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Advances in Anatomy, Embryology and Cell Biology

Ennio Pannese

Biology and
Pathology of
Perineuronal
Satellite Cells in
Sensory Ganglia
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226
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Ennio Pannese

Biology and Pathology

of Perineuronal Satellite
Cells in Sensory Ganglia
Ennio Pannese
University of Milan
Milan
Italy

ISSN 0301-5556     ISSN 2192-7065 (electronic)

Advances in Anatomy, Embryology and Cell Biology
ISBN 978-3-319-60139-7    ISBN 978-3-319-60140-3 (eBook)
https://doi.org/10.1007/978-3-319-60140-3

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To Marisa and Lucia
Acknowledgments

The author thanks Prof. F. Scaravilli (Department of Neuropathology, UCL, London,

UK) and Prof. L. Zerboni (Department of Pediatrics/Infectious Diseases, Stanford
University, Stanford, California, USA) who kindly provided micrographs, Mrs. A.
Cerri for her advice during the making of the book, Mr. D. Ward for his help with
the English, and Mr. G. Macor (Studio Macor, Milano) who digitalized the figures.

vii
Contents

 iology and Pathology of Perineuronal Satellite

B
Cells in Sensory Ganglia������������������������������������������������������������������������������������   1
1.1 Historical Note������������������������������������������������������������������������������������   1
1.2 Organization of the Perineuronal Sheath in Adult Vertebrates ����������   2
1.3 Shape of Satellite Cells ����������������������������������������������������������������������   8
1.4 Structure of Satellite Cells������������������������������������������������������������������ 11
1.5 Molecular Characteristics of Satellite Cells���������������������������������������� 19
1.6 Relationships Between Satellite Cells������������������������������������������������ 25
1.7 Perikaryal Myelin Sheaths������������������������������������������������������������������ 26
1.8 Neuron-Satellite Cell Boundary���������������������������������������������������������� 28
1.9 Boundary Between the Satellite Cell Sheath and the Interstitial
Connective Tissue ������������������������������������������������������������������������������ 33
1.10 Quantitative Relationships Between Nerve and Satellite Cells���������� 35
1.11 Origin and Development of Satellite Cells ���������������������������������������� 36
1.12 Physiological Properties of Satellite Cells������������������������������������������ 43
1.13 Mitotic Activity of Satellite Cells ������������������������������������������������������ 44
1.14 Phagocytic Activity of Satellite Cells ������������������������������������������������ 45
1.15 Age-Related Changes�������������������������������������������������������������������������� 45
1.16 Roles of Satellite Cells Under Physiological Conditions ������������������ 48
1.16.1 Control of Traffic to Neurons������������������������������������������������� 48
1.16.2 Homeostasis of the Perineuronal Microenvironment�������������� 49
1.16.3 Neuroprotection���������������������������������������������������������������������� 50
1.16.4 Influence on Neuronal Morphology���������������������������������������� 50
1.17 Communication Between Neurons and Satellite Cells ���������������������� 50

ix
x Contents

1.18 Reaction of Satellite Cells to Experimental Conditions �������������������� 51

1.18.1 In Vitro Cultures���������������������������������������������������������������������� 51
1.18.2 Chemical Agents �������������������������������������������������������������������� 52
1.18.3 Radiation �������������������������������������������������������������������������������� 54
1.18.4 Axon Injury���������������������������������������������������������������������������� 54
1.18.5 Other Experimental Conditions���������������������������������������������� 57
1.19 Reaction of Satellite Cells to Pathological Conditions ���������������������� 57
1.19.1 Viral Infections����������������������������������������������������������������������� 57
1.19.2 Hereditary Neuropathies �������������������������������������������������������� 58
1.19.3 Degenerative Disorders���������������������������������������������������������� 59
1.20 Role of Satellite Cells in Neuropathic Pain���������������������������������������� 60

References ���������������������������������������������������������������������������������������������������������� 65
Abbreviations

CNS Central nervous system

E face (of the plasma membrane) Inner face of the outer (=External) leaflet of
the split plasma membrane
kD Kilodalton
mV Millivolt
MΩ Megohm
nm Nanometer
P face (of the plasma membrane) Outer face of the inner (=Protoplasmic)
­leaflet of the split plasma membrane
PNS Peripheral nervous system
RNA Ribonucleic acid
μm Micrometer

xi
Biology and Pathology of Perineuronal
Satellite Cells in Sensory Ganglia

1.1 Historical Note

A cell sheath enveloping the body of the neurons in sensory ganglia was mentioned
for the first time in 1836 by Valentin, a pupil of Purkinje. In some illustrations of his
paper, the nuclei of cells adjacent to the surface of the nerve cell body, both in the
trigeminal ganglion and in the ganglia of the autonomic nervous system, were clearly
shown (Fig. 1.1a) even though they were misinterpreted as pigment granules. Since
Remak (1838) denied the existence of this perineuronal sheath, Valentin (1839) pro-
vided a more detailed description of it, illustrated with new drawings (Fig. 1.1b), the
captions of which gave a correct interpretation of the satellite cell nuclei.
Small perineuronal cells (or perineuronal nuclei) were then described in both
sensory and autonomic ganglia by many authors under a variety of names such as
Polarkerne (Courvoisier 1868), Mantelzellen and Amphicyten (Lenhossék 1897),
intrakapsuläre Zellen (Holmgren 1901, 1902), Randzellen and Scheidenzellen
(Kohn 1907), Satellitenkörperchen (Ramón y Cajal 1907) or corpuscules ou cel-
lules satellites (Ramón y Cajal 1909), Trophozyten (Nemiloff 1908), gliocitos (De
Castro 1921, 1946), Hüllzellen, Hüllplasmodium and Nebenzellenplasmodium
(Stöhr jr. 1928), subcapsular cells (Penfield 1932), Scheidenplasmodium (Riegele
1932), capsular cells (Quade 1939), ganglionar neuroglia (Río Hortega et al. 1942),
capsule cells (Kuntz and Sulkin 1947), and periphere Glia (Herzog 1954).
Eventually, the term satellite cells became widely accepted. Since the term satellite
cell is also used to refer to progenitor cells of skeletal muscle fibers, the satellite
cells of sensory and autonomic ganglia are now often called satellite glial cells.
However, oligodendrocytes and less frequently astrocytes may be found applied to
the surface of nerve cell bodies in the CNS, so that the term satellite glial cells may
refer to these oligodendrocytes and astrocytes. Therefore, to avoid confusion, the
site of these cells should always be specified (e.g., satellite [glial] cells in the tri-
geminal ganglion).

© Springer International Publishing AG, part of Springer Nature 2018 1

E. Pannese, Biology and Pathology of Perineuronal Satellite Cells in Sensory
Ganglia, Advances in Anatomy, Embryology and Cell Biology 226,
https://doi.org/10.1007/978-3-319-60140-3_1
2 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

a b

Fig. 1.1 Nerve cell bodies of sympathetic ganglia with the nuclei of satellite cells on the neuronal
surface. Redrawn from Valentin; (a) 1836; (b) 1839. In his 1836 paper (a), Valentin misinterpreted
these nuclei as pigment granules (Pigmentkörperchen), but in his 1839 paper (b) he gave a correct
interpretation of the same nuclei

1.2  rganization of the Perineuronal Sheath

O
in Adult Vertebrates

Suggestions that the perineuronal sheath might be absent in certain sensory ganglia
or around some sensory neurons had been advanced in the past (e.g., see Schultze
1871; Lenhossék 1907; Levi 1907; Truex 1939). In light microscope preparations,
some nerve cell bodies seem to be without a satellite cell envelope (Fig. 1.2).
However, all the sensory neurons studied under the electron microscope have been
shown to possess a satellite cell sheath. It was also debated whether the perineuronal
sheath had a syncytial structure or consisted of discrete cells (for more details, see
Pannese 1981). The advent of the electron microscope resolved this dispute show-
ing that the sheath is built of discrete cells (Wyburn 1958 and many later authors).
In the sensory ganglia of adult vertebrates, both the nerve cell body and the initial
segment of its axon are tightly enveloped by a satellite cell sheath, which is covered
by a basal lamina. The satellite cell sheath with its basal lamina is in turn completely
surrounded by the interstitial connective tissue of the ganglion (Fig. 1.3). Each
nerve cell body together with its satellite cell sheath forms therefore a discrete struc-
tural unit (Pannese 1981). Furthermore, because of their close functional relation-
ships (see Sects. 1.16 and 1.17), the body of the sensory ganglion neuron and its
associated satellite cells also form a functional unit. Usually, each nerve cell body is
completely isolated from every other; however, clusters of two or three nerve cell
1.2 Organization of the Perineuronal Sheath in Adult Vertebrates 3

Fig. 1.2 Nerve cell bodies with their satellite cells (rabbit spinal ganglion). The nuclei of the satel-
lite cells are evident, while their cytoplasm can be identified only in some places; consequently
some portions of the neuronal surface seem to be without a satellite cell covering. Arrows point to
axonal glomeruli. Note that there are numerous blood vessels; some are marked with v. Light
micrograph of an 1-μm plastic section stained with toluidine blue, ×540
4 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

Fig. 1.3 Unit consisting of a nerve cell body (N1) and its satellite cell (sc) sheath (rabbit spinal
ganglion). The satellite cell sheath belonging to this unit is sharply separated from those encircling
the adjacent nerve cell bodies (N) by the interstitial connective tissue (ct). The neuron-satellite cell
boundary is outlined in ink. Note that the chromatin is distributed differently in the nuclei of satel-
lite cells and in that of the neuron. v blood vessel. Transmission electron micrograph, ×4500

bodies enclosed within a common connective envelope have also been described
(Fraentzel 1867; Holmgren 1901; De Castro 1921; Nawzatzky 1933; Mannu 1935;
Hossack and Wyburn 1954; Wyburn 1958; McCracken and Dow 1973a; Pannese
1981). The percentage of nerve cell bodies arranged in clusters is highest in neo-
nates and decreases progressively with age (Pannese et al. 1993). In the sensory
ganglia of adult animals, the percentage of nerve cell bodies arranged in clusters
range from 9.4 in the lizard, 5.6 in the rat, to 4.3 in the rabbit (Pannese et al. 1991,
1993). Sometimes, the nerve cell bodies of a given cluster are in direct mutual con-
tact (Figs. 1.4 and 1.5); in other cases, they are separated from one another by a thin
satellite cell sheet (Pannese et al. 1991). Interestingly, chemical transmission occurs
1.2 Organization of the Perineuronal Sheath in Adult Vertebrates 5

Fig. 1.4 A cluster of two nerve cell bodies (N1 and N2) enclosed within a common connective (ct)
envelope (rat spinal ganglion). Between the two arrowheads, these nerve cell bodies are in direct
contact. SC satellite cells. Transmission electron micrograph, ×4250

between the nerve cell bodies of a cluster even when the bodies themselves are sepa-
rated by a thin satellite cell sheet (Rozanski et al. 2012, 2013).
The satellite cell sheath may show a variously complicated pattern of organization.
It may consist of one single layer of flattened cells or of several layers of cells which
6 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

Fig. 1.5 Portions of the neurons of Fig. 1.4 are shown here at greater magnification (rat spinal
ganglion). Perikaryal projections are absent from the neuronal surface in direct contact with the
other neuron (above), but are present on the neuronal surface covered by satellite cells (below).
Arrows point to projections which in this section appear in continuity with the neuronal perikaryon;
* indicates projections which in this section appear as isolated entities because they arise from the
neuronal perikaryon at other levels. Transmission electron micrograph, ×36,000
1.2 Organization of the Perineuronal Sheath in Adult Vertebrates 7

Fig. 1.6 Portion of a perineuronal sheath in which several layers of satellite cells overlap in a
complex fashion (rabbit spinal ganglion). Cisternae of the granular endoplasmic reticulum are
evident in the nucleated portion of a satellite cell; several vesicles can be seen as free in the satellite
cell cytoplasm. Arrows point to pinocytotic vesicles; * indicates a cross section of a projection
which arises from the neuronal perikaryon (N) at another level. bl basal lamina; sc satellite cell
nucleus. Note that the clefts intervening between the apposed plasma membranes of adjacent satel-
lite cells open into the light space under the basal lamina (double arrow) at one end and into the
interval between the neuron and the satellite cell sheath at the other (arrowhead). Transmission
electron micrograph, ×48,000

overlap in a complex fashion (Fig. 1.6). Both the arrangement of the satellite cells and
the thickness of the sheath may vary from area to area within a given sheath. In spinal
ganglia of Xenopus laevis, fowl, guinea pig, and rabbit, the sheath may vary in thick-
ness from 40–50 nm to 4–6 μm; in the gecko it may vary from about 30 nm to about
3 μm and in the lizard from about 30 nm to about 1.5 μm. The sheath can sometimes
be very thin, e.g., 18 nm in the eight cranial nerve ganglion of the goldfish (Rosenbluth
and Palay 1961). Thus the satellite cell sheath can sometimes be below the limit of
resolution of the light microscope. This explains why the sheath may have appeared
discontinuous to some optical microscopists (e.g., Holmgren 1901; Penta 1934).
8 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

Although in electron microscope preparations, the satellite cell sheath usually

appears as a continuous structure, gaps of various width may leave the surface of
the neuron directly exposed to the basal lamina. Such gaps were occasionally
observed in spinal ganglia of rat (Cervós-Navarro 1960; Andres 1961), bovine
(McCracken and Dow 1973a), fowl, guinea pig (Pannese, unpublished observa-
tions), as well as in the spiral ganglion of the cat (Adamo and Daigneault 1973). In
rabbit spinal ganglia, the gaps are from 0.06 to 0.75 μm in length (Pannese et al.
1996). The portions of the neuronal plasma membrane not covered by satellite cells
are undercoated by a layer of dense material (Pannese et al. 1996), which is usually
absent beneath the plasma membrane covered by satellite cells. These gaps are less
rare in autonomic than in sensory ganglia and are more numerous and extensive in
old age (see Sect. 1.15).

1.3 Shape of Satellite Cells

In the past, various opinions were expressed on the shape of satellite cells. (1) Satellite
cells had a laminar shape (Fig. 1.7) and lacked processes (Hannover 1840, 1844;
Fraentzel 1867; Key and Retzius 1873; Penta 1934; Palumbi 1944). (2) Satellite cells
bore variably long and branching processes (Holmgren 1901, 1902; Ortiz-Picón 1932,
1949, 1955; Bertrand and Guillain 1933; Della Pietra 1937; Río Hortega et al. 1942;
Scharenberg 1952; Stramignoni 1953; Herzog 1954; Fig. 1.8). Some of the satellite
cells associated with the initial segment of the axon appeared as narrow sheets wind-
ing spirally around the initial segment (called espirocitos by Río Hortega). (3) Satellite
cells lying close to the neuron bore processes while laminar cells forming an outer
sheet lacked processes (Ramón y Cajal and Oloriz 1897; Ramón y Cajal 1909). The
laminar cells were regarded by Ramón y Cajal (1909) as endothelial cells.

a b

Fig. 1.7 The satellite cells are shown as laminar elements with an irregular polygonal shape.
Redrawn and slightly modified from Fraentzel (1867). In (a) satellite cells are shown with their
nuclei; in (b) only the outline of the same cells is evident
1.3 Shape of Satellite Cells 9

Fig. 1.8 According to the results of Río Hortega et al. (1942), both the satellite cells associated with the
axon (a) and those associated with the nerve cell body (b) are shown as elements bearing processes

Experiments carried out on spinal ganglia using various fixatives have shown
that the long, branching processes of satellite cells described in the past are the
result of distortion of the cell shape (Fig. 1.9) due to the procedures used (Pannese
1960). As a rule, satellite cells are laminar and irregular in outline. Even after long-­
term in vitro culturing of sensory ganglia, satellite cells maintain shapes similar to
10 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

a b

c d

e f
1.4 Structure of Satellite Cells 11

those observed in vivo (Shimizu 1965; Bunge et al. 1967; Waxman et al. 1977). In
cultures of dissociated ganglia, these cells often appear aggregated in an epithelial-­
like pattern. By 1873 Key and Retzius had already suggested that satellite cell pro-
cesses could be artifactual formations due to shrinkage of the ganglionic neuron.
Even the cleft which is sometimes apparent between the nerve cell and the perineu-
ronal connective tissue in light microscope preparations (Fig. 1.9) is the result of an
artifactual shrinkage of the neuronal body, as suggested by several early authors
(e.g., Koneff 1887; Flemming 1895; Schaffer 1896; Lenhossék 1897; Buehler 1897;
Nemiloff 1908).
Satellite cells are endowed with projections (Fig. 1.20) that increase their surface
area. The projections may be fingerlike (from 50 to 100 nm in diameter) or may
have a lamellar shape (from 30 to 100 nm in thickness). They are numerous espe-
cially at the cell surface facing the sensory neuron. It is not known whether these
projections are stable or transient structures.

1.4 Structure of Satellite Cells

In general, the satellite cell has only one nucleus. Binucleate satellite cells have only
occasionally been observed (Kubota and Hioki 1943; Forssmann 1964). In several
species, the nucleated portion of the satellite cell is apposed to a flattened area of the
neuronal surface; in the cat, on the other hand, the nucleated portion of the satellite
cell indents the neuronal surface. The nucleus is often elliptical (Fig. 1.2), less fre-
quently round, kidney shaped, or nearly triangular in section; in the South African
toad, it often shows one or more deep indentations. Chromatin (Fig. 1.3) usually
occurs in centrally located clumps and in a peripheral band (Bunge et al. 1967;
Pineda et al. 1967), which is separated from the inner surface of the nuclear enve-
lope by a fibrous lamina. In the nuclei of neurons ensheathed by satellite cells, by
contrast, the chromatin is usually widely dispersed (Fig. 1.3).
Free polysomes and cisternae of the granular endoplasmic reticulum (Figs. 1.6
and 1.10) are common in the cytoplasm (Hess 1955; Wyburn 1958). These cisternae
may be arranged in stacks (Pannese 1960, 1964, 1969; Bunge et al. 1967)
[Fig. 1.11]. These stacks of cisternae with their associated ribosomes may corre-
spond to the basophilic granules seen in satellite cells under the light microscope by
Kubota and Hioki (1943) and Palumbi (1944). Subsurface cisternae (Fig. 1.12) may

Fig. 1.9 Shape of satellite cells in spinal ganglia fixed in Bouin’s fluid (a, c), formaldehyde (e),
and OsO4 (b, d, and f). (a, b, and d) horse; (c) ox; (e) rabbit; (f) guinea pig. Note that in the ganglia
fixed in Bouin’s fluid (a, c), a cleft is apparent around the nerve cell body (N) where satellite cells
(sc) bearing branching processes can be seen. In OsO4-fixed ganglia (b, d, and f), no cleft can be
seen around the nerve cell body (N), and the satellite cells (sc) lie in close contact with the latter
and appear as laminar elements. sp spiral processes of satellite cells coiled around axons. Phase
contrast micrographs, (a–d) ×1000; (e, f) ×1450
12 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

b
1.4 Structure of Satellite Cells 13

be observed closely applied to the plasma membrane adjacent to another satellite

cell and rarely to the plasma membrane facing the neuron (see also Sect. 1.8).
Confronting subsurface cisternae can rarely be seen in two adjacent satellite cells.
Tubules and cisternae of the agranular endoplasmic reticulum are less frequently
observed, except in frog autonomic ganglia, where they are abundant. The Golgi
apparatus usually lies near the nucleus. Under the electron microscope, each section
of this organelle appears built of a stack of three to six flattened and smooth-
surfaced cisternae with a cluster of associated vesicles (Fig. 1.10).
Mitochondria (Fig. 1.10) show the distinctive structural features well known
from the literature (e.g., see Pannese 2015). Mitochondrial cristae, in general, take

Fig. 1.11 Numerous cisternae of the granular endoplasmic reticulum arranged in a stack can be
seen in the satellite cell cytoplasm (rat spinal ganglion). The outer contour of the satellite cell
sheath facing the connective tissue (ct) is lined by a basal lamina (bl). Note that the cytoplasmic
process of a connective tissue cell (*) is devoid of a basal lamina. Open triangle indicates a projec-
tion of the neuronal perikaryon (N) which invaginates the inner contour of the satellite cell sheath.
Transmission electron micrograph, ×21,800

Fig. 1.10 Cytoplasmic organelles in satellite cells (rabbit spinal ganglion). Cisternae of the granu-
lar endoplasmic reticulum and mitochondria can be seen in (a); a centriole (c), an autophagic vacu-
ole (double arrow), and several sections of the Golgi apparatus can be seen in (b). Arrows point to
pinocytotic vesicles; open triangle indicates a neuronal projection which invaginates the inner
contour of the satellite cell sheath. ct connective tissue; N neuronal perikaryon; sc satellite cell
nucleus. Transmission electron micrograph, ×40,000
14 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

c
1.4 Structure of Satellite Cells 15

the form of thin folds and, less frequently, of slender tubules; both platelike and
tubular cristae may be found in the same mitochondrion. Cristae are usually ori-
ented transversely to the long axis of the mitochondrion; sometimes however they
are oriented longitudinally (Fig. 1.21). Cristae oriented transversely at one end of
the mitochondrion and longitudinally at the other end can also be observed. Small
dense granules may be found in the mitochondrial matrix. In rabbit spinal ganglia,
a small percentage of mitochondria contain, together with common cristae, atypical
cristae, resembling those described by Newcomb et al. (1968) in mitochondria of
plant cells. These cristae (Fig. 1.12), which always occur in elongated mitochon-
dria, have a major axis approximately coincident with that of the mitochondrion;
their membrane appears denser than that of the common cristae. Similar cristae have
also been described in neuroglial cells of the CNS of lizard under apparently normal
conditions (Gray 1960) and in other cell types under experimentally modified con-
ditions (e.g., Adoutte et al. 1972; Tuchweber et al. 1972). In rabbit spinal ganglia,
the mean percentage of cytoplasmic volume occupied by mitochondria is about
30% greater in nerve cell bodies than in their associated satellite cell sheaths
(Martinelli et al. 2006b, 2007). Elongated organelles with two paired enveloping
membranes and a filamentous content have been occasionally observed in satellite
cells of the frog spinal ganglia (Kohno 1969). These bodies, whose significance is
unclear, have been called gliosomes as they resemble organelles found in neuroglial
cells of the CNS (Held 1909; Fieandt 1910 and, more recently, Farquhar and
Hartmann 1957; Fleischhauer 1958; Gray 1959; Srebro 1965; Donelli et al. 1975)
and named gliosomen (gliosomes) by Fieandt (1910). These organelles should not
be confused with the glial plasmalemmal vesicles described by Nakamura et al.
(1993), which have also been termed gliosomes.
Lysosomes have been detected cytochemically in spinal ganglia of rat (Citkowitz
and Holtzman 1973) and chick embryo (Pannese et al., unpublished observations).
Autophagic vacuoles (Fig. 1.10) are sometimes present in satellite cells. Whether
they contain lytic enzymes and, therefore, are autolysosomes, has not yet been
determined. Peroxisomes have been detected cytochemically in spinal ganglia of rat
(Citkowitz and Holtzman 1973) and in the trigeminal ganglion of mouse (Hanker
et al. 1974). They appear as small (about 0.2 μm in diameter), membrane-bounded
bodies with a matrix of moderate electron density but no core or nucleoid.
Multivesicular bodies are also present (Pannese 1964, 1969; Bunge et al. 1967).
Microtubules (Bunge et al. 1967; Pannese 1969), 20–30 nm in diameter, and
intermediate filaments (Rosenbluth 1962a; Pannese 1964; Moses et al. 1965), about

Fig. 1.12 Cytoplasmic organelles in satellite cells (spinal ganglia of bullfrog (a), rabbit (b), and
lizard (c)). Arrows point to pinocytotic vesicles; crossed arrows point to subsurface cisternae; open
triangle indicates a neuronal projection which invaginates the inner contour of the satellite cell
sheath; white square encloses cross-sectioned microtubules; bl basal lamina; c centrioles, one of
which serves as the basal body of a cilium (ci); c1 a centriole in cross section; f cross-sectioned fila-
ments; g glycogen particles; m1 dumbbell-shaped mitochondrion; m2 elongated mitochondrion
with longitudinally oriented “atypical” cristae; N neuronal perikaryon; sc satellite cell nucleus.
Transmission electron micrographs. (a) ×64,200; (b) and inset ×42,800; (c) ×32,100; and inset
×64,200
16 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

10 nm in thickness, occur throughout the cytoplasm, generally lying more or less

parallel to both the outer and inner surfaces of the satellite sheath (Figs. 1.12 and
1.21). They are particularly numerous around the axon hillock and the initial seg-
ment of the axon.
Centrioles, observed by Kubota and Hioki (1943) under the light microscope,
usually lie near the nucleus and the Golgi complex (Figs. 1.10, 1.12 and 1.13).
Under the electron microscope, they appear as cylinders (0.3–0.5 μm in length
and 0.2 μm in diameter), whose wall (Fig. 1.12) is composed of the usual nine
triplets of microtubules (Pannese 1964, 1969; Bunge et al. 1967). Solitary primary
cilia (Figs. 1.12 and 1.13) have been occasionally observed in satellite cells (auto-
nomic ganglia: Grillo and Palay 1963; sensory ganglia: Pannese 1964). The cil-
ium originates from a basal body (Fig. 1.13), which sometimes bears coarse
appendages extending radially from its wall and, more rarely, a cross-striated
rootlet. The shaft of the cilium, 0.2–0.3 μm in diameter, projects into a narrow
channel of the extracellular space formed by a deep invagination of the plasma
membrane and may be directed toward the adjacent neuron or the connective tis-
sue space. These cilia lack the central pair of microtubules and only show the nine
pairs of peripheral microtubules, as do those in neurons, in Schwann cells, and in
astrocytes. The finding of specific receptors on the solitary cilia of certain neurons
(for a review, see Pazour and Witman 2003) supports the hypothesis that these
cilia are sensory organelles. The cilia of satellite cells may have a similar sensory
function; however, there appear to be no data on the presence of specific receptors
on the cilia of these cells.
Lipofuscin granules may occur in the satellite cells of sensory ganglia (Andres
1961; Pannese 1964; Glees and Gopinath 1973). They are more often present in the
perinuclear cytoplasm than elsewhere. These granules are bounded by a membrane
and have a dense matrix which contains homogeneous vacuoles of lower density.
Membranous arrays can sometimes be seen in the dense matrix. It has been sug-
gested that satellite cells actively cooperate in the elimination of lipofuscin
­accumulated within spinal ganglion neurons. Lipofuscin granules would be trans-
ferred from the neuronal perikaryon to the cytoplasm of surrounding satellite cells
and then to the connective tissue and, finally, removed via the capillaries (Glees and
Gopinath 1973). However, observations in rat and rabbit spinal ganglia do not sup-
port this hypothesis (van den Bosch de Aguilar and Vanneste 1983; Ledda et al.
1999). Glycogen particles (25–30 nm in diameter) may occur singly or grouped in
small clusters (Fig. 1.12). Lipid inclusions (Fig. 1.14) have been found in satellite
cells (Kubota and Hioki 1943; Andres 1961; Rosenbluth 1962a; Cravioto and
Merker 1963; Arnold 1970). In mammals and birds, these inclusions are usually
scarce and do not exceed 1 μm in diameter; in amphibians, by contrast, at certain
periods of the year, they can be very numerous and so large (several micrometers in
1.4 Structure of Satellite Cells 17

Fig. 1.13 Mitochondria, dense bodies, cisternae of the granular endoplasmic reticulum (*),
and Golgi complexes (G) can be seen in the cytoplasm of a satellite cell. Microtubules and
intermediate filaments are interposed between the other organelles (rabbit spinal ganglion).
Arrow points to a pinocytotic vesicle along the satellite cell plasma membrane facing the
interstitial connective tissue (ct). Crossed arrow points to a subsurface cisterna. c centrioles,
one of which serves as the basal body of a cilium (ci); N neuronal perikaryon. Transmission
electron micrograph, ×28,000
18 Biology and Pathology of Perineuronal Satellite Cells in Sensory Ganglia

b c
1.5 Molecular Characteristics of Satellite Cells 19

Fig. 1.14 (a) Cytoplasmic lacuna (L) in a satellite cell (rabbit spinal ganglion). Some microvilli
and a cilium (ci) project into the lacunar space. Arrows point to pinocytotic vesicles, and the
crossed arrow points to a subsurface cisterna; bl basal lamina; N neuronal perikaryon; sc satellite
cell nucleus. (b, c) Lipid inclusions (li) in satellite cells (b fowl spinal ganglion; c Xenopus spinal
ganglion). Note the abundant, agranular endoplasmic reticulum in the satellite cell of Xenopus.
The crossed arrow points to a subsurface cisterna; N neuronal perikaryon; sc satellite cell.
Transmission electron micrographs, (a, b) ×39,500; (c) ×23,800

diameter) as to distort the outline of the nucleus and even that of the whole cell
(Rosenbluth 1962a; Arnold 1970).
In rabbit spinal ganglia, large lacunae (Fig. 1.14) have been occasionally observed
beneath the outer surface of the satellite cell sheath. A continuity between the lacu-
nar space and the perineuronal connective tissue space has not been traced so far.
The largest lacuna observed measured 12 × 6 μm in section. Sometimes the lacuna
appears partitioned by thin cytoplasmic septa devoid of organelles. Microvilli and
sometimes also the shaft of a cilium may project into the lacunar space (Fig. 1.14).
An electron transparent or a flocculent, moderately dense material fills the lacunar
space. The significance of these cytoplasmic lacunae is unclear. So far they have
been described only in the rabbit.
The plasma membrane of satellite cells, like that of neuroglial cells in the
CNS, appears thinner and less dense than that of neurons (Figs. 1.14, 1.18 and
1.20). Assemblies of orthogonally arranged particles have been found in the
freeze-­fractured plasma membrane of satellite cells (Fig. 1.15). The center-to-
center spacing of these particles is about 7 nm. Such assemblies have been found,
for example, in the satellite cell plasma membrane of the chick (Pannese et al.
1977) and rat (Gotow et al. 1985) but not the frog (Matsumoto and Rosenbluth
1986). Similar specializations also are found in astrocytes, ependymal cells of
higher vertebrates, and other cell types, whereas they have never been recog-
nized within the plasma membranes of oligodendrocytes or neurons. The number
per unit surface area of these assemblies is always lower in the plasma membrane
of satellite cells than in that of astrocytes. These assemblies are composed of
aquaporin-4 (Verbavatz et al. 1997; Rash et al. 1998). Aquaporins are channel-
forming membrane proteins that are involved in water transport across the plasma
membrane. Unlike aquaporin-4, other aquaporins do not usually form assemblies
of orthogonally arranged particles.

1.5 Molecular Characteristics of Satellite Cells

Knowledge in this field is still fragmentary. A number of molecules found in satel-

lite cells are listed in Table 1.1.
Under normal conditions, the perineuronal satellite cells of sensory ganglia
express low levels of glial fibrillary acidic protein (see Table 1.1 for references),
Another random document with
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 ¹ Or, before.

8. over all Israel] in 2 Samuel v. 17, over Israel. In both passages

the reference is to the later anointing by the whole people (2 Samuel
v. 3).

all the Philistines] David, as king of Judah, was of little or no

political importance to the Philistines; as king of united Israel, he
became a possible menace, and was accordingly attacked without
delay.

went up] i.e. from their own low-lying territory by the sea into the
hill-country of Judah.

went out against them] margin went out before them, i.e.
anticipated them, did not wait for them to attack him. In 2 Samuel v.
17 went down to the hold, an expression which might refer to some
part of the difficult hill-country of Judah in which he had long defied
Saul, or may mean the “hold” of Jerusalem, which David had seized
from the Jebusites (see note on xi. 5).

⁹Now the Philistines had come and made a

raid in the valley of Rephaim.
9. the valley of Rephaim] probably the shallow valley, now called
Beḳā‘a, across which runs the road from Jerusalem to Beth-lehem
(Bädeker, Palestine⁵, pp. 15, 99).

¹⁰And David inquired of God, saying, Shall I go

up against the Philistines? and wilt thou
deliver them into mine hand? And the Lord
said unto him, Go up; for I will deliver them
into thine hand.
 10. inquired of God] doubtless by means of the sacred lot, the
Urim and Thummim (see Hastings’ Dictionary of the Bible s.v., and
Kirkpatrick’s notes on 1 Samuel x. 22, xxiii. 6).

¹¹So they came up to Baal-perazim, and David

smote them there; and David said, God hath
broken ¹ mine enemies by mine hand, like the
breach of waters. Therefore they called the
name of that place Baal-perazim ².
¹ Or, broken forth upon mine enemies.

² That is, The place of breakings forth.

11. Baal-perazim] probably to be identified with the Mount

Perazim of Isaiah xxviii. 21, but the situation is unknown.

like the breach of waters] i.e. like the breach made by waters,
Probably the scene of the victory was a hill deeply scarred with
watercourses. The force with which God broke through the army of
the Philistines is compared with that of a torrent bursting forth from
the hill-side or forcing its way through all obstacles. Baal-perazim =
the Lord of breakings forth, i.e. upon the foe.

¹²And they left their gods there; and David

gave commandment, and they were burned
with fire.
12. David gave commandment, and they were burned] In 2
Samuel v. 21 (Revised Version) David and his men took them away.
The Chronicler alters this statement so as to make David’s conduct
agree with the Law (Deuteronomy vii. 5, 25) which enjoined that
graven images were to be burnt with fire.
 ¹³And the Philistines yet again made a raid in
the valley.
13. yet again] This invasion of “all the Philistines” (verse 8) was
too serious to be repelled by a single defeat.

in the valley] in 2 Samuel v. 22, in the valley of Rephaim, as in

verse 9 above.

¹⁴And David inquired again of God; and God

said unto him, Thou shalt not go up after
them: turn away from them, and come upon
them over against the mulberry ¹ trees.
¹ Or, balsam trees.

14. Thou shalt not go up after them] In 2 Samuel v. 23 the words

after them are connected with the following verb: Thou shalt not go
up: make a circuit behind them. In Samuel the command is to assail
the rear of the enemy, in Chronicles to avoid the rear (which was
perhaps protected by a rear-guard) and to attack (presumably) the
flank. The reading in Chronicles is to be preferred as a harder
reading, which yields good sense on examination.

from them] The Hebrew word suggests that David occupied a

commanding position from which he would be tempted to attack.

over against the mulberry trees] Render, along, parallel to. The
line of David’s attack is to be parallel to a line of mulberry trees (or to
a ridge on which mulberry trees stood) situate probably at right
angles to the line of the Philistine march. Thus David’s advance
would be concealed from the Philistines until the very moment of the
attack, which would fall on the flank of the Philistine march.
 mulberry trees] or, as margin, balsam trees. Some kind of tree or
shrub from which gum exudes seems to be meant.

¹⁵And it shall be, when thou hearest the sound

of marching in the tops of the mulberry trees,
that then thou shalt go out to battle: for God is
gone out before thee to smite the host of the
Philistines.
15. the sound of marching] the sound of the wind in the trees is to
be taken as an omen from Jehovah, indicating the favourable
moment for the assault. The Targum, characteristically, has the
sound of angels coming to thy help.

thou shalt go out to battle] Samuel has a more vivid phrase, thou
shalt bestir thyself.

¹⁶And David did as God commanded him: and

they smote the host of the Philistines from
Gibeon ¹ even to Gezer. ¹⁷And the fame of
David went out into all lands; and the Lord
brought the fear of him upon all nations.
¹ In 2 Samuel v. 25, Geba.

16. smote the host of the Philistines from Gibeon even to Gezer]
This victory was decisive; the main army of the Philistines was
routed.

Gezer] compare vi. 67, note.

 Chapter XV.
1‒24.
David’s Preparations for Bringing the Ark to Jerusalem.

There is no parallel in Samuel to this section.

In 2 Samuel vi. 12 the reason given for the renewal of David’s

attempt to bring the Ark to Jerusalem is the report of the blessing
which was said to have befallen Obed-edom, in whose house the
Ark had been left. The Chronicler is not ignorant of this tradition
since he refers to it incidentally in xiii. 14, but it would be very far
from his sense of the fitness of things to adduce it as the motive for
David’s action. On the contrary he declares in this section that David
was prompted by a realisation that the ill-success of the first attempt
was due to failure to observe the regulations of the Levitical Law. Full
attention now being given to the prescribed ritual, David succeeds in
his pious purpose.

¹And David made him houses in the city of

David; and he prepared a place for the ark of
God, and pitched for it a tent.
1. made him houses] Compare 2 Samuel v. 9.

a tent] a new tent, not the old tabernacle which the Chronicler
believed to be at Gibeon (see xvi. 39).

²Then David said, None ought to carry the ark

of God but the Levites: for them hath the Lord
chosen to carry the ark of God, and to minister
unto him for ever.
2. None ... but the Levites] Numbers i. 50, vii. 9. Nothing is said in
the parallel place (2 Samuel vi. 13) of the Levites, but bearers (and
not a cart) are spoken of with regard to this second attempt.
Compare 2 Chronicles v. 4, note.

³And David assembled all Israel at Jerusalem,

to bring up the ark of the Lord unto its place,
which he had prepared for it. ⁴And David
gathered together the sons of Aaron, and the
Levites:
3. assembled all Israel] It was a solemn religious assembly
(Hebrew Ḳāhāl, Greek ἐκκλησία).

⁵of the sons of Kohath; Uriel the chief, and his

brethren an hundred and twenty: ⁶of the sons
of Merari; Asaiah the chief, and his brethren
two hundred and twenty: ⁷of the sons of
Gershom; Joel the chief, and his brethren an
hundred and thirty: ⁸of the sons of Elizaphan;
Shemaiah the chief, and his brethren two
hundred: ⁹of the sons of Hebron; Eliel the
chief, and his brethren fourscore: ¹⁰of the sons
of Uzziel; Amminadab the chief, and his
brethren an hundred and twelve.
5‒10. Remark that besides the three great Levitical divisions,
Kohathites, Gershonites, and Merarites, three additional classes
(sons of Elizaphan, of Hebron, and of Uzziel) are given in verses 8‒
10. This unusual sixfold division, and the smallness of the numbers
of Levites have been taken as indicating that the whole passage xv.
1‒15 is drawn by the Chronicler from an earlier source, but the
argument is not convincing. “The text does not imply that Elizaphan,
Hebron, and Uzziel were coordinated with Kohath, Gershom, and
Merari”; and the small numbers are accounted for by the view that
only selected Levites were chosen for the task (so Curtis,
Chronicles, p. 127).

5. the sons of Kohath; Uriel] Kohath had four sons (Exodus vi. 18
= 1 Chronicles vi. 18): Amram, Izhar, Hebron, and Uzziel. Here the
descendants of Amram (exclusive of the priests, the Aaronites)
represented by Uriel head the list (verse 5), and the descendants of
Izhar, Hebron, and Uzziel appear in verses 8, 9, 10 respectively.
Elizaphan (verse 8) either stands for the Izhar of Exodus vi. 18, or is
the name of some prominent descendant of Izhar after whom the
whole family was named. He is mentioned again in 2 Chronicles
xxix. 13. As regards number the Kohathites were 512 against 350 of
the sons of Merari and the sons of Gershom combined. In vi. 60‒63
(45‒48, Hebrew) 23 cities are reckoned to Kohath against 25 to
Merari and Gershom combined. The Kohathites formed the largest
and most important of the three divisions of the Levites.

¹¹And David called for Zadok and Abiathar the

priests, and for the Levites, for Uriel, Asaiah,
and Joel, Shemaiah, and Eliel, and
Amminadab,
11. Zadok and Abiathar] This double priesthood (2 Samuel viii.
17, xv. 29, 35, xix. 11, xx. 25) came to an end in the reign of
Solomon (1 Kings ii. 27, 35). Zadok is always mentioned first as
being descended from Eleazar the third son of Aaron, while Ithamar
from whom Abiathar (Ahimelech) was descended through Eli (1
Kings ii. 27) was the fourth son (xxiv. 1, 3). In two of the passages
quoted in this note Abiathar (probably being confused with his father)
is called Ahimelech or Abimelech (2 Samuel viii. 17 = 1 Chronicles
xviii. 16; 1 Chronicles xxiv. 3). Conversely in Mark ii. 26 Ahimelech is
called Abiathar. In the Chronicler’s list of high-priests (vi. 4‒14)
Zadok alone is mentioned, the line of Eleazar alone being given.
 the priests] Only the two chief priests are mentioned here. Other
priests blew with the trumpets in front of the Ark (verse 24).

¹²and said unto them, Ye are the heads of the

fathers’ houses of the Levites: sanctify
yourselves, both ye and your brethren, that ye
may bring up the ark of the Lord, the God of
Israel, unto the place that I have prepared for
it.
12. sanctify yourselves] Compare 2 Chronicles xxix. 5. For the
method of sanctifying compare Exodus xix. 10, 15.

¹³For because ye bare it not at the first, the

Lord our God made a breach upon us, for
that we sought him not according to the
ordinance. ¹⁴So the priests and the Levites
sanctified themselves to bring up the ark of
the Lord, the God of Israel.
13. made a breach] xiii. 11, xiv. 11 (compare margin).

we sought him not] i.e. God; but a better rendering is we sought

not unto it. Compare note on xiii. 3.

according to the ordinance] For its observance, see verse 15.

¹⁵And the children of the Levites bare the ark

of God upon their shoulders with the staves
thereon, as Moses commanded according to
the word of the Lord.
 15. the children of the Levites bare ... upon their shoulders] in
accordance with the regulation of Numbers i. 50, vii. 9, which was
not observed in the first attempt when the Ark was placed in a cart,
xiii. 7.

the staves] Exodus xxv. 13, 14.

¹⁶And David spake to the chief of the Levites

to appoint their brethren the singers, with
instruments of music, psalteries and harps
and cymbals, sounding aloud and lifting up the
voice with joy.
16. psalteries] See note on xiii. 8.

¹⁷So the Levites appointed Heman the son of

Joel; and of his brethren, Asaph the son of
Berechiah; and of the sons of Merari their
brethren, Ethan the son of Kushaiah;
17. Heman the son of Joel] a descendant of Samuel the prophet;
vi. 33 (vi. 18, Hebrew). Compare Psalms lxxxviii. (title). As Heman
was descended from Kohath, Asaph from Gershom, and Ethan from
Merari, each division of the Levites was represented by a chief
musician. Heman was king’s seer (xxv. 5).

Asaph the son of Berechiah] a descendant of Gershom; vi. 39‒43

(24‒28, Hebrew). Asaph was the chief of the musicians; xvi. 5, 7.
One of the small collections of Psalms from which our Psalter was
compiled was named after him; compare the titles of Psalms l.,
lxxiii.‒lxxxiii.

Ethan the son of Kushaiah] a descendant of Merari; vi. 44‒47.

Compare Psalms lxxxix. (title). He is apparently called Jeduthun in
xxv. 1‒6. See also the note on xvi. 41.
 18‒24. These verses present several obscurities which can
hardly be explained except by the supposition that the original text of
the Chronicler has been added to by a later writer with intricate
results. Several reconstructions are possible, the most plausible
being that of Curtis which is followed in these notes.

¹⁸and with them their brethren of the second

degree, Zechariah, Ben, and Jaaziel, and
Shemiramoth, and Jehiel, and Unni, Eliab, and
Benaiah, and Maaseiah, and Mattithiah, and
Eliphelehu, and Mikneiah, and Obed-edom,
and Jeiel, the doorkeepers.
18. their brethren of the second degree] Read rather their twelve
brethren: twelve being the number of names from Zechariah to
Mikneiah. The last two, Obed-edom and Jeiel, were “doorkeepers,”
not “singers,” although they were mistakenly supposed to belong to
the list of singers by the author of verses 19‒21 (see further
regarding Obed-edom the note on xvi. 38).

Ben] This word, which means “son,” is an error. Read probably

Bani.

the doorkeepers] See the notes on ix. 17.

¹⁹So the singers, Heman, Asaph, and Ethan,

were appointed, with cymbals of brass to
sound aloud;
19‒21. Probably an addition interpolated by someone interested
in the detailed organisation of the Levitical choirs. The names are
taken from verse 18, except that Ben is omitted, and a new name
Azaziah is added at the end of the list. Since Obed-edom and Jeiel
are included among the singers here, the reading “of the second
degree” (which is regarded above as an error for an original “twelve”:
a slight change in Hebrew) must have been found in the text of verse
18 which the interpolator used.

to sound aloud] The cymbals mark the time for the other
instruments.

²⁰and Zechariah, and Aziel, and Shemiramoth,

and Jehiel, and Unni, and Eliab, and
Maaseiah, and Benaiah, with psalteries set to
Alamoth;
20. set to Alamoth] an obscure phrase, its musical significance
being uncertain; compare Psalms xlvi. (title), Revised Version.

²¹and Mattithiah, and Eliphelehu, and

Mikneiah, and Obed-edom, and Jeiel, and
Azaziah, with harps set to the Sheminith, to
lead.
21. set to the Sheminith] As in the case of Alamoth, the precise
musical significance of Sheminith is obscure. Compare Psalms vi.
(title, Revised Version margin).

²²And Chenaniah, chief of the Levites, was

over the song ¹: he instructed about the song ¹,
because he was skilful.
¹ Or, the carrying of the ark Hebrew the lifting up.

22. was over the song] The Hebrew word (massa) here twice
rendered “song” means “uplifting,” either of the voice in song, or in a
physical sense = “burden”; hence margin was over the carrying of
the ark.
 ²³And Berechiah and Elkanah were
doorkeepers for the ark.
23. were doorkeepers for the ark] The same statement is made in
verse 24 concerning Obed-edom and Jehiah (= Jeiel)! On Curtis’
view, this verse was added by the same writer as verses 19‒21,
who, having taken Obed-edom and Jeiel as part of the list of singers
in verse 18 no doubt thought that the names of the doorkeepers (the
last word of verse 18) had somehow been omitted. He supplied
therefore here the names Berechiah and Elkanah (taken perhaps
from ix. 16). A still later writer has attempted to put matters straight
by further adding at the conclusion of verse 24 “and Obed-edom and
Jehiah (Jeiel) were doorkeepers for the ark.”

²⁴And Shebaniah, and Joshaphat, and

Nethanel, and Amasai, and Zechariah, and
Benaiah, and Eliezer, the priests, did blow with
the trumpets before the ark of God: and Obed-
edom and Jehiah were doorkeepers for the
ark.
24. the priests] In Numbers x. 1‒10 it is enjoined to make two
silver trumpets to be blown by the priests on days of joy and on
feast-days. This festal trumpet was different from the “cornet” (verse
28), properly a ram’s horn, which was freely used for secular
purposes. See Driver, Amos, pp. 144 ff. (with illustrations).

25‒XVI. 3 (compare 2 Samuel vi. 12‒20).

The Bringing Home of the Ark. Michal despises David.

²⁵So David, and the elders of Israel, and the

captains over thousands, went to bring up the
ark of the covenant of the Lord out of the
house of Obed-edom with joy: ²⁶and it came to
 pass, when God helped the Levites that bare
the ark of the covenant of the Lord, that they
sacrificed seven bullocks and seven rams.
26. when God helped the Levites] In 2 Samuel vi. 13, when they
that bare the ark of the Lord had gone six paces. The Chronicler
interprets the safe start as a sign of Divine assistance.

seven bullocks and seven rams] In Samuel an ox and a fatling

(so Revised Version, not, oxen and fatlings as Authorized Version).
The smaller sacrifice of Samuel is represented as the king’s own
offering, the larger sacrifice of Chronicles as that of the king and his
elders combined.

²⁷And David was clothed with a robe of fine

linen, and all the Levites that bare the ark, and
the singers, and Chenaniah the master of the
song ¹ with the singers: and David had upon
him an ephod of linen.
¹ Or, the carrying of the ark Hebrew the lifting up.

27. of the song] margin, of the carrying of the ark. Compare verse
22, note.

an ephod of linen] worn exceptionally by David for the purpose of

the religious procession. A linen ephod was the ordinary vestment
for all priests (1 Samuel xxii. 18). The high-priest’s ephod was a
more elaborate garment (Exodus xxviii. 6‒12), fitted with the means
of divination (1 Samuel xxiii. 6, 9‒12).

²⁸Thus all Israel brought up the ark of the

covenant of the Lord with shouting, and with
 sound of the cornet, and with trumpets, and
with cymbals, sounding aloud with psalteries
and harps.
28. with shouting] The Hebrew word (tĕrū‘ah) is technical in the
sense of a blast with the festal trumpets (Numbers x. 1‒10), and in
this sense it should be taken here, since the Chronicler has
expanded the account given in Samuel by introducing a mention of
these trumpets.

²⁹And it came to pass, as the ark of the

covenant of the Lord came to the city of
David, that Michal the daughter of Saul looked
out at the window, and saw king David
dancing and playing; and she despised him in
her heart.
29. playing] a synonym of dancing, obsolete in modern English.
The closest rendering is perhaps, leaping as in sport. The
unrestrained joyousness of this action might easily degenerate (as in
idolatrous worship) into licence. The Chronicler omits to say that the
dancing was “before the Lord” (2 Samuel vi. 16). David’s subsequent
interview with Michal (2 Samuel vi. verses 20‒23) is also passed
over in Chronicles.
 Chapter XVI.
¹And they brought in the ark of God, and set it
in the midst of the tent that David had pitched
for it: and they offered burnt offerings and
peace offerings before God.
1. the tent] Compare xv. 1, note.

they offered] In 2 Samuel vi. 17, David offered. The Chronicler

associates the elders with David as in xv. 26.

burnt offerings] Compare Leviticus i. 1‒9.

peace offerings] The “peace offering” (Hebrew shelem) was a

thank-offering or an offering made in expiation of a vow; compare
Proverbs vii. 14.

²And when David had made an end of offering

the burnt offering and the peace offerings, he
blessed the people in the name of the Lord.
2. blessed the people] Compare 2 Chronicles vi. 3.

³And he dealt to every one of Israel, both man

and woman, to every one a loaf of bread, and
a portion of flesh ¹, and a cake of raisins.
¹ Or, of wine.
 3. a loaf of bread] A flat round cake such as is still made in Egypt
is meant.

a portion of flesh] margin “of wine.” The meaning of the Hebrew

word is unknown. Of flesh is rightly in italics here as in 2 Samuel vi.
19.

a cake of raisins] Compare Isaiah xvi. 7 (Revised Version) where

the same Hebrew word is used.

4‒6 (compare verses 37, 38).

David’s Arrangements for Ministration before the Ark.

⁴And he appointed certain of the Levites to

minister before the ark of the Lord, and to
celebrate and to thank and praise the Lord,
the God of Israel:
4. to celebrate] The literal meaning is to call to mind; compare
verse 12 (remember). Compare Psalms xxxviii., lxx. (titles).

⁵Asaph the chief, and second to him

Zechariah, Jeiel ¹, and Shemiramoth, and
Jehiel, and Mattithiah, and Eliab, and Benaiah,
and Obed-edom, and Jeiel, with psalteries and
with harps; and Asaph with cymbals, sounding
aloud;
¹ In chapter xv. 18, Jaaziel.

5. Asaph] Compare xv. 17, note.

and Obed-edom] It is possible that the names Obed-edom, and

Jeiel and Asaph (in the latter part of the verse) have been inserted
by the interpolator who wrote xv. 19‒21 and wished to accommodate
these verses to the altered text in chapter xv.

⁶and Benaiah and Jahaziel the priests with

trumpets continually, before the ark of the
covenant of God.
6. Benaiah and Jahaziel] Two priests for the two trumpets.

Benaiah] In xxvii. 5, 6 a Benaiah son of Jehoiada the priest

(Revised Version) is mentioned who may possibly be identified with
the Benaiah who was one of the thirty heroes (xi. 24, 25). Compare
also xii. 27.

7‒36.
The Psalm of Praise.

⁷Then on that day did David first ordain ¹ to

give thanks unto the Lord, by the hand of
Asaph and his brethren.
¹ Or, make it the chief work.

The psalm which follows consists of Psalms cv. 1‒15, Psalms

xcvi. 1b‒13a, Psalms cvi. 1, 47, 48. It has been compiled from the
Psalms just mentioned and placed here as an utterance such as
would be appropriate to the situation. For detailed criticism as to the
original form and present text of these Psalms, the reader must be
referred to the commentaries on the Psalter. Only such comment is
here given as seems called for in their present setting.

8‒22 (= Psalms cv. 1‒15).

⁸O give thanks unto the Lord, call upon his name;

Make known his doings among the peoples.
8, 9. These verses are perhaps based upon Isaiah xii. 4, 5.

⁹Sing unto him, sing praises unto him;

Talk ¹ ye of all his marvellous works.

¹⁰Glory ye in his holy name:

Let the heart of them rejoice that seek the Lord.

¹ Or, Meditate.

9. Talk ye] margin Meditate. Meditation leads to fresh

proclamation.

marvellous works] (compare verse 12). i.e. works beyond man’s

expectation; compare Genesis xviii. 14, Is anything too hard
(wonderful, Revised Version margin) for the Lord?

¹¹Seek ye the Lord and his strength;

Seek his face evermore.

11. and his strength] Perhaps (altering only the points of the
Hebrew word) and be ye strong. So LXX. καὶ ἰσχύσατε (in Psalms
cv. 4 καὶ κραταιώθητε). A promise is sometimes expressed in Hebrew
by the imperative.

¹²Remember his marvellous works that he hath done;

His wonders, and the judgements of his mouth;
12. His wonders] in particular, the marvels of the deliverance from
Egypt; Psalms cv. 27‒36.

¹³O ye seed of Israel his servant,

Ye children of Jacob, his chosen ones.

13. of Israel] Psalms cv. 6, of Abraham.

¹⁴He is the Lord our God:

His judgements are in all the earth.

14. His judgements are in all the earth] Compare verses 20‒22.

¹⁵Remember his covenant for ever,

The word which he commanded to a thousand

generations;

¹⁶The covenant which he made with Abraham,

And his oath unto Isaac;

¹⁷And confirmed the same unto Jacob for a statute,

To Israel for an everlasting covenant:

 15. Remember] Read (with Psalms cv. 8) He hath remembered.
Compare Exodus xxiv. 3‒8, xxxiv. 10‒27.

¹⁸Saying, Unto thee will I give the land of Canaan,

The lot ¹ of your inheritance:

¹ Hebrew cord, or, line.

18. The lot] The Hebrew word (“ḥebel”) means a portion not
assigned by lot but measured by line; compare margin Canaan is co-
extensive with Israel’s inheritance.

inheritance] All nations receive an inheritance from God;

Deuteronomy xxxii. 8.

¹⁹When ye were but a few men in number;

Yea, very few, and sojourners in it;

19. When ye were] Psalms cv. 12, When they were.

sojourners] The patriarchs were not simply strangers, but

strangers who made a long sojourn in Canaan.

²⁰And they went about from nation to nation,

And from one kingdom to another people.

20. kingdom ... people] The “kingdom” is Egypt (Genesis xii.); the
“people” the Canaanite and Perizzite (Genesis xiii.).

²¹He suffered no man to do them wrong;