Differentially expressed genes among motor and prefrontal areas of macaque neocortex

doi:10.1016/j.bbrc.2007.08.039

Biochemical and Biophysical Research Communications

Volume 362, Issue 3, 26 October 2007, Pages 665-669

https://doi.org/10.1016/j.bbrc.2007.08.039 Get rights and content

Abstract

In higher primates, the motor-related areas of the neocortex are highly differentiated into several subareas based on both functional and cytoarchitectural aspects. To assess the molecular basis of this areal specialization, we investigated the gene expression profiles of the primary motor area (M1), premotor area (dorsal and ventral, PMd and PMv, respectively), and prefrontal area (A46) in rhesus monkeys using DNA microarray. We discovered that 476 genes were differentially expressed among these 4 areas. More than half of these genes were most abundantly expressed in M1, and most genes were complementarily expressed between M1 and A46. The expression profiles of PMd and PMv were quite similar to each other and different from those of M1 and A46. The data will provide a fundamental basis for the further analysis of the structure–function relationship of the primate brain.

Section snippets

Materials and methods

The experimental protocols were approved by the Committee of Animal Experimentation by National Institutes of Natural Sciences.

Animal and tissue preparations. Brain tissue was obtained from 3 adolescent rhesus monkeys (Macaca mulatta) aged between 2.6 and 2.7 years that had been bred in group cages without being subjected to any experimental treatment. Adequate measures were taken to minimize pain and discomfort, in accordance with the National Institute of Health Guide for the Care and Use of

Results and discussion

In order to identify differentially expressed genes among M1, PMd, PMv, and A46, we performed genome-wide screening using DNA microarrays with 24 brain tissues obtained from the 4 areas of the right and left hemispheres of 3 monkeys. We obtained 583 probe sets with which 476 differentially expressed genes were identified after eliminating redundant annotations among the probe sets, and the expression patterns of those genes were classified into 29 expression patterns by a multiple comparison

Acknowledgments

We thank the staffs of Amami Wild Animal Research Centre Inc. and M. Iwatate (RIKEN GSC) for their technical assistance. This study was supported by the Core Research for Evolutionary Science and Technology (CREST) of the Japan Science and Technology Agency (JST).

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Transgenic mouse models of ALS have helped to establish a causal relationship between the expression of specific genes and ALS (Collard et al., 1995; Kaur et al., 2016; Kiaei et al., 2004; Kostic et al., 1997). The present study suggests the importance of nonhuman primate studies in developing therapeutic intervention strategies for ALS because the corticospinal motor system, which contains particularly vulnerable neurons in ALS (Brown and Robberecht, 2001; Ravits et al., 2007; Sobue et al., 1987), is highly developed in certain primate species (Courtine et al., 2007) and specific gene expressions may have a role in the functional and structural specialization of the primate corticospinal motor system (Kojima et al., 2013; Sato et al., 2007). We note that the present results for ALS are preliminary because we do not provide direct evidence of the causality between SPP1 reduction and ALS.
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However, more systematic analysis of gene expression is necessary to obtain a whole picture of gene expression changes. In this regard, we have recently revealed the gene expression of the M1, premotor, and prefrontal cortices in macaque monkeys using gene chip analysis (Sato et al., 2007). Such a comprehensive analysis of changes in the gene expression pattern in these cortical areas might accelerate research in this direction.
This is a review of our investigations into the neuronal mechanisms of functional recovery after spinal cord injury (SCI) in a non-human primate model. In primates, the lateral corticospinal tract (l-CST) makes monosynaptic connections with spinal motoneurons. The existence of direct cortico-motoneuronal (CM) connections has been thought to be the basis of dexterous digit movements, such as precision gripping. However, recent studies have shown that after lesion of the direct CM connections, by a l-CST lesion at the C4/C5 level, precision gripping is initially impaired, but shows remarkable recovery with training within several weeks. Plastic changes of the neural circuits underlying the recovery occur at various levels of the central nervous system. In the subcortical networks, intracellular recordings from the motoneurons in anesthetized animals demonstrated that transmission through the disynaptic pathways from the CST was enhanced, presumably mediated by the propriospinal neurons in the mid-cervical segments. The γ-band musculo-muscular coherence (MMC), with a peak frequency around 30 Hz, appeared over a wide range of forelimb muscles and was strengthened in parallel to the recovery of the precision grip. Appearance of the γ-band MMC also paralleled the change in the activation pattern of forelimb muscles; muscles which were antagonists before the lesion showed co-activation after recovery. Such γ-band MMC is thought to originate in the subcortical network, presumably in the brainstem or spinal cord. In the cortical networks, a combination of positron emission tomography and reversible inactivation techniques has shown that the bilateral primary motor cortex (M1) and ventral premotor cortex (PMv) have different contributions to functional recovery depending on the recovery stage; the bilateral M1 plays a major role in early stage recovery (< 1 month), whereas the contralateral M1 and bilateral PMv are the prominent contributors to the later stages (3–4 months). Such changes in cortical activity in M1 and PMv have been shown to accompany changes in the expressions of plasticity-related genes, such as GAP-43. Changes in the dynamic properties of neural circuits, both at the cortical and subcortical levels, are time-dependent. Multidisciplinary studies to clarify how the changes in the dynamic properties of individual components of the large-scaled networks are coordinated during recovery will help to develop effective therapeutic strategies to recovery from SCI.
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The expression patterns of the genes within the first group are similar to each other, and within-group similarities are also noticeable in the second group, particularly between RBP and PNMA5. On the other hand, the third group contains genes abundant in the motor area (Watakabe et al., 2001; Sato et al., 2007; Higo et al., 2010). The first gene that we identified as a primary-visual-cortex-selective gene was OCC1.
The neocortex, which is characteristic of mammals, has evolved to play important roles in cognitive and perceptual functions. The localization of different functions in different regions of the neocortex was well established within the last century. Studies on the formation of the neocortex have advanced at the molecular level, thus clarifying the mechanisms that control neural or glial cell differentiation and sensory projections. However, mechanisms that underlie cortical area specialization remain unsolved. To address this problem, our approach has been to isolate and characterize the genes that are selectively expressed in particular subsets of neocortical areas in primates; these areas are most distinctive among mammals. By differential display and restriction landmark cDNA scanning (RLCS) methods, we have identified two major classes of genes that are specifically expressed in the adult macaque monkey neocortical areas: one is expressed in the primary sensory areas, particularly, in the primary visual cortex (V1) and the other is expressed in the association areas. The genes that show these specific expression patterns are limited to only several gene families among our large-scale screening. In this review, I first describe the isolation and characterization of these genes, along with another class of genes specifically expressed in motor areas. Then, I discuss their functional significance in the primate neocortex. Finally, I discuss the implication of these gene expression patterns in neocortical specialization in primates and possible future research directions.
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Genes selectively expressed in the visual cortex of the old world monkey
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Differentially expressed genes among motor and prefrontal areas of macaque neocortex

Abstract

Section snippets

Materials and methods

Results and discussion

Acknowledgments

Physiol. Behav.

Neuron

Curr. Opin. Neurobiol.

Curr. Opin. Neurobiol.

Neurosci. Res.

Mol. Cell. Neurosci.

Behav. Brain Res.

Sequential organization of multiple movements: involvement of cortical motor areas

Annu. Rev. Neurosci.

Corticospinal Function and Voluntary Movement

Vergleichende Lokalisationslehre der Grosshirnrinde

The neocortex of Macaca mulatta