[NOTE: The following is an unpublished summary about nervous
system design and function in the blackworm, Lumbriculus variegatus
(Class Oligochaeta). This worm is being used at high
school and college levels for student laboratory exercises and research
projects. It has proven quite useful and reliable for studies of segment
regeneration, circulatory physiology, locomotion, eco-toxicology, and
neurobiology (Drewes, 1996a; Lesiuk and Drewes, 1998;
Drewes and Cain, 1998). The following article provides students and instructors
with general information about this worm’s nervous system which is not
currently available in any biology texts. Correspondence or questions about
this information are welcome. Please address to: Charles Drewes, EEOB Dept,
Room 339 Science II Building, Iowa State University, Ames, IA, 50011; or phone:
(515) 294-8061; or email: cdrewes@iastate.edu ]. Web: http://www.eeob.iastate.edu/faculty/DrewesC/htdocs
-------------------------------------------------------------------------------------------------------------
Functional
organization of the nervous system
in Lumbriculus variegatus
C. Drewes (April. 2002)
The gross anatomy of the nervous system in Lumbriculus variegatus was originally described more than 70 years
ago by Isossimow (1926), with an English summary of
that work given in Stephenson’s book, The
Oligochaeta (1930). Virtually no published
studies of this worm’s neurophysiology or behavior were done until the late
1980s. The central nervous system in Lumbriculus consists
of a cerebral ganglion (or ‘brain’), located in segment #1, and a
ventral nerve cord that extends through every body segment (Figure
1). In each segment, except the first
two, the ventral nerve cord gives rise to four pairs of segmental nerves.
[Comparative note: In the earthworm, Lumbricus terrestris, there are three pairs of
segmental nerve in each segment.] The
segmental nerves extend laterally into the body wall where they form a series
of parallel rings that extend within and around the body wall (for review, see
Stephenson, 1930). Some fibers in these nerves are sensory in function and
detect stimulation of the body surface. Other fibers are motor in function and
innervate circular muscle, longitudinal muscle, or chaetal
muscles in the body wall.
Fig. 1. Dorsal view of the central nervous system in the anterior end of Lumbriculus variegatus.
Abbreviations: PN, prostomial nerves; CG, cerebral
ganglion; n1-n4, segmental nerves 1-4; VNC, ventral nerve cord.
Clusters of neurons are
found in the ventral nerve cord of each segment. Some of these are sensory
neurons, others are motor neurons, and many are interneurons.
Some of the fibers arising from motor and sensory neurons extend into segmental
nerves, while other fibers from these neurons extend into a central region of
the ventral nerve cord, termed the neuropile. The
neuropile is a region where many synaptic connections
are made between all types of neurons. Some of these connections involve
neurons within the same segment, and others involve connections between neurons
in neighboring segments. These pathways and connections are formed in an
orderly fashion, thus providing an anatomical basis for the neuronal
circuits and reflex pathways that control the worm’s coordinated
movements and behavior.
A cross-section through the
ventral nerve cord reveals three exceptionally large diameter nerve fibers in
the dorsal part of the cord (Figure 2). These are the worm's so-called giant
nerve fibers that are seen in the ventral nerve cord of nearly all oligochaetes; these fibers have a key role in the worm’s
rapid escape responses (Drewes, 1984; Zoran and
Drewes, 1987; Drewes and Fourtner, 1990; Drewes and
Fig. 2. Cross-sectional
view of Lumbriculus
ventral nerve (dorsal portion of posterior ventral nerve cord). MGF, medial giant fiber; LGF lateral giant fiber. Note the
small-diameter fibers in the neuropil region below
the giant nerve fibers. Also note the heavy myelin-like sheath surrounding the giants fibers.
Brinkhurst, 1990). Each of the three giant fibers is derived from an
aligned, tandem sequence of enlarged axons that arise from segmentally
arranged interneurons (Fig. 3). Electrical synapses
interconnect these axons, thus allowing uninterrupted impulse conduction along
the entire fiber. The giant nerve fibers in Lumbriculus are tightly wrapped
by glial cell membranes, except at points where small
branches emerge ventrally from the fibers (see anterior left LGF in Fig. 2). This
glial wrapping gives the same appearance and probably
serves the same function (increased conduction velocity) as the myelin sheath
in vertebrate nerve fibers. In Lumbriculus, as in other oligochaetes,
the giant fiber branches that emerge ventrally and interrupt the glial wrapping appear to have a dual function: they may act
as functional “nodes” in initiating action potentials and they may receive
synaptic connections from other neurons (Zoran et
al., 1988; Drewes, 1997).
The giant nerve fibers form two functionally different pathways, as shown in Figure 3. The medial giant fiber (or MGF) is excited by touch sensory stimuli to anterior segments. Once excited, the MGF conducts impulses along the ventral nerve cord and excites segmental motor neurons which, in turn, excite longitudinal muscle, resulting in rapid shortening and withdrawal of anterior segments. In contrast, the two lateral giant fibers (or LGFs) are excited by touch stimuli to posterior segments. The LGFs are excited together and conduct impulses as a single unit along the ventral nerve cord. LGF impulses also excite motor neurons and longitudinal muscle, thus leading to rapid shortening of posterior segments. In addition to touch sensory stimulation, the LGFs are also be excited by a shadow stimulus when the worm’s tail is projected to the water surface. Photoreceptors in the worm’s tail detect the shadow. This triggers LGF impulses and rapid shortening of the tail (Drewes and Fourtner, 1989).
The giant fibers in Lumbriculus offer a rare technical opportunity for neurophysiological study. All-or-none action potentials
from the MGF or LGF can be detected non-invasively in freely moving worms, thus
eliminating the need for anesthesia, dissection, and restraint. MGF and LGF
conduction velocities increase in relation to increased fiber diameter. Diameter,
in turn, varies in relation to location along the worm’s body, age, and stage
of segment regeneration (Zoran and Drewes, 1987;
Drewes and Brinkhurst, 1990; Drewes and Fourtner, 1990). Conduction velocity may also be
momentarily increased to “super-normal” values as a result of previous impulse
conduction (Turnbull and Drewes, 1996). Giant fiber excitability and conduction
velocity may be decreased by exposure to a wide variety of environmental
toxicants (Rogge and Drewes, 1993; Drewes, 1997).
Although there have been numerous studies of giant
fiber-mediated rapid escape behavior in Lumbriculus, there have been no physiological studies of the
neural control of other movements or locomotor
behaviors that are also important to this animal. For example, the neuronal
circuits that control this worm’s swimming and crawling behaviors have not been
studied. Since swimming and crawling are rhythmic and patterned movements
(Drewes and Cain, 1998), we would expect and assume that each of these
behaviors is controlled by some type of central pattern generator in the
worm’s ventral nerve cord. The term “central pattern generator” (abbreviated
CPG) refers to any network of neurons that generates patterned, and usually
rhythmic outputs of neuronal activity which, in turn, control a particular
behavior. Examples in invertebrates include the CPG’s
for rhythmic feeding in snails, swimming in leeches, as well as walking,
running and flying in many arthropods. In Lumbriculus, CPG’s probably control forward and
rearward peristaltic crawling movements which are produced by coordinated waves
of circular and longitudinal muscle contraction. The helical swimming movements
in Lumbriculus
(Drewes, 1996b) are probably also under the control of a different CPG. The
biomechanics and timing of helical swimming movements are indirect reflections
of the outputs of the CPG for swimming. The timing and mechanics of swimming
movements in various ages of Lumbriculus have been recently described (Drewes, 1998).
Fig. 3. Generalized diagrams of escape reflex organization
in Lumbriculus.
Note the segmentally arranged cell bodies (CB) of the
medial (M) and lateral (L) giant nerve fibers.
References
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Drewes, C.D. (1996a) Heads or tails? Patterns
of segmental regeneration in a freshwater oligochaete.
In: Tested Studies for Laboratory Teaching, Volume 17, J.C. Glase, ed., Association for Biology Laboratory Education
(ABLE).
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C.D. (1996b) Those wonderful worms.
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