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First published online January 19, 2006
Journal of Experimental Biology 209, 493-503 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02030
Functions of the subesophageal ganglion in the medicinal leech revealed by ablation of neuromeres in embryos
1 Division of Biological Sciences, Neurobiology Section, University of
California, San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0357,
USA
2 Department of Biological Sciences, California State University, San
Marcos, San Marcos, CA 92096, USA
* Author for correspondence (e-mail: kfrench{at}ucsd.edu)
Accepted 12 December 2005
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Key words: annelid, anterior brain, central nervous system, cephalic brain, Hirudo medicinalis, leech, subesophageal ganglion
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)
suggest that this pattern evolved early and persisted because it was so
successful. The more recent discovery that homologous molecules are expressed
in very similar patterns during the development of the nervous system in
Drosophila and in mice reinforces the notion that the fundamental
organization of the nervous system evolved early and was then conserved
(Kammermeier and Reichert,
2001; Reichert and Simeone,
2001), as does the homology in structure observed in many taxa
(Ghysen, 2003). Although the
term `brain' has proven to be somewhat difficult to define, one characteristic
that distinguishes a brain from a ganglion is that a brain typically serves
the entire organism, not simply a particular segment or body part
(Sarnat and Netsky, 2002), and
that it is organized into functionally separate regions
(Delcomyn, 1998).
In leeches, which are annelid worms, the central nervous system (CNS)
includes two brains, one at the anterior end of the ventral nerve cord and the
other at the posterior end. The anterior and posterior brains are compacted
collections of several segmental ganglionic equivalents of neurons
(Muller et al., 1981).
Although their nervous system is relatively simple (a large fraction of the
neurons in the CNS are located in ganglia strung along the ventral nerve cord,
with one ganglion in each of the 21 midbody segments), leeches display a wide
variety of behaviours including shortening, locomotion, probing, neuronally
controlled heartbeat and a variety of segmental behaviours; the neuronal basis
of many of these behaviours is well understood
(Kristan et al., 2005;
Mazzoni et al., 2005). This
richness of background information, coupled with the relative simplicity of
the annelid nervous system, makes leeches a particularly useful group in which
to explore the effects of centralization and cephalization in the nervous
system.
The anterior `head brain' of Hirudo medicinalis L. (the European
medicinal leech) is composed of a supraesophageal ganglion (SupraEG) and a
subesophageal ganglion (SubEG). This brain lacks large and well-defined
sensory projection areas, such as the olfactory antennal lobe or the complex
visual processing areas in the brains of insects
(Bullock and Horridge, 1965;
Burrows, 1996;
Gupta, 1987). Instead, the
SupraEG is undivided, and the SubEG consists of four regions called
neuromeres. The SupraEG, which arises from the anteriormost part of the embryo
called the prostomium (Stent et al.,
1992), contains a variety of peptidergic neurons
(Crisp et al., 2002), and its
function remains relatively unexplored. The SubEG arises embryonically from
four ganglion-like clusters of neurons at the anterior of the ventral nerve
cord (Stent et al., 1992), and
in adults this embryonic origin is reflected in the four bilaterally symmetric
neuromeres (Fig. 1A,B). In
adults, the cells of the SubEG are tightly compacted and the neuromere
boundaries are somewhat obscured, making well-defined ablations with clean
boundaries difficult to produce. To explore the function of the brain in
adults, previous workers entirely removed the SupraEG or the SubEG. Bullock
(Bullock and Horridge, 1965)
reported that removing the entire SupraEG caused increased activity,
heightened excitability and changes in the pattern of swimming. By contrast,
removing the SubEG depressed spontaneous activity, although the leeches could
still crawl and swim if prodded sufficiently.
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At the opposite end of the experimental spectrum, the function of the SubEG
has been explored one neuron at a time. Many neurons that are found in the
segmental ganglia [e.g. mechanosensory neurons
(Yau, 1976) and the
serotonergic neuromodulatory Retzius cells
(Lent, 1977)] are present in
the SubEG. In addition, previous work has revealed that many neurons with
distinctive functions are found only in the SubEG. For example, cell Tr1 can
initiate swimming (Brodfuehrer and Friesen,
1986; Kristan and Weeks,
1983), and cells SIN-1 and Tr2 can terminate or suppress swimming
(Brodfuehrer et al., 1995a;
Taylor et al., 2003). Cell
R3b1 participates in the choice of whether a leech will swim or crawl
(Esch et al., 2002). These
identified neurons occupy predictable positions and are distributed among the
neuromeres of the SubEG, rather than being clustered together. This pattern
suggests that the SubEG is not organized into circumscribed regions, each of
which controls a particular behaviour (e.g. swimming or locomotion), but
individual neuromeres might still have distinctive functions. Ablating defined
subregions of the brain has been widely used in studying the functional
anatomy of the vertebrate brain (Mogensen
et al., 2005), but the small and highly compacted brain of many
invertebrates, including the leech (Fig.
1A), makes clean ablation of subsections difficult. This problem
can be circumvented during leech embryogenesis, because in the middle of
development the precursors of the SubEG are separate from one another
(Fig. 1B) and can be ablated
independently.
To explore the function of the SubEG of Hirudo as a whole and to
ask if it includes functionally distinct regions, we ablated one or more
neuromeres about half-way through development, and when each leech completed
development we evaluated its behaviour. Some of our results have been
previously presented in abstract form
(French et al., 2004).
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Surgical manipulations
Surgery was performed on embryos at 48-50% of embryonic development (ED;
Reynolds et al., 1998b) in
ice-cold normal leech saline (in mmol l-1: 115 NaCl, 4 KCl, 1.8
CaCl2.2H2O, 1.5 MgCl2.6H2O, 10
glucose, 4.6 Tris-maleate, 5.4 Tris-base, pH 7.4,) containing 8% ethanol.
After surgery, leeches were transferred to ice-cold embryo water that was
allowed to warm up to room temperature.
In one type of surgery, all or part of the SubEG was removed using electrolytically sharpened tungsten pins and very fine scissors. We refer to these leeches as `ablated'. Removing posterior neuromeres effectively disconnects any remaining anterior neuromeres from the ventral nerve cord, so we usually started all ablations at the anterior of the SubEG.
All SubEG ablations also severed the sensory and motor connections between the CNS and peripheral structures in the head. To determine how the behaviours were modified by disconnecting the SubEG from the periphery, we performed the same tests on animals in which the SubEG was intact and still connected with the ventral nerve cord, but all nerves to the periphery in the head had been cut. We call this group of embryos `nerve cuts' or just `cut'. For sham-operated controls, we exposed the neuromere precursors and nerves in the head but did not cut any neuronal structures. Throughout the study, embryos were maintained individually in embryo water in 35 mm Petri dishes, and their water was changed every other day.
Behavioural observations
Many behaviours of Hirudo medicinalis have been well described in
adults (Kristan et al., 2005)
and in embryos (French et al.,
2005; Reynolds et al.,
1998a). In the present study, we observed and characterized
additional behaviours in juvenile leeches shortly after hatching
(Table 1 summarizes all of the
behaviours observed). After they reached 100% ED, leeches were observed in
their Petri dishes every other day for 6 days, for a total of three
observations per leech. Embryonic leeches heal rapidly and completely, so it
was typically impossible to tell from visual inspection which leeches had been
treated surgically, and after surgery all embryos were coded so the observer
was unaware of each embryo's surgical treatment.
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We observed both spontaneous and elicited behaviours. For `spontaneous behaviour' we watched each individual for a 6-min period after moving its Petri plate to the stage of a dissecting microscope and illuminating it with bright light. We recorded the time the leech spent in each behaviour and expressed the times as a percentage of the total time. For most groups of leeches we then observed `elicited behaviour' by gently prodding the leech with round-ended forceps on the dorsal surface at each of three locations: anterior (very close to the head), midbody (about half-way between the head and tail) and posterior (just anterior to the rear sucker). Leeches typically responded to this stimulation; the notation `no response' was rare. During each trial the animal was allowed to complete its response and return to baseline behaviour prior to the next stimulation, and a minimum of 20 s separated stimuli to minimize habituation or sensitization. Leeches were stimulated in each location three times during each observation period for a total of nine stimuli per session, and the order of stimulation was randomized. If a leech executed more than one behaviour successively in response to a single stimulus, all behaviours were recorded. (Most responses consisted of a single behaviour, and it was rare to observe more than two.)
We observed a total of 95 individuals from 10 cocoons (fertilized
Hirudo eggs develop encased in a cocoon secreted by the parent leech;
Fernandez and Stent, 1982).
The spontaneous behaviour of all leeches was recorded. The elicited locomotory
behaviour of most of the leeches was observed, but many leeches never moved
around spontaneously, so the total number of animals in which we observed
spontaneous locomotion was 84. In a subset of the embryos (41 embryos from
four cocoons), the full behavioural repertoire in response to touch at the
anterior, middle and posterior of the body was observed.
Evaluation of surgery
The extent of each ablation or cut was recorded immediately after surgery,
and it was confirmed in each individual by postmortem dissection
(Fig. 1C,D). Leeches were
transferred to ice-cold normal leech saline containing 16% ethanol, the SubEG
was exposed, and the animal was incubated for 1-3 h in 0.1% Neutral red
(Sigma, St Louis, MO, USA) dissolved in standard leech saline to label the
monoaminergic neurons (Stuart et al.,
1974). The number and position of labelled Retzius neuron somata
indicated the number of neuromeres remaining following ablation. The general
morphology of the SubEG and its associated nerves was noted. In some cases, a
solution of 0.2% methylene blue dye (Sigma) was applied and then washed off to
reduce ambiguity in the structure of the neuromeres and of the nerves
connecting the SubEG to the periphery.
Statistical analyses
All juvenile leeches executed a wide variety of behaviours, and to
determine whether surgery had produced changes in their behavioural
repertoires we used a direct ordination method called canonical correspondence
analysis (CCA) (Ter Braak,
1986). CCA is a multivariate technique that has been used in
zoology, botany and ecology but, to our knowledge, has not previously been
applied to neurobiological data. It generates a reduced number of synthetic
variables that summarize information about groups of several raw variables (in
this case, behaviours) that were measured in the observed `experimental units'
(in this case, individual animals). The synthetic variables (called CCA axes)
can then be used to evaluate patterns of responses across multiple raw
variables simultaneously.
CCA is designed for discrete - rather than continuous - variables and it constrains axes to correlate maximally with pre-assigned sets of independent variables, in this case the treatment group of the animal (i.e. control, nerve cut or neuromere ablation). The method imposed no particular ordering with respect to the experimental treatment.
Although CCA will detect linear responses, the data do not have to be linear. CCA is applicable to unimodal patterns in which the discrete variables (in this study, the behaviours) change in frequency from uncommon to common and then back to uncommon again in a non-linear fashion. For example, in our study, treatments that differed in severity could produce this pattern of change if unique behaviours were seen in leeches with moderately severe ablations, but not in control leeches or in leeches with very severe ablations. A CCA `individual score' is a numerical representation of the entire suite of behaviours that an individual exhibited (e.g. Fig. 2C); individuals with similar scores exhibited similar behavioural repertoires. These individual scores can be interpreted by comparing them with `behaviour scores' (e.g. Fig. 2B), which are calculated simultaneously with the individual scores. Just as leeches with similar individual scores displayed a similar suite of behaviours, constellations of behaviours with similar scores were typically performed by individual leeches. This property of the analytic method effectively emphasized the behaviours that were most different among the groups. Behavioural scores furthest from zero contributed most to distinctions among the groups. (The sign of the scores is arbitrary; if all signs were reversed, the conclusions would be the same.)
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).
Briefly, the test is based on randomly reshuffling the observed behaviours
without constraining them into experimental groups. The test statistic in this
method is a `pseudo-F', or the ratio of the constrained (by the surgical
treatments) to the unconstrained (ignoring surgical treatment) `inertia',
which is a multivariate measure of variance. Because this pseudo-F does not
follow the usual F-distribution, the behavioural data were repeatedly and
randomly reshuffled, and a new CCA was calculated each time (we used 999
repeats). A pseudo-F was calculated for each reshuffled CCA, and the pseudo-F
calculated for the data was compared with the entire distribution of
reshuffled pseudo-Fs. If the observed pseudo-F was larger than all of the 999
randomly reshuffled values, then the probability of obtaining such an
observation by chance is estimated to be 1/1000, or P
0.001.
Individual scores from significant CCAs were subjected to a one-way analysis
of variance (ANOVA), followed by a Student's t-test post-hoc
procedure, to assess for significance differences among treatment groups. CCA produces as many axes as there are raw behavioural variables, but preliminary analysis confirmed that the first CCA axis captured the major effects of surgical treatment or touch location. Thus, rather than presenting results by plotting CCA1 against CCA2, we have confined our presentation to CCA1 individual and behaviour scores for all analyses.
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Elicited behaviour: the effect of stimulus location
To determine how elicited behaviours varied with the touch location, we
touched each leech with moderate pressure (enough to indent the skin but not
enough to do damage) on the dorsal side of the body at the anterior, midbody
or posterior of the animal (Fig.
3A). Control leeches stimulated anteriorly most often shortened
(sh), i.e. they withdrew from the touch by contracting the entire
body longitudinally while keeping the tail sucker attached to the substrate. A
much less common response to anterior touch was to release the front sucker
(fsr). Although two other behaviours, detaching (det) and
freezing (freeze), were more common than fsr, CCA indicated
that sh and fsr together best distinguished the control
response to anterior touch from touches elsewhere on the body
(Fig. 3B,C). When control
leeches were touched in the midbody (Fig.
3A), their most common response was local bending (lb),
in which the body wall at the site of the touch contracts while the body wall
on the side opposite to the touch relaxes, causing the body to move away from
the site of the touch (Kristan,
1982). Touching control leeches at the posterior typically
elicited crawling (crawl).
In general, locomotory responses (i.e. crawl, swim and ic) were more common in response to posterior touch than in response to touch at other locations, and, in control animals, crawl was the most likely response (Fig. 3A). Whole-body contraction (wbc) was elicited by posterior touch, but it was typically produced in conjunction with other behaviours, and this tendency to combine with other behaviours reduced the absolute value of its CCA behaviour score. A similar trend was seen in the behaviour score for lb in response to posterior touch; it was generally seen along with other behaviours that were more strongly associated with posterior stimulation. Distributions of the individual scores (Fig. 3C) revealed that when the scores for the behaviours in control animals were grouped by touch location, all groups were significantly different from one other (ANOVA, F2,192=64.2, P<0.001, N=195).
Elicited behaviour: the effect of surgical manipulation
Anterior stimulation elicited sh in all groups of leeches,
regardless of treatment (Fig.
4A), so failed to distinguish among treatment groups. CCA showed
that anterior touch characteristically also elicited probe, fsr and
crawl in control animals (Fig.
4B,C), whereas following ablation, pivoting (pivot) and
lb were more common. Leeches with nerve cuts displayed a behavioural
profile in which there was less probing than in control leeches but more
probing than in leeches with ablations. CCA scores for individual leeches with
nerve cuts lay between the scores of controls and those of leeches with
ablations (Fig. 4C). The
overall distribution effect of surgery was significant (ANOVA,
F2,38=6.86, P<0.001, N=41), but the
only pair of groups that were significantly different from one another were
control and ablated leeches.
Because midbody stimulation most often elicited lb in all treatment groups (Fig. 5), this behaviour did not distinguish among the groups, whereas less common behaviours did (Fig. 5B). Probe and crawl were the most distinctive responses seen in control leeches, whereas swim and pivot behaviours distinguished leeches with ablations of the SubEG (Fig. 5C). Leeches with nerve cuts were once again intermediate between the control leeches and the leeches with ablations. The overall effect of surgery was significant (ANOVA, F2,38=12.33, P<0.001, N=41), which was due to significant differences between control and ablated leeches and between nerve cut and ablated leeches.
Posterior stimulation elicited locomotion in all three groups, but the form of the locomotion varied among the groups (Fig. 6A), so swimming and crawling effectively distinguished among the treatments (Fig. 6B). The most common response of control leeches to posterior touch was crawling, whereas leeches with SubEG ablations swam more often than they crawled (Fig. 6A). Touching the posterior end of the leech also elicited movements at the anterior end of the leech, and, in this case, probing was more typical of control leeches, whereas pivoting was more common following ablation. The overall effect of surgery was significant (ANOVA, F2,38=19.8, P<0.001, N=41) due to significant differences between control and ablated and between nerve cut and ablated leeches (Fig. 6C).
Severity of ablation
In the previous analyses, leeches with ablations were lumped into a single
group, but we also wanted to know whether ablating only part of the SubEG
would produce either a qualitative or a quantitative difference. To ask this
question, we focused on locomotory behaviours for three reasons. First,
locomotion requires coordination of the whole body and thus might be affected
by brain function. Second, unlike many elicited behaviours that were produced
wherever the animal was touched, locomotion was common only in response to
posterior touch, so we could focus our analysis on posterior touch. And third,
although locomotion was produced in all three experimental groups following
posterior touch, the form it took varied with experimental treatment (Figs
2A,
6A).
Ablating some or all of the SubEG affected both the level and the form of spontaneous locomotion, but surprisingly there were no statistically significant differences among leeches that were missing different numbers of neuromeres (Tukey's HSD, P>0.05; Fig. 7A). All leeches with SubEG ablations were inactive much of the time. However, when they did move around spontaneously, they typically swam or executed only part of the crawling cycle (ic), unlike controls and animals with nerve cuts, which crawled normally (Fig. 2A). In addition, once leeches with ablations began to swim, they typically continued for much longer than either control leeches or those with nerve cuts (data not shown), a pattern that was seen in all ablation groups regardless of severity. Similarly, we found no statistically significant differences among leeches missing different amounts of the SubEG when we considered elicited locomotion (Fig. 7B). These results suggest that many of the SubEG neurons affecting locomotion may be located in anterior neuromeres, so ablating posterior neuromeres in addition to the anterior ones produces relatively little additional effect.
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General level of activity
The most general conclusion from our results is that the head brain plays a
major role in setting the level of arousal, responsiveness and general
activity in the whole animal. Control leeches that crawled and actively probed
provided a stark contrast to surgically manipulated leeches, which spent more
than half of their time doing nothing at all or performing only slow probing
behaviours. This result is consistent with the results reported by Bullock
(Bullock and Horridge, 1965)
and suggests that generalized excitation descends from the SubEG to the rest
of the CNS. All neuromere ablations in this study severed the connection
between the SupraEG and the ventral nerve cord, and future experiments will
explore the effects of ablating just the SupraEG, while leaving all other
connections of the SubEG intact.
Changes in whole-body behaviour
Crawling behaviour consists of a set of sequential actions that must be
executed correctly and in the proper order if they are to produce forward
motion (Baader and Kristan,
1995; Cacciatore et al.,
2000; Stern-Tomlinson et al.,
1986). Following ablations, leeches produced some parts of
crawling behaviour, but they were typically uncoordinated, poorly executed and
ineffective. The SubEG controls the use of the front sucker, which may explain
part of this erosion of effective crawling following ablations. However,
cutting the nerves projecting from the SubEG, which disables the front sucker
as effectively as ablations, produced relatively little effect on crawling,
whereas even partial ablation of the SubEG all but eliminated normal crawling
(Fig. 7). We conclude that the
SubEG, in addition to controlling the use of the front sucker, must contribute
to organizing movements of the entire body during crawling; i.e. the
elongation and contraction along the entire body, as well as placement of the
rear sucker, which is likely also to depend heavily on neurons in the
posterior brain.
The marked increase in both spontaneous and elicited swimming that we
observed following ablations in the SubEG confirmed previous reports that the
SubEG suppresses swimming (Brodfuehrer and
Friesen, 1986). Leeches lacking a SubEG swam effectively but
seemed unable to stop; they often swam for much longer periods of time than
did control leeches. Similarly, adult leeches swim for much longer periods
immediately after the connection between the head brain and the ventral nerve
cord is severed (an effect well known among bait shop salespeople in the
American Midwest). Following ablations, leeches produced swimming that
appeared to be normal, which strongly suggests that the ablations left
connections within the ventral nerve cord unchanged. We suggest that swimming
is suppressed much of the time in intact leeches by neurons of the SubEG, such
as Tr2 and SIN-1 (Brodfuehrer et al.,
1995a,b;
Taylor et al., 2003). Tonic
suppression of swimming by the SubEG may then permit crawling in the absence
of stimuli that lead specifically to swimming, but, when cephalic inhibition
is lost, the default locomotory behaviour appears to be swimming.
We are beginning to understand the cellular basis for the choice between
swimming and crawling. In the head brain, a neuron called R3b1 can cause
either swimming or crawling depending on whether the leech is in deep water,
in which case it swims, or in shallow water, in which case it crawls
(Esch et al., 2002).
Interfering with the acquisition of sensory information from receptors in the
head changes this behavioural choice. For example, in one set of experiments
on adult leeches, the head brain was deafferented and the animals were tested
in water whose depth was equal to the thickness of the body. Leeches with
deafferented brains were highly likely to swim in this condition, whereas
normal leeches were most likely to crawl (S. Copado, W. B. Kristan, III and W.
B. Kristan, Jr, unpublished data). Thus, it appears that identifiable cells in
the SubEG participate in processing sensory information coming from cephalic
receptors and may play a central role in behavioural selection.
Locally controlled behaviours
Many studies have explored behaviours that are locally controlled by
neurons in segmental ganglia of Hirudo
(Kristan et al., 2005;
Kristan, 1982). This pattern
of local control remained intact following deafferentation or ablation of the
SubEG. In our experiments, moderate touch to locations in the anterior, middle
and posterior regions of the body elicited generally the same behaviours
regardless of which surgical group the individual belonged to: shortening in
response to anterior touch, local bending following midbody touch, and
locomotion following posterior touch (Figs
3,
4,
5,
6). If anything, these
responses to touch were slightly enhanced following SubEG ablations,
suggesting that modulatory signals descend from the SubEG. Thus, although our
results indicate that the SubEG exerts some control over behaviour, the
distributed nature of the leech nervous system allows many behaviours to be
controlled on a local level, much as vertebrate stretch reflexes are confined
to one or a few spinal segments with modulation descending from higher centres
(Kandel et al., 2000).
Ablations vs nerve cuts
In each of our analyses, cutting the nerves connecting the SubEG to the
periphery of the head produced a pattern of behaviour intermediate between the
control group and the leeches that were missing at least some of the SubEG
(Figs 2,
3,
4,
5,
6,
7). In advance of the analyses,
there was no compelling reason to predict this outcome, and, although the CCA
took account of the experimental group to which each individual belonged, it
imposed no particular ordering of the groups. This result suggests that one
important role of the SubEG is to integrate signals from cephalic sensory
neurons with signals from neurons in the rest of the body; when sensory input
from the head is no longer available, there is erosion in the behaviour, but
the animal neither falls into lassitude nor shifts to an entirely novel set of
behaviours.
Comparison with other animal groups
The literature describing brain structure and function in other
invertebrate groups is enormous and complex but, until recently, tended to be
biased toward exquisite descriptions of anatomy
(Bullock and Horridge, 1965;
Gupta, 1987). Much attention
has been paid to the brains of arthropods, especially the complex brains of
insects. Progress has been made in elucidating function in the brain regions
devoted to sensory processing, e.g. the olfactory system
(Christensen and Hildebrand,
2002; Galizia and Menzel,
2000) and the visual system in insects
(Egelhaaf and Borst, 1993;
Egelhaaf and Kern, 2002). The
mushroom bodies in the insect brain seem to be association centres that play a
variety of roles. They are thought to participate in the control of locomotion
(Heisenberg, 1998;
Zars, 2000), they are
typically associated with olfaction
(Strausfeld et al., 1998) and
they contribute to learning and memory
(Menzel, 2001;
Strausfeld et al., 1998). All
of these structures are located in the supraesophageal brain, whose structure
can be highly elaborate. The subesophageal ganglion (SubEG) in arthropods has
a simpler structure, and it exerts both excitatory and inhibitory control,
providing coordination of several behaviours, including locomotion
(Altman and Kien, 1987) and
stridulation (Heinrich, 2002;
Heinrich et al., 1998).
The brain in molluscs varies from relatively simple ganglion-like
collections of neurons, as in snails
(Chase, 2000), to the highly
complex brains of the cephalopods
(Williamson and Chrachri,
2004). Here, too, we know more about anatomy than about function,
except in specific instances, such as olfactory function in the brain of the
slug Limax (Cooke and Gelperin,
2001; Gelperin et al.,
2000) and control of escape behaviour in the squid Loligo
(Williamson and Chrachri,
2004). In addition, particular regions of the brain in
Octopus are required for learning sensory discriminations.
Our results suggest that, in spite of the distributed nature of the annelid CNS and the relative morphological simplicity of the head brain, the SubEG plays many of the roles seen in a large variety of other animals, including the vertebrates: it provides general excitation that increases the activity of the animal; it is a source of inhibition that shapes the behaviour exhibited by the animal either subtly, as in the local responses to touch or, dramatically, as in the changes in locomotory pattern that accompany ablation of the SubEG; it integrates sensory information coming from receptors in the head with signals coming from other parts of the body; and it plays a crucial role in orchestrating whole-body behaviour such as crawling. We therefore suggest that these functions of the brain may well be primitive characters that have been preserved through evolution. Other abilities, such as learning and memory, have been added to the work of the brain in many taxa, but the relatively large size and small number of neurons in the leech SubEG may provide an excellent opportunity to understand many brain functions at a cellular and network level.
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Acknowledgments |
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References |
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