Primate Organization Research Articles

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair‐living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair-living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio-collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair-living anthropoid primates. Findings support the hypothesis that social relations in pair-living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode.

Evolution of a behavior-linked microsatellite-containing element in the 5' flanking region of the primate AVPR1A gene

BackgroundThe arginine vasopressin V1a receptor (V1aR) modulates social cognition and behavior in a wide variety of species. Variation in a repetitive microsatellite element in the 5' flanking region of the V1aR gene (AVPR1A) in rodents has been associated with variation in brain V1aR expression and in social behavior. In humans, the 5' flanking region of AVPR1A contains a tandem duplication of two ~350 bp, microsatellite-containing elements located approximately 3.5 kb upstream of the transcription start site. The first block, referred to as DupA, contains a polymorphic (GT)25 microsatellite; the second block, DupB, has a complex (CT)4-(TT)-(CT)8-(GT)24 polymorphic motif, known as RS3. Polymorphisms in RS3 have been associated with variation in sociobehavioral traits in humans, including autism spectrum disorders. Thus, evolution of these regions may have contributed to variation in social behavior in primates. We examined the structure of these regions in six ape, six monkey, and one prosimian species.ResultsBoth tandem repeat blocks are present upstream of the AVPR1A coding region in five of the ape species we investigated, while monkeys have only one copy of this region. As in humans, the microsatellites within DupA and DupB are polymorphic in many primate species. Furthermore, both single (lacking DupB) and duplicated alleles (containing both DupA and DupB) are present in chimpanzee (Pan troglodytes) populations with allele frequencies of 0.795 and 0.205 for the single and duplicated alleles, respectively, based on the analysis of 47 wild-caught individuals. Finally, a phylogenetic reconstruction suggests two alternate evolutionary histories for this locus.ConclusionThere is no obvious relationship between the presence of the RS3 duplication and social organization in primates. However, polymorphisms identified in some species may be useful in future genetic association studies. In particular, the presence of both single and duplicated alleles in chimpanzees provides a unique opportunity to assess the functional role of this duplication in contributing to variation in social behavior in primates. While our initial studies show no signs of directional selection on this locus in chimps, pharmacological and genetic association studies support a potential role for this region in influencing V1aR expression and social behavior.

Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans.

The goal of the present study was to determine whether the architectonic criteria used to identify the core region in macaque monkeys (Macaca mulatta, M. nemestrina) could be used to identify a homologous region in chimpanzees (Pan troglodytes) and humans (Homo sapiens). Current models of auditory cortical organization in primates describe a centrally located core region containing two or three subdivisions including the primary auditory area (AI), a surrounding belt of cortex with perhaps seven divisions, and a lateral parabelt region comprised of at least two fields. In monkeys the core region can be identified on the basis of specific anatomical and physiological features. In this study, the core was identified from serial sets of adjacent sections processed for cytoarchitecture, myeloarchitecture, acetylcholinesterase, and cytochrome oxidase. Qualitative and quantitative criteria were used to identify the borders of the core region in individual sections. Serial reconstructions of each brain were made showing the location of the core with respect to gross anatomical landmarks. The position of the core with respect to major sulci and gyri in the superior temporal region varied most in the chimpanzee and human specimens. Although the architectonic appearance of the core areas did vary in certain respects across taxonomic groups, the numerous similarities made it possible to identify unambiguously a homologous cortical region in macaques, chimpanzees, and humans.

Determinants of group size in the red colobus monkey ( Procolobus badius ): an evaluation of the generality of the ecological-constraints model

The ecological-constraints model proposes that increased group size increases within-group feeding competition, necessitating increased travel and, consequently, constraining group size. Previous studies have supported the model for frugivores, but its applicability to folivores remains untested. This study evaluated the generality of the model by re-examining the relationship between day range and group size for a folivorous species for which published accounts have not found a relationship between these factors. This study differs from earlier studies by accounting for variation in food availability, which may drive changes in day range. We quantified the relationships among food availability, day range, and group size for two red colobus groups at Kibale National Park, Uganda. Mean day range and home range were significantly greater for the group of 48 individuals compared to the group of 24 individuals. The large group traveled more and rested less than the small group. The large group also traveled more rapidly than the small group. Food availability significantly predicted mean day range for the large group, but not for the small group. Analyses of covariance demonstrated that the large and small group responded differently to changes in food availability. These observations suggest that the large red colobus group experiences greater levels of within-group feeding competition than the small group. This study provides added support for the generality of the ecological-constraints model and contributes toward an understanding of the mechanisms controlling feeding competition and social organization in primates.

Primates exposed to cocaine in utero display reduced density and number of cerebral cortical neurons.

This study examined the effects of cocaine use during the second trimester of pregnancy on cerebral neocortical volume and density, and total number of neocortical neurons and glia in offspring. We also evaluated the extent of postnatal recovery of cytoarchitectural abnormalities previously observed in the neocortex of two-month-old primates born from cocaine-treated mothers (Lidow [1995] Synapse 21:332-334). Pregnant monkeys received cocaine orally (20 mg/kg/day) from the 40th to 102nd days of pregnancy (embryonic day [E]40-E102). On E64 and E65, the animals were injected with [(3)H]thymidine. Cerebral hemispheres of the offspring were examined at three years of age. We found a reduction in the neocortical volume and density and total number of neocortical neurons. The observed reduction in neuronal number within the neocortex was not accounted for by the increase in the number of neurons in the white matter of cocaine-exposed animals, because the number of these "extra" neurons was equal to only half that of missing neurons. We detected no significant changes in the number of neocortical glia. The cytoarchitectural abnormalities in the neocortex of prenatally cocaine-exposed three-year-old monkeys closely resembled previously described neocortical abnormalities in similarly exposed two-month-old animals: the neocortex lacked a discernible lamination; the majority of the cells labeled by [(3)H]thymidine injected during neocortical neurogenesis did not reach their proper position within the cortical plate. Therefore, postnatal maturation is not associated with significant improvement in neocortical organization in primates prenatally exposed to cocaine. There was, however, a postnatal recovery of low glial fibrillary acidic protein (GFAP) immunoreactivity previously observed in 2-month-old cocaine-exposed animals.

Characterization of the Human Xq21.3/Yp11 Homology Block and Conservation of Organization in Primates

The Xq21.3/Yp11 homology block on the human sex chromosomes represents a recent addition to the Y chromosome through a transposition event. It is believed that this transfer of material occurred after the divergence of the hominid lineage from other great apes. In this paper we investigate the structure and evolution of the block through fluorescence in situ hybridisation, contig assembly, the polymerase chain reaction, exon trapping, sequence comparison, and annotation of sequence data. The overall structure is well conserved between the human X chromosome and the Y chromosome as well as between the X chromosomes from different primates. Although the sequence data reveal a high level of nucleotide sequence identity for the human X and Y, there are regions of significant divergence, such as that around the marker DXS214. These are presumably the consequence of multiple rearrangements during evolution and are of particular importance with respect to the potential gene content in this segment of the interval.

Chapter 18 Visual cortex organization in primates: theories of V3 and adjoining visual areas

After years of experimentation and substantial progress, there is still only limited agreement on how visual cortex in primates is organized, and what features of this organization are variable or stable across lines of primate phylogeny. Only three visual areas, V1, V2, and MT, are widely recognized as common to all primates, although there are certainly more. Here we consider various concepts of how the cortex along the outer border of V2 is organized. An early proposal was that this region is occupied by a V3 that is as wide and as long as V2, and represents the visual hemifield as a mirror image of V2. We refer to this notion as the classical V3 or V3-C. Another proposal is that only the dorsal half of V3-C exists, the half representing the lower visual quadrant, and thus the representation is incomplete (V3-I) by half. A version of this proposal is that V3-I is discontinuous, extremely thin in places, and highly variable across individuals, much as a vestigial or degenerate structure might be (V3-IF-incomplete and fragmented). A fourth proposal is that there is no V3. Many results suggest that a series of visual areas border V2, none of which has the characteristics of V3. Alternatively, the possibility exists that primate taxa differ with regard to visual areas bordering V2. Currently, much of the supporting evidence for a classical V3 comes from fMRI studies in humans, much of the evidence for a series of bordering areas comes from New World Monkeys and prosimian galagos, and much of the evidence for a V3-I or V3-IF comes from macaque monkeys. Possibly all these interpretations of visual cortex organization are valid, but each for only one of the major groups of primate evolution. Here, we suggest that none of these interpretations is correct, and propose instead that a modified V3 (V3-M) exists in a similar form in all primates. This V3-M is smaller and thinner than V3-C, discontinuous in the middle, but with comparable dorsal and ventral halves representing the lower and upper visual hemifields, respectively. Because the evidence for V3-M is limited, and it stems in part from our ongoing but incomplete comparative studies of V1 connections in primates, this suggestion requires further experimental evaluation and it remains tentative.

Functional organization of tactile inputs from the hand in the cuneate nucleus and its relationship to organization in the somatosensory cortex

Central processing of tactile inputs from the hand begins in the main cuneate nucleus and continues in the thalamus and area 3b cortex. Little is known about cuneate functional organization in primates or about how cuneate and area 3b organization are related. In this study, neurophysiologic approaches were used to evaluate how tactile inputs from the hand and adjacent body are organized in the cuneate nucleus of squirrel monkeys. Cuneate data on the organization of hand inputs were then compared with analogous area 3b data from our earlier cortical studies that used the same approaches. Evaluations of several cuneate properties, including (1) responsiveness to tactile stimulation, (2) incidences and sizes of receptive fields, (3) somatotopic progressions, (4) properties of representations, and (5) relationships between functional inputs and cytochrome oxidase staining, suggest that tactile afferents from the hand form consistently organized cuneate representations that, in turn, relate to the parcellated organization of cuneate structural substrates. Comparisons of cuneate and area 3b organization indicate that tactile processing from the brainstem to cortex involves a preservation of tactile responsiveness and somatotopic organization but, in addition, involves transformations that produce receptive field sharpening, suppression of hairy hand inputs, amplification and refinement of glabrous inputs, and relocations of representations. Ascending lemniscal substrates are characterized by cascading excitatory convergence/divergence that increments at successively higher levels between sensory afferents and area 3b. It is suggested that the observed preservations and transformations reflect this organization but, in addition, reflect mechanisms that cause counterbalancing sharpening and suppressions of hand inputs. J. Comp. Neurol. 411:369–389, 1999. © 1999 Wiley-Liss, Inc.

Functional organization of tactile inputs from the hand in the cuneate nucleus and its relationship to organization in the somatosensory cortex

Central processing of tactile inputs from the hand begins in the main cuneate nucleus and continues in the thalamus and area 3b cortex. Little is known about cuneate functional organization in primates or about how cuneate and area 3b organization are related. In this study, neurophysiologic approaches were used to evaluate how tactile inputs from the hand and adjacent body are organized in the cuneate nucleus of squirrel monkeys. Cuneate data on the organization of hand inputs were then compared with analogous area 3b data from our earlier cortical studies that used the same approaches. Evaluations of several cuneate properties, including (1) responsiveness to tactile stimulation, (2) incidences and sizes of receptive fields, (3) somatotopic progressions, (4) properties of representations, and (5) relationships between functional inputs and cytochrome oxidase staining, suggest that tactile afferents from the hand form consistently organized cuneate representations that, in turn, relate to the parcellated organization of cuneate structural substrates. Comparisons of cuneate and area 3b organization indicate that tactile processing from the brainstem to cortex involves a preservation of tactile responsiveness and somatotopic organization but, in addition, involves transformations that produce receptive field sharpening, suppression of hairy hand inputs, amplification and refinement of glabrous inputs, and relocations of representations. Ascending lemniscal substrates are characterized by cascading excitatory convergence/divergence that increments at successively higher levels between sensory afferents and area 3b. It is suggested that the observed preservations and transformations reflect this organization but, in addition, reflect mechanisms that cause counterbalancing sharpening and suppressions of hand inputs.

THE STRUCTURE OF SOCIAL RELATIONSHIPS AMONG FEMALE SAVANNA BABOONS IN MOREMI RESERVE, BOTSWANA

Abstract Here we examine the effects of maternal kinship, reciprocity, and dominance rank on the social relationships of female baboons (Papio cynocephalus ursinus) in a well-habituated, free-ranging group in the Okavango Delta of Botswana. These data are useful for testing comparative hypotheses about the ecological and demographic factors that shape the evolution of social organization in primates and other animals. In this group, adult females had well-differentiated grooming relationships with one another, and limited their grooming to a relatively small subset of available partners. Although there were 19 adult females in the group, the average female groomed only 8 other females, and devoted at least 5% of her grooming to only four other females. Females groomed maternal kin at significantly higher rates and for significantly longer periods than they groomed other females. The bias in favor of maternal kin was not an artifact of a general attraction toward females of adjacent rank. However, members of high-ranking lineages did devote a relatively greater fraction of grooming to maternal kin than members of low-ranking lineages did. Females most often groomed the females from whom they received the most grooming and grooming was very evenly balanced within the majority of dyads. Female rank had little impact upon grooming patterns and there was no evidence that females competed overtly over access to high-ranking partners.

Chapter 15 Theories of visual cortex organization in primates: areas of the third level

This brief review has a few main points. (1) Early proposals on how extrastriate cortex is subdivided were inconsistent with each other, and differences in interpretation were not resolved. (2) Brodmann's proposal of two ring-like areas, 18 and 19, surrounding primary visual cortex gained great acceptance despite the lack of agreement among different investigators considering the same evidence. (3) The concepts of areas 18 and 19, transposed to signify V2 and V3, have had great impact on recent and even current theories of extrastriate visual cortex organization in primates. (4) Nevertheless, Brodmann's areas 18 and 19, as defined in humans and Old World monkeys, correspond to none of the fields currently proposed for these primates. (5) All or most mammals appear to have a V2, and there is now widespread complete agreement over the extent and organization of this area in all studied primates. V2 is commonly referred to as area 18 because of its correspondence to area 18 as defined by Brodmann is some mammals. Yet, we should recognize that V2 is about half the size of Brodmann's area 18 in Old World monkeys and humans. (6) Current concepts of V3 differ greatly from the ring-like area 19 of Brodmann. We question the validity and usefulness of retaining the concept of V3 in primates. Our proposal for DM and other visual areas along the outer border of V2 seems more consistent, not only with the evidence from New World monkeys, but with evidence from Old World and prosimian primates, and even mammals most closely related to primates (see Kaas and Preuss, 1993). In all of these primates and close relatives of primates, the evidence indicates that more than one field forms the outer border of V2.

Laminar organization of acetylcholinesterase and cytochrome oxidase in the lateral geniculate nucleus of prosimians

Hess and Rockland [Hess and Rockland (1983) Brain Res. 289, 322–325] proposed that the distribution of acetylcholinesterase within the lateral geniculate nucleus might correlate with the daily activity patterns shown by primates. In diurnal primates, the magnocellular laminae show a greater acetylcholinesterase reaction product. In nocturnal primates, the parvocellular laminae are more heavily stained. We have examined the laminar distribution of acetylcholinesterase and cytochrome oxidase in the lateral geniculate nucleus of a series of rare prosimian primates. In all prosimians examined, the most dense acetylcholinesterase reaction product is seen in the parvocellular layers of the lateral geniculate nucleus. Heavy cytochrome oxidase activity is seen in both the magnocellular and parvocellular layers, but not the koniocellular layers of the prosimian lateral geniculate nucleus. We have also employed a polyclonal antibody to choline acetyltransferase to examine the laminar organization or cholinergic activity in the Galago (Bushbaby) lateral geniculate nucleus. We report that choline acetyltransferase immunoreactivity does not correlate with acetylcholinesterase activity in the prosimian lateral geniculate nucleus. Although the lateral geniculate nucleus is more immunoreactive than most other thalamic structures and although the intercalated koniocellular laminae demonstrate somewhat lighter choline acetyltransferase immunoreactivity, no great difference in staining intensity is seen between the parvocellular and magnocellular laminae. In addition, we examined the phenotype of known inputs to assess the laminar specificity of cholinergic projections to the bushbaby lateral geniculate nucleus. Layer VI of primary visual cortex, which is known to be a source of acetylcholinesterase in the parvocellular layers, does not contain cholinergic cells, nor does the pretectal nucleus, which projects mainly to the parvocellular layers. The parabigeminal nucleus is cholinergic; however, this nucleus is known to project to the koniocellular layers, along with the noncholinergic superior colliculus. Finally, the pedunculopontine tegmental nucleus, which provides a strong input to many regions of the thalamus, including the lateral geniculate nucleus, is cholinergic. The laminar organization of its input to the lateral geniculate nucleus is not known. Increased acetylcholinesterase reaction product within the parvocellular layers of the lateral geniculate nucleus is common to all strepsirhine primates. The pattern is also seen in the only two nocturnal haplorhine primates, Tarsius and Aotus (owl monkey). The relation of this increased acetylcholinesterase activity to cholinergic function remains unclear. We note exceptions to the suggested correlation between nocturnality and increased density of acetylcholinesterase within the parvocellular layers. We hypothesize that rather than reflecting nocturnal/diurnal lifestyles, the acetylcholinesterase staining pattern may be a primitive feature of geniculate organization in primates.

Oculomotor nerve nuclear complex syndrome: A case with clinicopathological correlation

A patient presented with bilateral upward gaze palsy and right-sided ophthalmoplegia as prominent signs of a midbrain infarction. The lesion involved the third nerve nuclear complex and intramedullary nerve root of the right side. It extended to the hypothalamus, but was exclusively right-sided. This midbrain lesion may have been responsible for the left-sided superior rectus palsy, since this finding is consistent with current models of organization in primates, indicating that the superior rectus muscle is innervated by the contralateral oculomotor nucleus.

The pulvinar nucleus of Galago senegalensis.

The present study was undertaken to analyze the connections of the pulvinar nucleus in a prosimian. The experiments, which rely on the Fink-Heimer ('67) method for staining degenerating axons and their terminals, fall into two parts: first, the tracing of ascending tectal projections to the caudal thalamus and second, the tracing of projections from this thalamic target to the cortex. Large lesions of the superior colliculus resulted in dense degeneration in the caudal half of the inferior subdivision of the pulvinar complex. This pathway could be identified when the lesion was restricted to the superficial layers of the superior colliculus, signifying that it is a visual pathway. In general, the projections of the deep and superficial layers of the superior colliculus were distinct and in this respect Galago resembles Tupaia. The inferior pulvinar nucleus in turn projects to area MT, a conspicuous subdivision of the temporal cortex. The superior division of the pulvinar, in contrast to the inferior division, is not a major target of ascending projections from the superior colliculus and projects to the areas of the occipital and temporal lobe intercalated between areas MT and 17. When these results are compared with similar studies in nonprimates, notably studies of Tupaia, a striking difference in organization emerges. In Tupaia, and in distantly related mammals such as the squirrel, the target of the tecto-pulvinar system includes area 18 adjacent to area 17. This feature is important since the two parallel projection systems seem to be related to each other in terms of the way in which the zero vertical meridian is spatially represented. However, in Galago the subdivision of the pulvinar receiving projections arising from the superior colliculus does not project to area 18. Area 18 is indeed the target of pulvinar projections, but these projections arise from that portion of the pulvinar which is not a recipient of ascending tectal projections. It is not easy to see how this primate organization, if indeed the Galago is representative of primates, evolved from the organization reflected in Tupais.

RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT.

RECEPTIVE FIELDS AND FUNCTIONAL ARCHITECTURE IN TWO NONSTRIATE VISUAL AREAS (18 AND 19) OF THE CAT.