Inverted pyramidal neurons in chimpanzee sensorimotor cortex are revealed by immunostaining with monoclonal antibody SMI-32
TL;DR: The monoclonal antibody SMI-32 was used to label pyramidal cells of sensorimotor cortex in two chimpanzees and found that a small population of pyramsidal cells varied from this orientation, so that the apical dendrites were 20 degrees or more from radial, and were often inverted, extending away from the pial surface.
Abstract: We used the monoclonal antibody SMI-32 to label pyramidal cells of sensorimotor cortex in two chimpanzees.The majority of the pyramidal cells had typical vertically oriented apical dendrites that extended towards the pial surface. A small population of pyramidal cells varied from this orientation, so that the apical dendrites were 20 or more from radial, and were often inverted, extending away from the pial surface.When numbers of non-inverted and inverted pyramidal cells were compared, less than 1% were found to be inverted.
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TL;DR: Compared to Old World monkeys, the orofacial representation of area 4 in great apes and humans was characterized by an increased relative thickness of layer III and overall lower cell volume densities, providing more neuropil space for interconnections, suggesting phylogenetic differences in microstructure might provide an anatomical substrate for the evolution of greater volitional fine motor control of facial expressions in great ape and humans.
Abstract: Social life in anthropoid primates is mediated by interindividual communication, involving movements of the orofacial muscles for the production of vocalization and gestural expression. Although phylo
98 citations
TL;DR: The region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined, suggesting that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry.
Abstract: This study presents a comparative stereologic investigation of neurofilament protein- and calcium-binding protein-immunoreactive neurons within the region of orofacial representation of primary motor cortex (Brodmann's area 4) in several catarrhine primate species (Macaca fascicularis, Papio anubis, Pongo pygmaeus, Gorilla gorilla, Pan troglodytes, and Homo sapiens). Results showed that the density of interneurons involved in vertical interlaminar processing (i.e., calbindin- and calretinin-immunoreactive neurons) as well pyramidal neurons that supply heavily-myelinated projections (i.e., neurofilament protein-immunoreactive neurons) are correlated with overall neuronal density, whereas interneurons making transcolumnar connections (i.e., parvalbumin-immunoreactive neurons) do not exhibit such a relationship. These results suggest that differential scaling rules apply to different neuronal subtypes depending on their functional role in cortical circuitry. For example, cortical columns across catarrhine species appear to involve a similar conserved network of intracolumnar inhibitory interconnections, as represented by the distribution of calbindin- and calretinin-immunoreactive neurons. The subpopulation of horizontally-oriented wide-arbor interneurons, on the other hand, increases in density relative to other interneuron subpopulations in large brains. Due to these scaling trends, the region of orofacial representation of primary motor cortex in great apes and humans is characterized by a greater proportion of neurons enriched in neurofilament protein and parvalbumin compared to the Old World monkeys examined. These modifications might contribute to the voluntary dexterous control of orofacial muscles in great ape and human communication.
58 citations
Cites background from "Inverted pyramidal neurons in chimp..."
...…Sherwood/Holloway/Erwin/Hof studies of NPNFP staining in area 4 of macaques, chimpanzees, and humans [Baleydier et al., 1997; Preuss et al., 1997; Gabernet et al., 1999; Qi et al., 1999; Geyer et al., 2000], two prominent bands of immunoreactive tissue spanning layers III and V were apparent (fig....
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...Because the highest density of NPNFP staining typically occurs in these sublayers [Baleydier et al., 1997; Preuss et al., 1997; Gabernet et al., 1999; Qi et al., 1999; Geyer et al., 2000], a more restricted laminar analysis was pursued in order to enhance sensitivity to interspecific differences....
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TL;DR: The current study provides the first documentation of neuronal morphology in frontal and occipital regions of the African elephant and elaborate on the evolutionary roots of Afrotherian brain organization and highlight unique aspects of neural architecture in elephants.
Abstract: 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.
53 citations
Cites background from "Inverted pyramidal neurons in chimp..."
...%) of all pyramidal neurons (Qi et al. 1999)....
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...In chimpanzees, inverted pyramidal neurons are located in layers III, V and especially VI of sensorimotor cortices, constituting a small percentage (\1%) of all pyramidal neurons (Qi et al. 1999)....
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TL;DR: This study used immunohistochemistry to examine the distribution and morphology of neocortical neurons stained for nonphosphorylated neurofilament protein, calbindin, calretinin, parvalbumin, and neuropeptide Y in three xenarthran species and traced the evolution of certain cortical architectural traits using phylogenetic analysis.
Abstract: Interpreting the evolution of neuronal types in the cerebral cortex of mammals requires information from a diversity of species. However, there is currently a paucity of data from the Xenarthra and Afrotheria, two major phylogenetic groups that diverged close to the base of the eutherian mammal adaptive radiation. In this study, we used immunohistochemistry to examine the distribution and morphology of neocortical neurons stained for nonphosphorylated neurofilament protein, calbindin, calretinin, parvalbumin, and neuropeptide Y in three xenarthran species—the giant anteater (Myrmecophaga tridactyla), the lesser anteater (Tamandua tetradactyla), and the two-toed sloth (Choloepus didactylus)—and two afrotherian species—the rock hyrax (Procavia capensis) and the black and rufous giant elephant shrew (Rhynchocyon petersi). We also studied the distribution and morphology of astrocytes using glial fibrillary acidic protein as a marker. In all of these species, nonphosphorylated neurofilament protein-immunoreactive neurons predominated in layer V. These neurons exhibited diverse morphologies with regional variation. Specifically, high proportions of atypical neurofilament-enriched neuron classes were observed, including extraverted neurons, inverted pyramidal neurons, fusiform neurons, and other multipolar types. In addition, many projection neurons in layers II–III were found to contain calbindin. Among interneurons, parvalbumin- and calbindin-expressing cells were generally denser compared to calretinin-immunoreactive cells. We traced the evolution of certain cortical architectural traits using phylogenetic analysis. Based on our reconstruction of character evolution, we found that the living xenarthrans and afrotherians show many similarities to the stem eutherian mammal, whereas other eutherian lineages display a greater number of derived traits.
44 citations
Cites background from "Inverted pyramidal neurons in chimp..."
...ously been described in many other mammalian species, such as rodents, lagomorphs, primates, carnivores, and cetaceans (Garey et al. 1985; Glezer and Morgane 1990; Mendizabal-Zubiaga et al. 2007; Qi et al. 1999)....
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...Spiny and aspiny inverted pyramidal neurons have also previously been described in many other mammalian species, such as rodents, lagomorphs, primates, carnivores, and cetaceans (Garey et al. 1985; Glezer and Morgane 1990; Mendizabal-Zubiaga et al. 2007; Qi et al. 1999)....
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...5% of profiles represented inverted pyramidal neurons among rats, rabbits, chimpanzees, and cats (Bueno-Lopez et al. 1991; Mendizabal-Zubiaga et al. 2007; Parnavelas et al. 1977; Qi et al. 1999)....
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...Depending on the region and species, 1–8.5% of profiles represented inverted pyramidal neurons among rats, rabbits, chimpanzees, and cats (Bueno-Lopez et al. 1991; Mendizabal-Zubiaga et al. 2007; Parnavelas et al. 1977; Qi et al. 1999)....
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TL;DR: The findings indicate that there is substantial regional differentiation in the expanded frontal cortex of this monotreme, and an updated nomenclature for cortical areas that more accurately reflects findings from functional and chemoarchitectural studies is presented.
Abstract: We have examined the topography of the cerebral cortex of the Australian echidna (Tachyglossus aculeatus), using Nissl and myelin staining, immunoreactivity for parvalbumin, calbindin, and nonphosphorylated neurofilament protein (SMI-32 antibody), and histochemistry for acetylcholinesterase (AChE) and NADPH diaphorase. Myelinated fibers terminating in layer IV of the cortex were abundant in the primary sensory cortical areas (areas S1, R, and PV of somatosensory cortex; primary visual cortex) as well as the frontal cortex. Parvalbumin immunoreactivity was particularly intense in the neuropil and somata of somatosensory regions (S1, R, and PV areas) but was poor in motor cortex. Immunoreactivity with the SMI-32 antibody was largely confined to a single sublayer of layer V pyramidal neurons in discrete subregions of the somatosensory, visual, and auditory cortices, as well as a large field in the frontal cortex (Fr1). Surprisingly, SMI-32 neurons were absent from the motor cortex. In AChE preparations, S1, R, V1, and A regions displayed intense reactivity in supragranular layers. Our findings indicate that there is substantial regional differentiation in the expanded frontal cortex of this monotreme. Although we agree with many of the boundaries identified by previous authors in this unusual mammal (Abbie [1940] J. Comp. Neurol. 72:429–467), we present an updated nomenclature for cortical areas that more accurately reflects findings from functional and chemoarchitectural studies. J. Comp. Neurol. 475:493–517, 2004. © 2004 Wiley-Liss, Inc.
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TL;DR: Results show that all neurons in the primate visual system have been generated, reached their final positions and formed their basic connections subserving ocular dominance before birth, i.e. before visual experience.
Abstract: Autoradiographic evidence from juvenile rhesus monkeys that had been exposed to a pulse of [3H]thymidine at different embryonic (E) and early postnatal (P) days indicates that all neurons which compose the visual system of this primate have been generated two months before birth. The first retinal ganglion cells (RGC) are generated around E30 preceding by a few days the onset of genesis of neurones destined for the dorsal lateral geniculate body (LGd) and superior colliculus (SC) both of which begin at E36. Production of neurons destined for the primary visual cortex (area 17) begins at approximately E43 and ends by E102. Neurons destined for layer IV, the major target of axons from the LGd, are generated between E70 and E85. The prenatal development of visual connections was studied by the autoradiographic method of anterograde axoplasmic transport in foetuses killed 14 days after unilateral eye injection of a mixture of [3H]proline and [3H]fucose. Initially, in the LGd and in the SC projections from both eyes overlap. Segregation of the axons and/or terminals from the two eyes occurs in the LGd and SC during the middle period of gestation. Transneuronal transport of tritium shows that although LGd axons form the optic radiation before E78, these fibres do not yet enter the developing cortical plate at this foetal age. During the second half of gestation, geniculocortical axons carrying input from each eye invade the cortex but are not yet segregated into ocular dominance columns. Rather, grains are distributed uniformly over the entire layer IV at E124. Three weeks before birth, at E144, segregation of afferents into sublayers IVA and IVC is apparent, and the first hint of ocular dominance columns is displayed by slight differences in grain counts in alternating areas of layer IV. These results show that all neurons in the primate visual system have been generated, reached their final positions and formed their basic connections subserving ocular dominance before birth, i.e. before visual experience. In the SC and LGD, monocular segregation is well established during the middle period of gestation, whereas in the cortex it has begun, but is not fully developed at birth.
719 citations
TL;DR: The cellular specificity of SMI‐32 immunoreactivity suggests that a subpopulation of neurons can be distinguished on the basis of differences in the molecular characteristics of basic cytoskeletal elements such as neurofilament proteins.
Abstract: A monoclonal antibody that recognizes a nonphosphorylated epitope on the 168 kDa and 200 kDa subunits of neurofilament proteins has been used in an immunohistochemical study of cynomolgus monkey (Macaca fascicularis) and human neocortex. This antibody, SMI-32, primarily labels the cell body and dendrites of a subset of pyramidal neurons in both species. A greater proportion of neocortical pyramidal neurons were SMI-32 immunoreactive (ir) in the human than in the monkey. SMI-32-ir neurons exhibited consistent differences in the intensity of their immunoreactivity that correlated with cell size. The cellular specificity of SMI-32 immunoreactivity suggests that a subpopulation of neurons can be distinguished on the basis of differences in the molecular characteristics of basic cytoskeletal elements such as neurofilament proteins. The size, density, and laminar distribution of SMI-32-ir neurons differed substantially across neocortical areas within each species and between species. Differences across cortical areas were particularly striking in the monkey. For example, the anterior parainsular cortex had a substantial population of large SMI-32-ir neurons in layer V and a near absence of any immunoreactive neurons in the supragranular layers. This contrasted with the cortical area located more laterally on the superior temporal gyrus, where layers III and V contained substantial populations of large SMI-32-ir neurons. Both areas differed significantly from the posterior inferior temporal gyrus, which was distinguished by a bimodal distribution of large SMI-32-ir neurons in layer III. Differences across human areas were less obvious because of the increase in the number of SMI-32-ir neurons. Perhaps the most notable differences across human areas resulted from shifts in the density of the larger SMI-32-ir neurons in deep layer III. A comparison between the species revealed that isocortical areas exhibited greater differences in their representation of SMI-32-ir neurons than primary sensory or transitional cortical areas. A comparison of distribution patterns of SMI-32-ir neurons across monkey cortical areas and data available on the laminar organization of cortical efferent neurons suggests that a common anatomic characteristic of this chemically identified subpopulation of neurons is that they have a distant axonal projection. Such correlations of cell biological characteristics with specific elements of cortical circuitry will further our understanding of the molecular and cellular properties that are critically linked to a given neuron's role in cortical structure and function.
369 citations
"Inverted pyramidal neurons in chimp..." refers background in this paper
...A monoclonal antibody to neurofilament protein, SMI32, labels the cells body and dendrites of a large subset of pyramidal cells in a Golgi-like manner (Campbell and Morrison, 1989, Hof et al., 1995a; 1995b; 1996; Nimchinsky et al., 1996; Preuss et al., 1997)....
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...In any case, the labeling favors large pyramidal neurons, especially those that have long projections (Campbell and Morrison, 1989)....
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...Presumably, the latter cells are unstained because they express little neurofilament protein, or express neurofilament proteins that lack the epitope recognized by SMI-32 monoclonal antibody (see Campbell and Morrison, 1989)....
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TL;DR: It is possible that neurofilament protein is crucial for the unique capacity of certain subsets of neurons to perform the highly precise mapping functions of the monkey visual system.
Abstract: Visual function in monkeys is subserved at the cortical level by a large number of areas defined by their specific physiological properties and connectivity patterns. For most of these cortical fields, a precise index of their degree of anatomical specialization has not yet been defined, although many regional patterns have been described using Nissl or myelin stains. In the present study, an attempt has been made to elucidate the regional characteristics, and to varying degrees boundaries, of several visual cortical areas in the macaque monkey using an antibody to neurofilament protein (SMI32). This antibody labels a subset of pyramidal neurons with highly specific regional and laminar distribution patterns in the cerebral cortex. Based on the staining patterns and regional quantitative analysis, as many as 28 cortical fields were reliably identified. Each field had a homogeneous distribution of labeled neurons, except area V1, where increases in layer IVB cell and in Meynert cell counts paralleled the increase in the degree of eccentricity in the visual field representation. Within the occipitotemporal pathway, areas V3 and V4 and fields in the inferior temporal cortex were characterized by a distinct population of neurofilament-rich neurons in layers II-IIIa, whereas areas located in the parietal cortex and part of the occipitoparietal pathway had a consistent population of large labeled neurons in layer Va. The mediotemporal areas MT and MST displayed a distinct population of densely labeled neurons in layer VI. Quantitative analysis of the laminar distribution of the labeled neurons demonstrated that the visual cortical areas could be grouped in four hierarchical levels based on the ratio of neuron counts between infragranular and supragranular layers, with the first (areas V1, V2, V3, and V3A) and third (temporal and parietal regions) levels characterized by low ratios and the second (areas MT, MST, and V4) and fourth (frontal regions) levels characterized by high to very high ratios. Such density trends may correspond to differential representation of corticocortically (and corticosubcortically) projecting neurons at several functional steps in the integration of the visual stimuli. In this context, it is possible that neurofilament protein is crucial for the unique capacity of certain subsets of neurons to perform the highly precise mapping functions of the monkey visual system.
263 citations
TL;DR: This is a survey of the distribution, form, and proportion of neurons immunoreactive for gamma‐aminobutyric acid (GABA) or glutamic acid decarboxylase (GAD) in cat primary auditory cortex (AI).
Abstract: This is a survey of the distribution, form, and proportion of neurons immunoreactive for gamma-aminobutyric acid (GABA) or glutamic acid decarboxylase (GAD) in cat primary auditory cortex (AI). The cells were studied in adult animals and were classified with respect to their somatic size, shape, and laminar location, and with regard to the origins and branching pattern of their dendrites. These attributes were used to relate each of the GAD-positive neuronal types to their counterparts in Golgi preparations. Each layer had a particular set of GABAergic cell types that is unique to it. There were 10 different GABAergic cell types in AI. Some were specific to one layer, such as the horizontal cells in layer I or the extraverted multipolar cells in layer II, while other types, such as the small and medium-sized multipolar cells, were found in every layer. The number and proportion of GABAergic cells were determined by using postembedding immunocytochemistry. The proportion of GABAergic neurons was 24.6%. This was slightly higher than the values reported elsewhere in the neocortex. The laminar differences in density and proportion of GABAergic and non-GABAergic neurons were also comparable (though somewhat higher) to those found in other cortical areas: thus, 94% of layer I cells were GABAergic, while the values in other layers ranged from 27% (layer V) to 16% (layer VI). Layer VI had the most heterogeneous population of GABAergic neurons. The proportion of these cells across different regions within AI was studied. Since some receptive field properties such as sharpness of tuning and aurality are distributed non-uniformly across AI, these might be reflected by regional differences across the cerebral cortex. There were significantly more GABAergic somata in layers III and IV in the central part of AI, along the dorsoventral axis, where physiological studies report that the neurons are tuned most sharply (Schreiner and Mendelson [1990] J. Neurophysiol. 64:1442-1459). Thus, there may be a structural basis for certain aspects of local inhibitory neuronal organization.
153 citations
"Inverted pyramidal neurons in chimp..." refers background in this paper
...One type of unusual pyramidal neuron, the Martinotti cell, with atypically oriented apical dendrites and vertically ascending axons (T Èomb Èol, 1984; Ferrer et al., 1986), may well be a specialized type of neuron (Prieto et al., 1994)....
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...…of the atypically oriented types (Van der Loos, 1965), and that they are more frequent in deeper layers (Van Brederode and Snyder, 1992; Ferrer et al., 1986a,b, 1987; Einstein and Fitzpatrick, 1991) and in abnormal cortex (Williams et al., 1975; Landrieu and Goffinet, 1981; Prieto et al., 1994)....
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TL;DR: The data indicate that neurons with extra‐cortically projecting axons (long axons) invariably possess spine‐rich dendrites forming domains with remarkably regular horizontal parameters (i.e. modular domains), and cells with axons limited to intra-cortical paths are characterized by spine‐poor or spine‐free dendrite forming domains which are highly variable in size and shape.
Abstract: Previous attempts at classification of cortical neurons have been based on a number of anatomical characteristics, some of doubtful physiological significance. In seeking a functionally more relevant scheme, we have based our classification on three neural attributes; (a) size and shape of the dendritic domain, (b) presence or absence of dendritic spines, and (c) intra or extra-cortical trajectory of the axon, as revealed in Golgi stained material. Our data indicate that neurons with extra-cortically projecting axons (long axons) invariably possess spine-rich dendrites forming domains with remarkably regular horizontal parameters (i.e. modular domains). Cells with axons limited to intra-cortical paths (short axons) are characterized by spine-poor or spine-free dendrites forming domains which are highly variable in size and shape. These two categories appear dependant on structural characteristics related both to input and output functions of cortical neurons, and are called Class I and II, respectively. The significance of synaptic arrangements along horizontal and vertical components of Class I dendritic modules are compared with those for Class II cells, and possible relationships between dendritic structure and temporo-spatial activity patterns are considered.
152 citations
"Inverted pyramidal neurons in chimp..." refers background in this paper
...…to estimate the proportion of atypically oriented pyramidal neurons, and yet his estimate of 18% in rabbit visual cortex (based on 33 atypical out of 183 pyramidal cells) is higher than subsequent estimates of 5% in rabbits (Globus and Scheibel, 1967) and 1% in rats (Parnavelas et al., 1977)....
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...…and atypically oriented pyramidal cells are present in the cortices of mice, rats, dogs, cats, monkeys, and humans (e.g., Van der Loos, 1965; Globus and Scheibel, 1967; Williams et al., 1975; Parnavelas et al., 1977; Ferrer et al., 1986; Miller, 1988), that inverted pyramids are one of the…...
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