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A callosal projection of area 17 upon the border region of area MT in the marmoset monkey, Callithrix jacchus.

Injections of the retrograde tracer HRP into the border region of the temporal visual area MT and adjoining cortex in Callithrix labeled pyramidal neurons in area 17 of the contralateral hemisphere. Evidence is presented that this newly discovered heterotopic callosal projection of the monkey striate cortex connects regions of representation of the zero vertical meridian of the visual field in a retinotopic order.

Animals↗

Studies on the evolution of multiple somatosensory representations in primates: the organization of anterior parietal cortex in the New World Callitrichid, Saguinus.

Because members of the New World family, Callithricidae, are generally regarded as the most primitive of monkeys, we studied the organization of somatosensory cortex in the tamarin (Saguinus) in hopes of better understanding differences in the organization of anterior parietal cortex in primates and how these differences relate to phylogeny. In most prosimian primates only one complete representation of cutaneous receptors has been found in the region of primary cortex, S-I, while in all Old and New World monkeys studied to date, two cutaneous representations exist in distinct architectonic fields, areas 3b and 1. In detailed microelectrode mapping studies in anesthetized tamarins, only one complete representation responsive to low-threshold cutaneous stimulation was evident in the S-I region. This topographic representation was in a parietal koniocortical field that architectonically resembles area 3b of other monkeys, and the general somatotopic organization of the field was similar to that of area 3b of other monkeys. Cortex rostral to the single representation was generally unresponsive to somatosensory stimuli, or required more intense stimulation for neural activation. Cortex caudal to the representation, in the region of area 1 of other monkeys, was generally either unresponsive or responded to only high-threshold stimulation, although some recording sites were activated by low-threshold tactile stimulation. The present evidence, together with that from previous studies, suggests that the single, complete body surface representation in Saguinus is homologous to the S-I representation found in some prosimians (Galago, Perodicticus) and the area 3b cutaneous representation found in New World Cebidae (Aotus, Saimiri, and Cebus) and Old World Macaca. Cortex rostral to S-I in Saguinus has the appearance of areas 3a and 4 of other primates. The cortex caudal to S-I in Saguinus, while resembling area 1 in some ways, does not have all of the features of area 1 of other monkeys. In particular, the field was not easily activated by low-threshold cutaneous stimuli, as area 1 is in other monkeys, and therefore a second cutaneous representation of all body parts was not demonstrated. Thus, cortex in the expected location of area 1 of Saguinus was not as responsive as area 1 of other monkeys, and it somewhat resembled the high-threshold fringe zones found caudal to S-I in anesthetized prosimians and some nonprimates. The results raise the possibility that the area 1 cutaneous representation that is characteristic of other New World monkeys and Old World monkeys evolved from a less responsive precursor along the caudal border of S-I in early monkeys.

Animals↗

Organization of the callosal connections of visual areas V1 and V2 in the macaque monkey.

The interhemispheric efferent and afferent connections of the V1/V2 border have been examined in the adult macaque monkey with the tracers horseradish peroxidase and horseradish peroxidase conjugated to wheat germ agglutinin. The V1/V2 border was found to have reciprocal connections with the contralateral visual area V1, as well as with three other cortical sites situated in the posterior bank of the lunate sulcus, the anterior bank of the lunate sulcus, and the posterior bank of the superior temporal sulcus. Within V1, callosal projecting cells were found mainly in layer 4B with a few cells in layer 3. Anterograde labeled terminals were restricted to layers 2, 3, 4B, and 5. In extrastriate cortex, retrograde labeled cells were in layers 2 and 3 and only very rarely in infragranular layers. In the posterior bank of the lunate sulcus, labeled terminals were scattered throughout all cortical layers except layers 1 and 4. In the anterior bank of the lunate sulcus and in the superior temporal sulcus, anterograde labeled terminals were largely focused in layer 4. Callosal connections in all contralateral regions were organized in a columnar fashion. Columnar organization of callosal connections was more apparent for anterograde labeled terminals than for retrograde labeled neurons. In the posterior bank of the lunate sulcus, columns of callosal connections were superimposed on regions of high cytochrome activity. The tangential extent of callosal connections in V1 and V2 was found to be influenced by eccentricity in the visual field. Callosal connections were denser in the region of V1 subserving foveal visual field than in cortex representing the periphery. In V1 subserving the fovea, callosal connections extended up to 2 mm from the V1/V2 border and only up to 1 mm in more peripheral located cortex. In area V2 subserving the fovea, cortical connections extended up to 8 mm from the V1/V2 border and only up to 3 mm in peripheral cortex.

Animals↗

Postnatal development of dendrites of relay neurons in the lateral geniculate nucleus of the marmoset (Callithrix jacchus): a quantitative Golgi study.

Dendrites of multipolar relay neurons in the lateral geniculate nucleus of the marmoset (Callithrix jacchus), at various ages from birth to adulthood, were studied in rapid Golgi preparations. The dendrites were analyzed by means of three-dimensional computer reconstructions and decomposed into intermediate and terminal segments, both of which were further classified according to their centrifugal order. Measurements were made of the number of segments per dendrite, the total length of dendrites, and the mean length of intermediate and terminal segments. In adult marmosets, there are four stem dendrites on average per neuron, and each dendrite divides into a mean of 14 segments. Between birth and 6 weeks of age, the mean dendritic length doubles, mainly because of changes in terminal segments. There is a significant decrease in dendritic length into adulthood. The total number of stem dendrites does not change after birth, but during the first postnatal week dendrites lose distal segments, after which there is a significant increase in the number of segments of orders 3 to 7. The mean length of intermediate segments does not change with age, nor with order, whereas the length of terminal segments increases from 50 to 120 microns from birth to 6 weeks of age, and then decreases to the adult value of 80 microns. In conclusion, during the period of most rapid visual development, important morphological changes occur in geniculate relay-cell dendrites, involving essentially terminal segments. These observations correlate well with changes of geniculate volume and neuronal density.

Animals↗

Connections of the primary auditory cortex in the common marmoset, Callithrix jacchus jacchus.

The afferent and efferent connections of the primary auditory cortex (AI) of common marmosets were traced following small injections of wheat germ agglutinin conjugated with horseradish peroxidase (WGA-HRP) made at best frequency (BF)-defined sites in the AI. After the injections the animals remained anesthetized for 15-23 hours; they were then perfused transcardially with fixative and the brains were processed for WGA-HRP reaction product. Examination of the disposition of labelled material revealed the following results. First, patches of terminal labelling, and to a lesser extent retrograde labelling, were found outside the injection site in the ipsilateral cortex rostral and caudal to the AI. Second, the region of the contralateral cortex corresponding to the injection site contained labelled terminals throughout the depth of the cortex; labelled neurons were found in the middle layers. Third, in each experiment a discrete region of the medial geniculate body (MG) contained retrogradely labelled neurons interspersed with anterogradely labelled terminals. These regions had a banded appearance, were found in the dorsal and rostral half of the MG, and shifted in location progressively dorsalward as the injection site BF increased. The presence of projection zones rostral and caudal to the AI of marmosets, and the disposition of the MG sources of projection in relation to BF, are similar to observations made on other New World monkeys. The ipsilateral corticocortical projections confirm electrophysiological evidence suggesting the existence of auditory fields rostral and caudal to the AI. The thalamocortical auditory system of the marmoset appears relatively simple, with a comparatively undifferentiated MG projecting to a cortical auditory system dominated by a large AI.

Animals↗

Serotoninergic system in the brainstem of the marmoset: a combined immunocytochemical and three-dimensional reconstruction study.

The distribution and morphology of serotoninergic neurons in the marmoset (New-World monkey) brainstem were studied by immunocytochemistry and computer-assisted three-dimensional reconstruction. The cytoarchitectonic localization of serotoninergic neurons was ascertained in series of adjacent immunostained and Nissl-stained sections, and the extent and shape of the serotoninergic nuclei were visualized by computer reconstruction. The overall distribution of the immunoreactive neurons is comparable to that already described for several species of primates. The serotoninergic nuclei are spatially well segregated into an anterior and a posterior group. The anterior group, in the mesencephalon and the rostral pons, contains the largest population of serotoninergic neurons. These neurons are not confined to the raphe nuclei near the midline, but rather expand laterally in the reticular formation. This expanded distribution of the neurons in the anterior group results in a partial fusion of the nuclei. In some nuclei, particularly the median raphe, subdivisions can be clearly delineated on the basis of the distinct morphology of the neurons and of their clustering. The neurons of the posterior group, in the caudal pons and the medulla, are almost all contained within the limits of the raphe nuclei. The serotoninergic neurons located in the reticular formation form a lateral column, which is clearly separated from the serotoninergic neurons found near the midline. Immunoreactive axons are distributed throughout the brainstem, but they innervate certain motor and sensory nuclei more densely. It was consistently found in newborn animals that the overall immunoreactive axonal network was richer than in juveniles or adults, suggesting that there may be a major modification in the function of the serotoninergic system around birth.

Animals↗

Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus.

The distribution of choline acetyltransferase-immunoreactive (ChAT-IR) neurons was studied in the brain of the common marmoset by using immunohistochemistry. ChAT-IR neurons were found in the medial septal nucleus, vertical and horizontal limb nuclei of the diagonal band, the nucleus basalis of Meynert, pedunculopontine nucleus and laterodorsal tegmental nucleus, and also in the striatum, habenula, and brainstem cranial nerve motor nuclei. The organization of ChAT-IR neurons in the basal forebrain, midbrain, and pons is consistent with the Ch1-Ch6 nomenclature introduced by Mesulam et al. ('83). The combination of the retrograde transport of HRP-WGA with ChAT immunohistochemistry revealed the distribution of neurons in the Ch4 cell group projecting to the dorsolateral prefrontal cortex. The activity of ChAT was highest in limbic cortical structures, such as the hippocampus, and lowest in association areas of the neocortex. Lesions at various loci in the basal forebrain resulted in differential patterns of ChAT loss in the cortex, which suggests some degree of topographical organization of Ch4 projections to the cortical mantle.

Animals↗

Connections of primary auditory cortex in the New World monkey, Saguinus.

Connections of primary auditory cortex (A-I) were investigated in the tamarin (Saguinus fuscicollis), a New World monkey. In each case, A-I was defined by multiunit recordings, and best frequencies were determined for neurons at different recording sites. Microlesions were placed to mark recording sites for correlation with cortical architecture. Following mapping, separate injections of up to three different tracers (HRP-WGA and fluorescent dyes) were placed into the representations of different frequencies within A-I. The results support several conclusions: (1) high to low frequencies are represented in a dorsocaudal to ventrorostral sequence in A-I, (2) intrinsic connections in A-I are more pronounced along isofrequency contours, (3) the pattern of connections between A-I and adjoining cortex suggests that this surrounding auditory cortex contains at least two tonotopically organized fields and possibly one or more additional auditory fields, (4) callosal connections of A-I are largely between parts of A-I matched for frequency representation, (5) thalamic connections of A-I include topographic connections with the ventral division of the medial geniculate complex (MGv) and more diffuse connections with the medial (MGm) and dorsal (MGd) divisions of the medial geniculate complex and the suprageniculate nucleus (Sg), and (6) A-I projects bilaterally to the dorsal cortex of the inferior colliculus.

Acoustic Stimulation↗

Distribution of two morphologically distinct subsets of serotoninergic axons in the cerebral cortex of the marmoset.

The serotoninergic innervation of the marmoset (New World monkey, Callithrix jacchus) cerebral cortex has been analyzed by using immunocytochemistry. The use of a sensitive monoclonal antibody against serotonin allowed the visualization of the fine morphology of individual axons. Two types of terminal axons were demonstrated: one has sparse, small, ovoid varicosities (dia. less than 1 micron), and the other has large, spheroidal varicosities (up to 5 microns in dia.), which are more densely clustered. The first type of axon is distributed through all cortical layers, with a characteristic laminar distribution that varies from area to area. The second type of axons was distributed sparsely in all regions but was markedly denser in the frontal and anterior parietal lobes, and in the hippocampal formation. Axons with large varicosities typically surrounded certain cell bodies and proximal dendrites, forming pericellular arrays, or baskets. These morphological specializations were most frequent in the frontal and anterior parietal cortex, where they were found around stellate and horizontal cells in layer I and around stellate and bipolar cells in layer II and III. Similar baskets were also found in the hippocampal formation, mainly along the border between the hilus and the granule cell layer of the dentate gyrus, across the CA4 field, and at each side of the pyramidal cell layer of the CA3 regions. The distribution and cellular morphology of the cell surrounded by the 5-HT basket fibres were suggestive of a subpopulation of interneurons, possibly GABAergic and/or peptidergic. In agreement with previous reports on the innervation of the cerebral cortex of other mammalian species, the marmoset cerebral cortex is innervated by two separate subsystems of serotoninergic axons. One of these may have a strong and specific influence on the cortical inhibitory circuitry, via relay through cortical interneurons.

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↗

High motivation toward food increases food-sharing in cotton-top tamarins.

In order to explore whether or not adult motivation influences transfer of food to infants in cotton-top tamarins (Saguinus oedipus oedipus), 2 experiments were carried out with 3 large captive family groups. Examination of (a) natural changes in food motivation during feeding, and (b) elevated motivation toward food by giving highly preferred items, showed that the adult monkeys shared food more when their own level of motivation was high. This suggests that food-transfer is not merely a consequence of adult satiation, but that matching sharing with high adult motivation is a mechanism which ensures that infants receive ample food, the best items, and also rare items of high quality.

Animals↗

Gender differences in caring for infant Cebuella pygmaea: the role of infant age and relatedness.

This paper describes a three-part study of the parenting behaviors of 6 family groups of Cebuella pygmaea (pygmy marmosets). In the first part, the parenting patterns of undisturbed family groups housed under laboratory conditions were scored throughout the first 10 weeks following the birth of their second infant(s). To further investigate the role of infant age in determining parental behavior, caretaking patterns were studied after a brief separation of infants of varying ages from their families. Finally, an unrelated infant, age 1-5 weeks, was placed inside the home cage of each family, and caretaking of this novel infant was scored. The main findings that emerged from the study were: (1) sex differences in carrying the infants were dependent upon the age of the infant, i.e., adult females were the predominant carriers of infants less than or equal to 3 weeks of age and males (either adult or juvenile) the main carriers for infants greater than 3 weeks of age; (2) some caretaking behaviors, e.g., grooming and protective retrieval, were performed predominantly by the adult females throughout infancy; and (3) the relatedness of the infant, i.e., one's own vs. another's, appeared to primarily affect the behavior of adult females. In general, experimental manipulations confirmed results of the observational part of the study and thus may be useful paradigms for testing specific hypotheses about parental behaviors.

Age Factors↗

Analysis of DR-like molecules on a marmoset Epstein-Barr virus-induced cell line using a monomorphic anti-human HLA-DR monoclonal antibody.

Mouse anti-HLA D region-related (DR) monoclonal antibodies have been found to cross-react with peripheral blood leukocytes from one primate species, the common marmoset (Callithrix jacchus). Immunoprecipitates of radioactively labeled cells extracted from a marmoset Epstein-Barr virus-induced cell line were analyzed by one- and two-dimensional gel electrophoresis and compared with the DR antigens of a human lymphoblastoid B cell line. Two chains of estimated molecular weights of 34 000 (alpha) and 28 000 (beta), similar to the human alpha and beta chains, have been observed in marmoset immunoprecipitates. Additionally, a set of spots located in the same area as the set of invariant spots found in human HLA-DR antigens is shown by two-dimensional gel electrophoresis. Thus, cross-reacting anti-human HLA-DR monoclonal antibodies could be used to analyze the expression and the structure of marmoset DR-like antigens.

Animals↗

Interleukin 2 production by a marmoset B cell line.

Several B cell lines constitutively secreting interleukin (IL) 2 were derived from the Epstein-Barr virus-positive marmoset B cell line, B95-8. A representative line, KRC-18, was cloned by limiting dilution and found to be 40% surface IgM+, 60% cytoplasmic IgM+, greater than 95% DR+, weakly Tac+ and devoid of T cell, monocyte and NK cell surface antigens. Supernatant from KRC-18 cells supported the long-term growth of an IL 2-dependent murine T cell line, HT-2, and contained 7-8 units/ml of IL 2 activity when compared to recombinant IL 2. The supernatant was fractionated by Sephadex G-75 gel filtration, and maximal proliferation of HT-2 cells was supported by the 20-22-kDa column fraction. The proliferative response of HT-2 cells to KRC-18 supernatant was inhibited by monoclonal antibodies to human IL 2 or the murine IL 2 receptor in a dose-dependent manner, suggesting that the KRC-18 IL 2 has epitopes that are similar to human IL 2, and that its activity is mediated through binding to the IL 2 receptor of the target cell line. When KRC-18 cells were analyzed for cytoplasmic IL 2, greater than 90% of the cells contained intracellular IL 2 in amounts equivalent to, or greater than, mitogen-activated T cells. These data indicate that certain B lineage cell lines are capable of IL 2 synthesis and secretion.

Animals↗

Studies of GB hepatitis agent in tamarins.

Three tamarins (Saguinus labiatus), two of which had previously been infected with hepatitis A virus and parenteral non-A, non-B hepatitis, were inoculated intravenously with the agent of GB hepatitis. All three animals developed alanine aminotransferase abnormalities 2 weeks after inoculation. Peak alanine aminotransferase levels were recorded 4 weeks postinoculation. These declined thereafter but continued to fluctuate at abnormal levels for 32 weeks. Liver biopsies showed liver cell swelling and inflammation with focal necrosis. Portal tracts and areas around central veins were heavily infiltrated with mononuclear cells. A fourth animal (no previous exposure to hepatitis viruses) inoculated with GB was killed on Day 15 postinoculation. Serum and extracts of liver and feces from this day were used as inocula for three other animals. Only the serum and liver extract transmitted GB hepatitis. The fecal specimen did not transmit and a fecal extract taken at a later date from another animal was also noninfectious. GB hepatitis virus is distinct from the viruses causing Type A and blood-borne non-A, non-B-hepatitis. Although the virus is present in serum and has previously been transmitted per os, it is not shed in feces.

Alanine Transaminase↗

Lymphoproliferative disease in a cotton-top marmoset after inoculation with infectious mononucleosis-derived Epstein-Barr virus.

Injection of concentrated EBV derived from cells of the Kaplan line of infectious mononucleosis (IM) origin resulted in malignant lymphoproliferation in one out of three cotton-top marmosets 6 weeks after inoculation. Two additional animals receiving the same isolate after incubation with an antibody-containing human serum did not develop tumors. Inoculation of concentrated virus derived from the P3HR-1 line of Burkitt origin did not lead to lymphoproliferations in five marmosets. Three of these received non-neutralized, and two received neutralized P3HR-1 virus. The tumor obtained with the Kaplan isolate revealed characteristics of a lymphosarcome. It contained EBV-specific DNA. In addition, EBV-synthesizing lymphoblastoid lines were established from a tumorous lymph-node, as well as from the spleen of the diseased marmoset. Virus recovered from these lines transformed lymphocytes derived from spleens of healthy marmosets. The tumor-bearing animal developed low levels of anti-VCA antibodies during the course of tumor growth. These data demonstrate the oncogenic potential of EBV directly derived from cells of IM origin.

Animals↗

Characteristics of three strains of feline fibrosarcoma virus grown in cat and marmoset monkey cells.

Two strains of feline fibrosarcoma virus (ST-FeSV and GA-FeSV) were found to induce tumors in cats and marmosets, and to transform feline and marmoset cells in vitro after primary inoculation. A third strain (SM-FeSV) failed to induce tumors or transform marmoset cells after primary inoculation; however, when SM-FeSV-injected marmoset cultures were passed 26 times in vitro, the cell cultures released infectious virus which transformed marmoset fibroblasts but still failed to induce tumors in marmosets. ST-FeSV induced mainly round-cell type transformation (r foci), GA-FeSV induced predominantly mixed round-fusiform cell type transformation (fr foci), and SM-FeSV induced r and fr type foci with a higher proportion of fusiform cells in the fr foci than seen with GA-FeSV. Transforming virus was obtained from r or mixed r/fr foci of ST-FeSV but not from fr foci; heat treatment changed the virus from producing almost exclusively r type foci to inducing an increased number of fr foci. Passage of FeSV in cat cells yielded viruses with a higher ratio of infectivity for feline vs marmoset cells, while passage of FeSV in marmoset cells yielded virus with a relatively higher infectivity ratio for marmoset cells; the three strains differed in the degree of change in the infectivity ratio. Despite the alteration of host range of SM-FeSV propagated in marmoset fibroblasts, the virus retained feline P-30 antigen by CF and FA assays. Neutralization tests did not indicate but also did not exclude an alteration of the surface antigens of ST-FeSV or SM-FeSV propagated in marmoset fibroblasts. The alteration of the relative infectivity of FeSV during passage in marmoset cells may be due to: (1) the selection of a variant present in the original heterogenous uncloned population; (2) mutation; or (3) recombination with some marmoset genetic material, possibly an as yet unidentified endogenous marmoset virus.

Animals↗

Epstein-Barr virus: experimental infection of Callithrix jacchus marmosets.

Eight common marmoset monkeys (Callithrix jacchus) were inoculated with about 10(4) transforming units of B95-8 virus; seven of the marmosets died 50-111 days post inoculation and all seven showed microscopic and/or macroscopic lesions compatible with a diagnosis of lymphoproliferative disease. Low levels of anti-VCA antibodies were detected in plasma from six marmosets. Attempts failed to establish continuous EBV-carrying lymphoblastoid cell cultures by cultivation in vitro of circulating lymphocytes or minced lymphoid tissues obtained at necropsy.

Animals↗