However, it remains unknown whether this regional specialization in the pyramidal cell phenotype is unique to simians, is unique to primates in general or is widespread amongst mammalian species. In the present study we investigated pyramidal cell structure in the prosimian galago (Otolemur garnetti). We found, as in simians, that the basal dendritic arbors of pyramidal cells differed between cortical areas. More specifically, pyramidal cells became progressively more spinous through the primary (V1), second (V2), dorsolateral (DL) and inferotemporal ( IT) visual areas. Moreover, pyramidal neurons in V1 of the galago are remarkably similar to those in other primate species, in spite of large differences in the sizes of this area. In contrast, pyramidal cells in inferotemporal cortex are quite variable among primate species. These data suggest that regional specialization in pyramidal cell phenotype was a likely feature of cortex in a common ancestor of simian and prosimian primates, but the degree of specialization varies between species. Copyright (C) 2005 S. Karger AG, Basel.

Fractal analysis as a tool for studying specialization in neuronal structure: The study of the evolution of the primate cerebral cortex and human intellect

We review recent findings that, using fractal analysis, have demonstrated systematic regional and species differences in the branching complexity of neocortical pyramidal neurons. In particular, attention is focused on how fractal analysis is being applied to the study of specialization in pyramidal cell structure during the evolution of the primate cerebral cortex. These studies reveal variation in pyramidal cell phenotype that cannot be attributed solely to increasing brain volume. Moreover, the results of these studies suggest that the primate cerebral cortex is composed of neurons of different structural complexity. There is growing evidence to suggest that regional and species differences in neuronal structure influence function at both the cellular and circuit levels. These data challenge the prevailing dogma for cortical uniformity.

Brain maps, great and small: lessons from comparative studies of primate visual cortical organization

In this paper, we review evidence from comparative studies of primate cortical organization, highlighting recent findings and hypotheses that may help us to understand the rules governing evolutionary changes of the cortical map and the process of formation of areas during development. We argue that clear unequivocal views of cortical areas and their homologies are more likely to emerge for 'core' fields, including the primary sensory areas, which are specified early in development by precise molecular identification steps. In primates, the middle temporal area is probably one of these primordial cortical fields. Areas that form at progressively later stages of development correspond to progressively more recent evolutionary events, their development being less firmly anchored in molecular specification. The certainty with which areal boundaries can be delimited, and likely homologies can be assigned, becomes increasingly blurred in parallel with this evolutionary/developmental sequence. For example, while current concepts for the definition of cortical areas have been vindicated in allowing a clarification of the organization of the New World monkey 'third tier' visual cortex (the third and dorsomedial areas, V3 and DM), our analyses suggest that more flexible mapping criteria may be needed to unravel the organization of higher-order visual association and polysensory areas.

Ipsilateral corticocortical projections to the primary and middle temporal visual areas of the primate cerebral cortex: area-specific variations in the morphology of connectionally identified pyramidal cells

We quantified the morphology of over 350 pyramidal neurons with identified ipsilateral corticocortical projections to the primary (V1) and middle temporal (MT) visual areas of the marmoset monkey, following intracellular injection of Lucifer Yellow into retrogradely labelled cells. Paralleling the results of studies in which randomly sampled pyramidal cells were injected, we found that the size of the basal dendritic tree of connectionally identified cells differed between cortical areas, as did the branching complexity and spine density. We found no systematic relationship between dendritic tree structure and axon target or length. Instead, the size of the basal dendritic tree increased roughly in relation to increasing distance from the occipital pole, irrespective of the length of the connection or the cortical layer in which the neurons were located. For example, cells in the second visual area had some of the smallest and least complex dendritic trees irrespective of whether they projected to V1 or MT, while those in the dorsolateral area (DL) were among the largest and most complex. We also observed that systematic differences in spine number were more marked among V1-projecting cells than MT-projecting cells. These data demonstrate that the previously documented systematic differences in pyramidal cell morphology between areas cannot simply be attributed to variable proportions of neurons projecting to different targets, in the various areas. Moreover, they suggest that mechanisms intrinsic to the area in which neurons are located are strong determinants of basal dendritic field structure.

Specializations of the granular prefrontal cortex of primates: Implications for cognitive processing

The biological underpinnings of human intelligence remain enigmatic. There remains the greatest confusion and controversy regarding mechanisms that enable humans to conceptualize, plan, and prioritize, and why they are set apart from other animals in their cognitive abilities. Here we demonstrate that the basic neuronal building block of the cerebral cortex, the pyramidal cell, is characterized by marked differences in structure among primate species. Moreover, comparison of the complexity of neuron structure with the size of the cortical area/region in which the cells are located revealed that trends in the granular prefrontal cortex (gPFC) were dramatically different to those in visual cortex. More specifically, pyramidal cells in the gPFC of humans had a disproportionately high number of spines. As neuron structure determines both its biophysical properties and connectivity, differences in the complexity in dendritic structure observed here endow neurons with different computational abilities. Furthermore, cortical circuits composed of neurons with distinguishable morphologies will likely be characterized by different functional capabilities. We propose that 1. circuitry in V1, V2, and gPFC within any given species differs in its functional capabilities and 2. there are dramatic differences in the functional capabilities of gPFC circuitry in different species, which are central to the different cognitive styles of primates. In particular, the highly branched, spinous neurons in the human gPFC may be a key component of human intelligence. (C) 2005 Wiley-Liss, Inc.

Efeito dos andrógenos na estabilização da preferência manual em machos adultos de sagui comum (Callithrix jacchus)

The role of steroids hormones on the behavior of vertebrates have been described as organizational and activational effects. These actions occur in different periods of the ontogenetic development as fetal, early post natal and during puberty (organizational effect) or modifying the expression of behavioral patterns during time life (activational effects). Studies on brain lateralization in hand use in human and non-human primates have shown that sexual hormones seems to participate in the process of handedness strength that begins in the puberal period and is stabilized at the adult age. The aim of this study was to investigate in adult male Callithrix jacchus if the strength of use of the hand in common marmoset adult male is stable (organizational effect) or androgens variations could affect its stability (activational effect). The preferential use of one hand in 14 common marmoset (Callithrix jacchus was studied in two contexts: (1) spontaneous holding food and directing the food to mouth (feeding episodes), and (2) forced reaching food tests where the animal have to reach the food through a hole within a cover plate with a central hole that allow the use of one hand only to reach the food. The records were made during 5 sessions/20 bouts each during baseline totalizing 100 episodes before two treatments. Firstly it was used GnRH antagonist: a single subcutaneous injection of 100µg de Cetrotide – acetate of cetrorrelix (Baxter Oncology GmbH, Germany) (n=10). Secondly, a single GnRH injection of 0.2mg of GnRH (Sigma – Aldrich) (n= 8) was used. After injections 20 successful attempts of hand use episodes was recorded in the 1st , 2 nd, 7th, 15th and 30 th days, totalizing in the whole period 100 episodes for each context, after both treatments. Fecal sampling to measure extracted fecal androgens was performed in all days of data collection across the length of the basal and during the experimental periods. Statistical analysis by mixed model, Tukey test to compare mean values after the two treatments, and Levene test to compare mean variance were used, all for p-value < 0.05. In basal phase 6 animals used preferentially the right hand, 5 the left and 3 were ambidextrous. Mean handedness index in basal phase were different from that after both treatment starting at 7th day. Mean variance of handedness index for spontaneous and forced activities does not differs before and after both treatments but the mean values for GnRH index were higher than that observed for its antagonist. These findings suggested that androgens have an activational effect on handedness in adult male C. jacchus

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.

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.

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

Circadian variation with a diurnal bimodal profile on scent-marking behavior in captive common marmosets (callitrhix jacchus)

Scent-marking behavior is associated with different behavioral contexts in callitrichids, including signalizing a territory, location of feeding resources, and social rank. In marmosets and tamarins it is also associated with intersexual communication. Though it appears very important for the daily routine of the individuals, very few researchers have investigated distribution through the 24-h cycle. In a preliminary report, we described a preferential incidence of this behavior 2 h before nocturnal rest in families of common marmosets. We expand the data using 8 family groups (28 subjects), 8 fathers, 6 mothers, 8 nonreproductive adults (4 sons and 4 daughters), and 6 juvenile (3 sons and 3 daughters) offspring that we kept in outdoor cages under natural environmental conditions. We recorded the frequency of anogenital scent marking for each group during the light phase, twice a wk, for 4 consecutive wks, from March 1998 to September 1999. Cosinor test detected 24- and 8-h variations in 89.3% and 85.7% of the subjects, respectively, regardless of sex or reproductive status. The 8-h component is a consequence of the 2 peaks for the behavior, at the beginning and end of the light phase. Daily distribution of scent marking is similar to that others described previously for motor activity in marmosets. The coincident rhythmical patterns for both behaviors seem to be associated with feeding behavior, as described for callitrichids in free-ranging conditions, involving an increase in foraging activities early in the morning and shortly before nocturnal rest

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