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The spinal cord integrates and relays somatosensory input, leading to complex motor responses. Research over the past couple of decades has identified transcription factor networks that function during development to define and instruct the generation of diverse neuronal populations within the spinal cord.

A number of studies have now started to connect these developmentally defined populations with their roles in somatosensory bos. Here, we review our current understanding of how neuronal diversity in the dorsal spinal cord is generated and we discuss the logic underlying bosse these neurons form the basis of somatosensory circuits.

These senses are largely relayed and processed in the bosw spinal cord. Primary sensory neuronal axons from the periphery enter the dorsal spinal cord through the dorsal root where they synapse on projection neurons, local circuit interneurons, or even directly onto motor neurons, providing the first level of circuit integration and processing for somatosensory information.

Broadly, the circuitry is spatially organized with nociceptive and thermosensitive afferents targeting the psdcc dorsal laminae, cutaneous afferents targeting more ventral dorsal laminae, and proprioceptive afferents targeting cells more ventrally in the intermediate and ventral spinal cord Fig. Spinal cord neurons use excitatory or inhibitory neurotransmitters, combined with multiple neuropeptides, to transmit and modulate these signals.

How the diversity of neurons in the dorsal spinal cord configure somatosensory circuits and how these neurons function to integrate and relay somatosensory information is beginning to be uncovered. Development of the spinal cord.

During development, an invagination of the neural plate closes to form the neural psdd, which will become the central nervous system. The most caudal parts of the neural tube will become the spinal cord. Rexed laminae I-X in the adult spinal cord are determined by cytoarchitectonic parameters. Commonly used anatomical names for Rexed laminae regions are described: Clarke’s column, or the dorsal osdc of Clarke CCresides in the medial aspect of lamina VII mainly in the thoracic spinal cord.

The spinal cord is generated from the developing vertebrate neural tube Fig. Rostral parts of the neural tube develop into the brain while caudal parts become the spinal cord. These studies have shown that cells within bosd caudal neural tube differentiate into diverse populations of neurons Alaynick et al. Although bosee cell types extend along the rostral-caudal axis, as demonstrated for motor neurons that reside in different columnar motor pools, dorsal-ventral patterning is a major determinant of cell identity in the developing spinal cord.

Indeed, cross sections through the neural tube demonstrate the existence of discrete domains of combinatorial transcription factor TF bode that define particular cell types Fig.

Summary of the transcription factors that set up spinal cord neuronal diversity. The key transcription factors TFs that coordinate neuronal diversity in the developing spinal cord are shown, highlighting those that are expressed in the various progenitor domains dP1-dP6, p0-p3 and pMN in the proliferating ventricular zone of the developing spinal cord and those that define mature neuronal populations dI, V and MN and their subsets in the differentiating mantle zone.

TFs containing a homeodomain are indicated in blue text. Msx1Msx2 Timmer ppsdc al. Several dynamic processes have been shown to influence the number ;sdc type of neurons that form during the early stages of spinal cord neurogenesis and neuronal specification.

i These processes include interplay between signaling pathways gose TF function, regulation of the timing of neurogenesis, mechanisms of cross-repression between TFs and the expression of TF-driven gene programs that are specific to neuronal identity.

While these developmental mechanisms that generate specific cell types in the caudal neural tube are still under investigation, an open question is: With the advent of genetic techniques in mice to trace the lineage of various progenitor populations into adulthood, the field is now beginning to understand how neurons born in different progenitor domains give rise to the spinal interneurons that contribute to different aspects of somatosensation.

The caudal neural tube is thus emerging as an important model system with which to understand not only how progenitor domains are established during development, but also if there is some logic tying the development of a neuron to its function. In this review, we first provide an overview of the molecular mechanisms that specify cell fate and generate neuronal diversity in the developing spinal cord.

We then explore how different developmental populations produce subsets of neurons with particular somatosensory functions.

We do not cover ventral spinal cord development and diversity as this topic has been reviewed elsewhere Alaynick et al. As the caudal neural tube develops into the spinal cord, cells within progenitor domains in the ventricular zone Fig. Examinations of the combinatorial expression of multiple families of TFs, largely homeodomain HD and basic helix-loop-helix bHLH factors, have led to the description of 11 early-born [embryonic day E E Six of these dorsal interneuronsdI are found in the dorsal neural tube, and the remaining five V0-V3 and MN are found in the ventral neural tube Fig.

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These defined populations can be further divided into subtypes using criteria such as axonal projections, resulting location in the spinal cord ik neuropeptide expression. For example, the dI1 population can be split into two populations that are distinguished by their spatial location and axonal projections: These 13 main bse designations are central to understanding how TF expression is patterned in response to morphogens and how TFs psdcc neuronal identity.

Importantly, most of the TFs that mark these populations are required within the lineages where they are expressed. Although the TFs that define spinal cord neuronal populations are often depicted in a single static figure as in Fig. Thus, just because a TF bbose as a lineage marker at iu stage does not mean that it serves that function throughout the development of the lineage. HD factors are, therefore, particularly bode as markers for defining neuronal populations in the dorsal spinal cord Fig.

While transcription factors have been shown to define discrete domains during spinal cord development, the molecular markers that define a particular Rexed lamina are less bise, in part because particular laminae may have different sensory afferent terminations with several different neuronal cell types. Nonetheless, recent studies have been bkse to molecularly refine subpopulations within a given laminae.

These molecular designations are summarized in the above image. Expression patterns were determined psfc antibody staining capitalized protein symbolmRNA detection italicized gene symbol or genetically modified mice green boxes.

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TRPM8 Bautista et al. Dynamic expression of transcription factors in the developing spinal cord. The expression of transcription factors TFs in the developing neural tube padc highly dynamic. Eventually, sustained expression of ASCL1 leads to neuronal differentiation. Multiple signaling pathways are active in the developing neural tube prior to the emergence of the TF-based patterning discussed bise.

As the role of morphogens and their signaling pathways have been recently reviewed Briscoe and Small, ; Gouti et al. Cross-repression between TFs in the developing neural tube.

Furthermore, cross-repressive activities between individual TFs, both direct and indirect, play an important role in setting up boundaries between interneuron domains. During patterning of the dorsal-ventral axis of the spinal cord, SHH produced at the floor plate is instrumental for the formation of ventral cell type identities and it acts by activating or repressing the expression of TFs largely HD TFs in a concentration-dependent manner Briscoe et al.

Thus, the gradient of SHH from the floor plate sets up the initial pattern of TF expression that is later refined through cross-regulatory mechanisms between TFs Ericson et al. These signals are produced largely in the roof plate, involve multiple family members and regulate proliferation as well as specification of the progenitors Chesnutt et al.

Alterations to BMP levels, for example through mutations or ablation of the roof plate, demonstrate that specification of the dorsal dI1-dI3 termed class A populations are dependent on these signals, whereas the more intermediate dI4-dI6 class B populations form independent of BMP signaling Fig. The transcriptional output from these signals results in different combinations of HD-containing homeobox HOX TFs being expressed in progenitors and postmitotic neurons. For example, Hox4-Hox8 are expressed at the cervical and brachial levels, while Hox8-Hox9 are expressed in thoracic regions and HoxHox13 in lumbar regions.

The combinations of HOX genes induced have also been shown to pattern motor columns in the ventral spinal cord, such that motor neurons at limb levels are different from those at intercostal or abdominal levels. The mechanisms that regulate rostral-caudal identity in the dorsal spinal cord projection neurons and interneurons are less well understood, although HOX genes are likely players there as well. Although the signaling molecules mentioned above are the primary ones influencing the patterning of neurons generated along the dorsal-ventral and rostral-caudal axes, they are not the only players.

Notably, the responsiveness of progenitors to these patterning signals changes over time, probably as a result of the TFs themselves altering components in the signaling pathways to enhance or attenuate the signals Nishi et al.

What are the mechanisms that signal progenitor cells to exit the cell cycle and begin the process of neurogenesis? Together, these factors are key for influencing the number of neurons generated.

In general, a high level of Notch signaling maintains cell proliferation, whereas high proneural bHLH levels drive differentiation of that cell. There are many complexities in the Notch pathway, including extensive post-translational modifications, localization of components in the endoplasmic reticulum ER versus the cell surface and crucial protease cleavage steps see review by Kopan and Ilagan,but the core of the canonical signaling pathway is as follows.

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NICD forms a transcriptional activator complex that, among other things, activates transcription of the HES1 transcriptional repressor. Because high levels of the proneural bHLH factors drive neuronal differentiation, repression of these factors biases cells to the progenitor stage.

Thus, one might expect that some proneural bHLH activity in surrounding cells is needed to keep Notch signaling active in the progenitor cell. A model emerges whereby low levels of proneural bHLH activity are in a balance with active Notch signaling to maintain progenitor cells Castro et al.

When an imbalance allows elevated levels of proneural bHLH expression, the progenitor differentiates. Because of feedback regulation of HES1, cross-regulatory relationships as stated above and instability of the factors involved, the levels of the TFs and Notch ligands oscillate. Indeed, an emerging model is the oscillation model for maintaining progenitors Kageyama et al.

In this model, progenitors are maintained in a proliferative state. When expression of the neural bHLH factors is elevated and sustained, the progenitors undergo cell cycle exit and neuronal differentiation. For details on this Notch signaling oscillation-based model and a description of the live cell imaging experiments that support the model, see recent reviews by Imayoshi et al.

Repressing inappropriate gene expression programs in a lineage is just as crucial to specifying appropriate cell fate as inducing the proper cell type-specific genes. Indeed, cross-repression between TFs has emerged as a major principle in setting up boundaries that delineate either progenitor domains or their resulting neurons Fig.

This concept was first described in the ventral neural tube where neighboring progenitors repressed each others’ expression of class I or class II HD TFs to generate discrete progenitor boundaries Briscoe et al. In the dorsal neural tube, cross-repression is also evident and has been shown to occur between bHLH factors. How can these bHLH factors, which are activators of transcription, repress fate in neighboring cells?

Furthermore, PRDM13 may function through switching ASCL1 from an activator of Tlx3 expression to a repressor as a means to shut down gene programs for alternative fates within a differentiating neuron. As another example, PRDM12 was shown to be a factor that supports the V1 lineage by repressing V0 genes in the progenitors of these neurons Thelie et al. Until recently, the cross-repressive mechanisms elucidated in the developing neural tube have been limited to gene programs in neighboring progenitor populations.

However, unbiased approaches for identifying specific targets of TFs, such as RNA-seq coupled with ChIP-seq, are beginning to uncover broader programs of repression than previously appreciated.

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This emphasizes the concept that there is broad transcriptional activation throughout the neural tube, possibly involving SOXB1 factors Bylund et al. Additionally, these repressor networks target multiple SHH signaling components, providing negative feedback to ongoing SHH signaling, emphasizing the dynamic relationship between TFs and signaling pathways Nishi et al. Lastly, cross-repression between TFs is not just seen in setting up progenitor domain boundaries, but is also a mechanism used in early postmitotic populations.

Thus, TLX3 provides a switch that specifies the excitatory neuronal phenotype while repressing inhibitory neuronal programs in these postmitotic populations Cheng et al. Extrinsic signaling can also influence the levels of these TFs.

Thus, cross-repression between TFs that specify neuronal subtypes in progenitors and postmitotic neurons, which can be influenced by activity-dependent processes, is a key mechanism in generating neuronal diversity and ensuring definitive cell identities in the spinal cord. As mentioned above, bHLH and HD TFs have been used extensively to define and couple progenitor populations to their terminal neuronal populations, but less is known about the identity of the direct downstream targets of these TFs that could connect them to terminal differentiation processes such as axon guidance and neurotransmitter or neuropeptide fate Avraham et al.

In addition, hexameric complexes containing the HD factors ISL1 and LHX3 in the ventral neural tube have been shown to directly regulate a battery of cholinergic pathway genes, such as those encoding acetylcholine synthesizing enzymes and transporters in developing motor neurons Cho et al. Thus, terminal neuronal phenotypes can be directly regulated by sustained expression of HD factors in mature neurons. Given the transient nature of expression of the bHLH regulators, as opposed to the more sustained expression of some HD TFs, it is possible that bHLH TFs act to set up chromatin accessibility for later persistently expressed TFs that maintain the expression of cell type-specific genes Borromeo et al.

In summary, the past two decades of research have yielded multiple fundamental principles that guide the development of neuronal diversity in the neural tube.

The use of TFs as markers to define progenitor and neuronal populations has been essential for uncovering strategies that direct neuronal diversity in the developing neural tube.