Virtually nothing is known about the morphology of cortical neurons in the elephant. To this end, the current study provides the first documentation of neuronal morphology in frontal and occipital regions of the African elephant (Loxodonta africana). Cortical tissue from the perfusion-fixed brains of two free-ranging African elephants was stained with a modified Golgi technique. Neurons of different types (N=75), with a focus on superficial (i.e., layers II-III) pyramidal neurons, were quantified on a computer-assisted microscopy system using Neurolucida software. Qualitatively, elephant neocortex exhibited large, complex spiny neurons, many of which differed in morphology/orientation from typical primate and rodent pyramidal neurons. Elephant cortex exhibited a V-shaped arrangement of bifurcating apical dendritic bundles. Quantitatively, the dendrites of superficial pyramidal neurons in elephant frontal cortex were more complex than in occipital cortex. In comparison to human supragranular pyramidal neurons, elephant superficial pyramidal neurons exhibited similar overall basilar dendritic length, but the dendritic segments tended to be longer in the elephant with less intricate branching. Finally, elephant aspiny interneurons appeared to be morphologically consistent with other eutherian mammals. The current results thus elaborate on the evolutionary roots of Afrotherian brain organization and highlight unique aspects of neural architecture in elephants.
Von Economo neurons (VENs), previously found in humans, all of the great ape species, and four cetacean species, are also present in African and Indian elephants. The VENs in the elephant are primarily found in similar locations to those in the other species. They are most abundant in the frontoinsular cortex (area FI) and are also present at lower density in the anterior cingulate cortex. Additionally, they are found in a dorsolateral prefrontal area and less abundantly in the region of the frontal pole. The VEN morphology appears to have arisen independently in hominids, cetaceans, and elephants, and may reflect a specialization for the rapid transmission of crucial social information in very large brains. Anat
Von Economo neurons (VENs) are a type of large, layer V spindle-shaped neurons that were previously described in humans, great apes, elephants, and some large-brained cetaceans. Here we report the presence of Von Economo neurons in the anterior cingulate (ACC), anterior insular (AI), and frontopolar (FP) cortices of small odontocetes, including the bottlenose dolphin (Tursiops truncatus), the Risso's dolphin (Grampus griseus), and the beluga whale (Delphinapterus leucas). The total number and volume of VENs and the volume of neighboring layer V pyramidal neurons and layer VI fusiform neurons were obtained by using a design-based stereologic approach. Two humpback whale (Megaptera novaeangliae) brains were investigated for comparative purposes as representatives of the suborder Mysticeti. Our results show that the distribution of VENs in these cetacean species is comparable to that reported in humans, great apes, and elephants. The number of VENs in these cetaceans is also comparable to data available from great apes, and stereologic estimates indicate that VEN volume follows in these cetacean species a pattern similar to that in hominids, the VENs being larger than neighboring layer V pyramidal cells and conspicuously larger than fusiform neurons of layer VI. The fact that VENs are found in species representative of both cetacean suborders in addition to hominids and elephants suggests that these particular neurons have appeared convergently in phylogenetically unrelated groups of mammals possibly under the influence of comparable selective pressures that influenced specifically the evolution of cortical domains involved in complex cognitive and social/emotional processes.
The human insular cortex is involved in a variety of viscerosensory, visceromotor, and interoceptive functions, and plays a role in complex processes such as emotions, music, and language. Across mammals, the insula has considerable morphologic variability. We review the structure and connectivity of the insula in laboratory animals (mouse, domestic cat, macaque monkey), and we present original data on the morphology and cytoarchitecture of insular cortex in less common species including a large carnivore (the Atlantic walrus, Odobenus rosmarus), two artiodactyls (the pigmy hippopotamus, Hexaprotodon liberiensis, and the Western bongo, Tragelaphus eurycerus), two cetaceans (the beluga whale, Delphinapterus leucas, and the minke whale, Balaenoptera acutorostrata), and a sirenian (the Florida manatee, Trichechus manatus latirostris). The insula shows substantial variability in shape, extent, and gyral and sulcal patterns, as well as differences in laminar organization, cellular specialization, and structural association with the claustrum. Our observations reveal that the insular cortex is extremely variable among mammals. These differences could be related to the role exerted by specific and selective pressures on cortical structure during evolution. We conclude that it is not possible to identify a general model of organization for the mammalian insular cortex.
Von Economo neurons (VENs) are defined by their thin, elongated cell body and long dendrites projecting from apical and basal ends. These distinctive neurons are mostly present in anterior cingulate (ACC) and fronto-insular (FI) cortex, with particularly high densities in cetaceans, elephants, and hominoid primates (i.e., humans and apes). This distribution suggests that VENs contribute to specializations of neural circuits in species that share both large brain size and complex social cognition, possibly representing an adaptation to rapidly relay socially-relevant information over long distances across the brain. Recent evidence indicates that unique patterns of protein expression may also characterize VENs, particularly involving molecules that are known to regulate gut and immune function. In this study, we used quantitative stereologic methods to examine the expression of three such proteins that are localized in VENs -activating-transcription factor 3 (ATF3), interleukin 4 receptor (IL4Rα) and neuromedin B (NMB). We quantified immunoreactivity against these proteins in different morphological classes of ACC layer V neurons of hominoids. Among the different neuron types analyzed (pyramidal, VEN, fork, enveloping, and other multipolar), VENs showed the greatest percentage that displayed immunostaining. Additionally, a higher proportion of VENs in humans were immunoreactive to ATF3, IL4Rα, and NMB than in other apes. No other ACC layer V neuron type displayed a significant species difference in the percentage of immunoreactive neurons. These findings demonstrate that phylogenetic variation exists in the protein expression profile of VENs, suggesting that humans might have evolved biochemical specializations for enhanced interoceptive sensitivity.
Von Economo neurons (VENs) are specialized projection neurons with a characteristic spindle-shaped soma and thick basal and apical dendrites. VENs have been described in restricted cortical regions, with their most frequent appearance in layers III and V of the anterior cingulate cortex, anterior insula, and frontopolar cortex of humans, great apes, macaque monkeys, elephants, and some cetaceans. Recently, a ubiquitous distribution of VENs was reported in various cortical areas in the pygmy hippopotamus, one of the closest living relatives of cetaceans. That finding suggested that VENs might not be unique to only a few species that possess enlarged brains. In the present analysis, we assessed the phylogenetic distribution of VENs within species representative of the superordinal clade that includes cetartiodactyls and perissodactyls, as well as afrotherians. In addition, the distribution of fork cells that are often found in close proximity to VENs was also assessed. Nissl-stained sections from the frontal pole, anterior cingulate cortex, anterior insula, and occipital pole of bowhead whale, cow, sheep, deer, horse, pig, rock hyrax, and human were examined using stereologic methods to quantify VENs and fork cells within layer V of all four cortical regions. VENs and fork cells were found in each of the species examined here with species-specific differences in distributions and densities. The present results demonstrated that VENs and fork cells were not restricted to highly encephalized or socially complex species, and their repeated emergence among distantly related species seems to represent convergent evolution of specialized pyramidal neurons. The widespread phylogenetic presence of VENs and fork cells indicates that these neuron morphologies readily emerged in response to selective forces,whose variety and nature are yet to be identified.
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