|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
Review |
Comparative neuroethology of feeding control in molluscs
1
Department of Biology, University of York, York YO10 5YW, UK
2
Faculty of Life Sciences, Gonda (Goldschmied) Medical Diagnostic Research
Center, Bar-Ilan University, Ramat-Gan 52 900, Israel
* e-mail: cje2{at}york.ac.uk
Accepted 16 January 2002
 |
Summary |
|---|
 TOP Summary IntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
Key words: feeding, Aplysia, Lymnaea, Limax, Helisoma, Pleurobranchaea, gastropod, mollusc, pattern generation, neuromodulation, arousal, learning, feeding choice, grandmother cell
|
Introduction |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
). Studies on neural systems generating feeding
have begun to provide rich insights into how complex regulatory phenomena
arise from the properties of individual neurones and their
interconnections. Investigations in some genera, notably Aplysia, have taken a top-down approach, beginning by characterizing behaviour and then proceeding to the nervous system. In these studies, new information on the cellular and network properties of neurones is systematically interpreted in the light of previous findings on behaviour. By contrast, in other genera (e.g. Lymnaea and Helisoma), the work initially had the aim of exploring the properties of relatively simple invertebrate nervous systems (Fig. 1). After the features of some of the neurones and networks had been determined, attempts were made to relate these findings to behaviour. Initially, this approach minimises functional explanations and stresses system properties and pharmacology. Over the years, work using the two approaches has converged. Our aim is to summarize and compare the results obtained in the different species and, thereby, to point to insights into the functioning of the nervous system that are of general interest.
|
Feeding has been studied in both carnivorous and herbivorous gastropods. Many aspects of feeding in both herbivores and carnivores will be discussed, although the emphasis will be on herbivores, particularly Aplysia and Lymnaea. These two genera are currently being studied by many more researchers than are the other gastropods and, consequently, there are many more recent publications on these molluscs.
|
Structure of the feeding system |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
;
Hermans and Satterlie, 1992).
In most gastropods, food is eventually engaged by the radula, which is
controlled by the buccal muscles. These muscles cause the radula to protract
out of the mouth towards the food and then to pull the food into the buccal
cavity, or to rasp the food, with a retraction movement
(Fig. 2). In some gastropods
(e.g. Aplysia and Pleurobranchaea), a fold in the centre of
the radula acts as a hinge that allows the two radula halves to open and close
(Kupfermann, 1974;
McClellan, 1982a).
|
The buccal mass is innervated by the paired buccal ganglia, which connect to the cerebral ganglia (or to the fused cerebral-pleural ganglia in Pleurobranchaea) by the paired cerebro-buccal connectives. The cerebral ganglia innervate the anterior portion of the animal, including many structures related to feeding, such as the rostral foot, the head, the sensory anterior and posterior tentacles (rhinophores), the lips and the mouth. The cerebral ganglia also innervate extrinsic buccal muscles, which cause forward and backward movements of the whole buccal mass. These ganglia also communicate with the rest of the central nervous system.
|
Feeding movements |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
;
Bovbjerg, 1968;
Bicker et al., 1982). Food
initiates appetitive behaviours, which generally include orientation and
locomotion towards food. These movements may be similar to those in response
to other attractive stimuli, such as potential mates (Leonard and Lukowiak,
1984,
1986;
Ziv et al., 1989). Locomotion
towards food may also be similar to locomotion away from noxious stimuli. In
addition, appetitive movements in Aplysia include head-lifting and
head-waving (Kupfermann,
1974; Teyke et al.,
1990a,b).
In Helix, the chemosensory posterior tentacles point towards food
before the animals locomote towards it
(Peschel et al., 1996).
Contact with food is sensed by both mechano- and chemoreceptors
(Rosen et al., 1982;
Bicker et al., 1982). These
initiate the next phase of feeding.
In carnivores, a separate prey-capture phase may occur after the appetitive
movements, but before the food is consumed. Appetitive and prey-capture
movements in carnivores are often highly specialised. For example,
prey-capture in Pleurobranchaea consists of an extension of a unique
structure, the proboscis, which precedes a ballistic bite/strike response
(Davis and Mpitsos, 1971).
Navanax pursue their prey (other gastropods) by following their mucus
trails (Paine, 1963). They
then engulf prey with an unusual expandable pharynx that lacks a radula
(Susswein et al., 1984a).
Clione evert specialised buccal cones surrounding the mouth. The
cones bear hooks, which pull at prey before it is consumed
(Hermans and Satterlie, 1992;
Norekian, 1995).
In Lymnaea and other pulmonates, such as Helisoma,
Planorbis and Helix, the consummatory phase of feeding consists
of a series of repetitions of three sequential movements: (i) protraction, in
which the radula extends to contact the food; (ii) retraction, in which the
radula rasps the food and brings it into the mouth; and (iii) swallowing or
hyper-retraction, in which the food is conveyed to the gut
(Fig. 2A)
(Kater, 1974;
Peters and Altrup, 1984;
Rose and Benjamin, 1979). In
addition, the radula can rotate over the underlying support tissue, allowing
flexibility in the amplitude of a rasp
(Smith, 1988). In
Lymnaea, the feeding pattern can be modified to produce egestion.
Furthermore, a motor sequence very similar to that in feeding is used in
egg-laying, to clean off the substratum on which animals will lay eggs.
Although the behaviour — seen from outside the snail — appears
similar to that in feeding, fine-wire recordings of the neural activity show
that the motor pattern for egg-laying is significantly different (Jansen et
al., 1997,
1999).
Consummatory movements in Aplysia differ from those in the
pulmonates in that there are only two phases, protraction and retraction.
Protraction and retraction are synchronized with movements of the lips and
jaws, and with radula opening and closing movements, to produce a variety of
functionally different consummatory movements. These include biting, which
causes food to enter the mouth
(Kupfermann, 1974),
swallowing, cutting and related movements triggered by food within the mouth
(Hurwitz and Susswein, 1992)
and at least two qualitatively different rejection movements, in which food or
a non-food object is pushed away
(Kupfermann, 1974; Morton and
Chiel,
1993a,b;
Nagahama et al., 1999). The
different movements are characterised by differences in the relative amplitude
of protraction and retraction and by differences in the coupling with radula
opening and closing and/or jaw movements. For example, in biting, the radula
protracts while open, and then closes on the food during retraction, thereby
pulling it in. By contrast, in rejection, protraction is accompanied by radula
closing, thereby pushing objects out (Morton and Chiel,
1993a,
b). Food is cut by swallowing
while holding the food in place with the jaws. Rasplike grazing movements
similar to those in Lymnaea may also occur
(Kupfermann and Carew, 1974).
When Aplysia consume their natural food (various species of
seaweeds), the frequency and nature of successive movements vary from cycle to
cycle, with many cycles representing intermediate states that are difficult to
classify.
In Pleurobranchaea, the initial bite/strike prey-capture response
is followed by two stages of consummatory movements. Repetitive biting
movements pull prey into the pharynx, and repetitive swallowing movements
transport the prey from the pharynx into the gut. The movements are similar to
those in Aplysia in that protraction and retraction movements are
coordinated with opening and closing of the radula halves
(Croll and Davis, 1981;
McClellan, 1982a).
Pleurobranchaea also perform a number of different types of movement
that clear objects from the pharynx and gut. These have variously been termed
egestion, rejection, regurgitation, writhing or vomiting
(Croll and Davis, 1981;
McClellan, 1982a,
b). These movements may be
signalled by the presence of non-food objects in the pharynx or noxious
chemical substances in the gut. There have been disagreements as to whether
these represent fundamentally different movements or are minor variants of a
single movement that are initiated in somewhat different behavioural contexts
(Croll et al., 1985a;
McClellan, 1982a,
b).
|
Neural circuitry organizing feeding movements |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
).
Identified neurone C-PR has a major role in organizing the head-lifting
movement (Nagahama et al.,
1993). Intracellular stimulation of C-PR produces such movements,
and neck motoneurones are excited (mostly polysynaptically, but in some cases
monosynaptically) by C-PR firing
(Nagahama et al., 1994).
In Helix, the tentacles that point towards food are innervated by
two peritentacular nerves (PTns), each projecting to approximately one
hemi-section of the tentacle wall. Stimulating the peritentacular nerves
causes the tentacles to bend downwards as they do when they orient towards
food (Peschel et al.,
1996).
Consummatory movements
Consummatory movements are initiated by command-like neurones projecting
from the cerebral to the buccal ganglia. These neurones were first
characterized in Pleurobranchaea, in which they were termed the
paracerebral neurones (Gillette et al.,
1978). In Lymnaea, Limax and Aplysia,
respectively, these are termed cerebral ventral 1 cells (CV1s), cerebral
buccal cells (CBs) or cerebral buccal interneurones (CBIs)
(Fig. 3)
(Delaney and Gelperin, 1990;
McCrohan, 1984;
Rosen et al., 1991). The
neurones are excited by food stimulating the lips
(Davis and Gillette, 1978;
Kemenes et al., 2001;
Whelan and McCrohan, 1996).
At least in Lymnaea and Aplysia, this activation may be
indirect. In Lymnaea, sucrose appears to activate the buccal central
pattern generator before the CV1 interneurones, whereas in Aplysia,
some of the CBIs are excited by neurone C-PR, which controls appetitive
movements (Hurwitz et al.,
1999b; Teyke et al.,
1990a). The CBIs directly excite buccal ganglia neurones that
generate the repetitive consummatory rhythm
(Rosen et al., 1991;
Sanchez and Kirk, 2000).
|
In Lymnaea, Aplysia and Pleurobranchaea, the commandlike
neurones are a heterogeneous population that are not equally effective in
eliciting consummatory movements (Hurwitz
et al., 1999b; Kovac et al.,
1983; McClellan,
1983a; McCrohan and Croll,
1997; Xin et al.,
1999). In Pleurobranchaea and Aplysia, it has
been suggested that different combinations of CBIs may work together at
different times and, thereby, differentially give rise to different feeding
movements (McClellan 1983a;
Xin et al., 1999). In
Pleurobranchaea and Aplysia, the cerebral ganglion
command-like neurones may receive input from identified buccal ganglion
neurones, which may modify their activity
(Davis et al., 1984;
Gillette et al., 1978;
Chiel et al., 1988) and may
influence the choice of the movements used in a feeding sequence. Additional
command-like neurones are also found in the buccal ganglia of
Pleurobranchaea and Lymnaea
(Gillette and Gillette, 1983;
Gillette et al., 1980;
McClellan, 1983b;
Yeoman et al., 1993), and
sucrose application to the lips in Lymnaea can recruit these to the
feeding pattern (Kemenes et al.,
2001).
The rhythmic pattern of consummatory movements is generated primarily by
buccal ganglion interneurones. In Lymnaea, Planorbis and
Helisoma, three classes of central pattern generator (CPG)
interneurone (termed N1, N2 and N3) have been identified. Instantly
recognisable (by both anatomy and physiology) homologues are present in all
three genera (Arshavsky et al.,
1988a,
b,
c;
Brierley et al., 1997b;
Elliott and Benjamin, 1985a;
Quinlan et al., 1995,
1997;
Quinlan and Murphy, 1996;
Rose and Benjamin, 1981b;
Murphy, 2001). These N-cells
fire bursts of action potentials in turn, with the activity in each class
confined to the corresponding phase in the feeding pattern. The N-cells are
mostly pre-motor interneurones providing a strong chemical synaptic drive to
motoneurones that is often supplemented by feedforward electrical connections.
In Lymnaea, it was initially believed that interneurones acting
together in phase are different-sized homologues, but more recent experiments
indicate that the interneurones within each group differ in many properties
(Brierley et al., 1997b;
Elliott and Benjamin, 1985a;
Vehovszky and Elliott, 2001).
Selective recruitment of different neurones provides a potential mechanism for
modulating the rhythm to produce different motor patterns.
In Lymnaea, Aplysia and Helisoma, rhythmic feeding
activity depends both on the endogenous membrane properties of the
interneurones and on the synaptic connections between them. As in other CPGs,
the membrane properties include bursting, post-inhibitory rebound and plateaux
potentials, and these properties control much of the timing of a phase. These
membrane properties are under modulatory control, and this contributes to the
patterning of the feeding rhythm (Straub
and Benjamin, 2001).
The synaptic connections determine the sequence of the phases
[Aplysia (Hurwitz and Susswein,
1996; Hurwitz et al.,
1997; Plummer and Kirk,
1990), Lymnaea
(Brierley et al., 1997a;
Elliott and Benjamin, 1985a)
and Planorbis (Arshavsky et al.,
1988b)]. As in many CPGs, interneurones active during the same
stage of feeding are often electrically and chemically coupled
(Brierley et al., 1997b;
Elliott and Benjamin, 1985a;
Susswein and Byrne, 1988),
whereas neurones active at different stages often show reciprocal inhibition.
However, interneurones active in different phases may also show weak
excitatory connections, which provide a mechanism for switching from an
earlier to a later phase. For example, in the Lymnaea CPG, the N1
(protraction) cells weakly excite the N2 (rasp) interneurones until the N2
interneurones fire, when they inhibit the N1 neurones and terminate
protraction (Elliott and Benjamin,
1985a; Brierley et al.,
1997b). In Aplysia, activity in the protraction-phase
interneurones (B63, B34 and B31/B32) is initiated by sensory inputs, in part
mediated via the cerebral-buccal interneurones (CBIs)
(Rosen et al., 1991). The
switch to retraction is initiated by depolarisation of neurones (B64 and B51)
that strongly inhibit protraction-phase neurones and strongly excite
retraction-phase neurones (Hurwitz et al.,
1994; Hurwitz and Susswein,
1996) A cycle is terminated in part via a neurone (B52)
that inhibits retraction-phase neurones
(Evans et al., 1999a).
Protraction-phase interneurones with remarkably similar properties are
found in Aplysia, Lymnaea and Planorbis
(Fig. 4) and in
Helisoma. These have axons in the contralateral cerebro-buccal
connective, display small spikes (presumably because the soma is inexcitable)
and gradually depolarise during a burst
(Arshavsky et al., 1988b;
Elliott and Kemenes, 1992;
Hurwitz et al., 1994,
1997). Although neurones with
similar small spikes are common in arthropods, in gastropods they have been
reported only from the buccal and cerebral (e.g.
Perrins and Weiss, 1998)
ganglia neurones associated with the control of feeding. The lack of
excitability in some portions of a neurone may allow different parts of a
neurone to fire at different rates or to use slow potentials in place of
spikes in local signalling at specific terminals. These neurones
morphologically and physiologically resemble in many ways the corollary
discharge (CD) neurones that in Pleurobranchaea have been shown to
allow communication from the buccal to the cerebral ganglia (see below).
|
Cyclic feeding movements are expressed in effector organs controlled by
both the buccal and cerebral ganglia. It was initially suggested that
independently oscillatory circuits are present in the brain (cerebro-pleural
ganglion) and buccal ganglia of Pleurobranchaea since each is capable
of responding with phasic bursts to tonic nerve stimulation. Functionally, the
rhythm is set in the buccal ganglia, and coordination between the separate
oscillators is effected by a group of `corollary discharge' or `efference
copy' neurones, which carry information from the buccal to the cerebral
ganglion (Davis et al., 1973).
However, later studies indicated that phasic bursts in the brain could be
generated in the absence of a separate oscillator, because buccal-cerebral
interneurones responded phasically to tonic stimulation
(Cohan and Mpitsos, 1983).
Nonetheless, later studies succeeded in demonstrating convincing phasic
bursting in the isolated brain, confirming that a second oscillator is indeed
present (Davis et al., 1984;
London and Gillette,
1984a,b).
Coupled oscillators are also present in the cerebral ganglia of
Aplysia (Perrins and Weiss,
1996) and Lymnaea.
Multifunctional neurones
Many neurones in the feeding circuit seem to have multiple functions.
Neurones with proposed multiple functions have been found in several
invertebrate circuits. However, the molluscan emphasis on parallel studies on
behaviour and on the nervous system has permitted researchers to understand
these functions in a detail not available in other systems. For some neurones,
the different functions of a neurone enhance one another. For example, in
Aplysia, neurone B51 acts both as a retraction-phase interneurone
(Plummer and Kirk, 1990) and
as a proprioceptor (Evans and Cropper,
1998). In addition to exciting many retraction-phase motoneurones,
B51 has sensory branches that are activated during retraction. These inputs
are enhanced by resistance to retraction and thereby act as a monitor of the
success of retraction, which can enhance retraction when the movement is not
successful.
A second example of related functions in a single neurone is seen in
neurone B52, whose outputs to other CPG neurones suggest that the neurone
terminates a cycle of activity (Evans et
al., 1999a). This neurone innervates a flap of connective tissue
that is stretched by retraction just before the end of a cycle, allowing the
sensory input to enhance the pattern-generating function. Similar peripheral
branches have been reported in retraction-phase neurones of Lymnaea
(Elliott and Benjamin, 1985a).
Electrical connections in Lymnaea between the motoneurones and
interneurones suggest that the motoneurones may also play a secondary part in
producing the rhythm (Staras et al.,
1998), but the weakness of the connections suggests that this is a
minor role.
B21 in Aplysia is a striking example of a multi-functional
neurone. B21 is a mechano-afferent that responds to food touching the radula
(Miller et al., 1994). It has
extensive chemical and electrical synapses onto the CPG and motoneurones, and
activity in B21 enhances the switch from protraction to retraction
(Rosen et al., 2000b). B21 is
also depolarised by the CPG during retraction. The central excitation enhances
the neurone's sensory function, since depolarising B21 enhances some of its
outputs (Rosen et al.,
2000a). In addition to acting as an exteroceptor sensing radula
touch, B21 also is a proprioceptor. The tissue innervated by B21 consists
partially of muscle. B21 senses this muscle's contraction during protraction,
causing B21 to fire during the protraction phase of biting. Thus, B21 acts as
a proprioceptor during protraction and as an exteroceptor during retraction
(Borovikov et al., 2000).
Some protraction-phase neurones in Aplysia combine interneurone
and motoneurone functions, with the different functions assigned to different
parts of the neurone. For example in B31/B32, activity in the soma functions
as part of the CPG, whereas activity in the axon drives a major
protraction-phase muscle (I2). Spikes in the axon do not actively invade the
pattern-generating portion of the neurone
(Hurwitz et al., 1994).
Switching between different feeding movements
As in other systems (Marder and
Calabrese, 1996), it has been found that a single CPG can give
rise to both quantitatively and qualitatively different patterns of activity.
However, the parallel studies on behaviour and the nervous system have allowed
researchers to examine in detail the relationship between cellular and systems
properties of a CPG and the behaviours that are the products of CPG
activity.
In Aplysia, Lymnaea, Helisoma and Pleurobranchaea, a
single CPG in the buccal ganglia generates a number of different patterns of
activity (Murphy, 2001). In
Aplysia and Pleurobranchaea, these patterns can be
correlated with the expression of different behavioural patterns (Croll and
Davis, 1981,
1982;
Hurwitz et al., 1996;
McClellan,
1982a,b;
Morton and Chiel,
1993a,b).
In the isolated central nervous system of Helisoma, an alternative
pattern can occur in which phase 2 (rasp) and phase 3 (swallow) can alternate
without phase 1 (protraction) (Quinlan
and Murphy, 1996). In Aplysia, a number of different
mechanisms contribute to the choice between different behaviours. One
mechanism is the recruitment of different combinations of command-like
neurones (Xin et al., 1999).
For example, in Aplysia, intracellular stimulation of CBI-2 and
CBI-12 differentially causes repetitive bursts of bite-like activity
(Church and Lloyd, 1994;
Hurwitz et al., 1999b),
whereas stimulation of CBI-1 induces a rejection-like burst
(Rosen et al., 2000a).
Other CBIs produce activity patterns that are difficult to classify. In
Pleurobranchaea, stimulating the paracerebral cells and the ventral
white cell in the buccal ganglia initiates different patterns of activity that
are correlates of different movements (Croll et al.,
1985b,c;
Gillette and Gillette, 1983;
McClellan,
1983a,b).
A second mechanism contributing to the choice of different behaviours is that
different combinations of buccal ganglia CPG neurones are called into play.
For example, neurone B34 fires during only some protraction movements. Its
activity makes movements more rejection-like, since this neurone amplifies the
activity of protraction-phase motoneurones and drives radula closer
motoneurones during protraction (Hurwitz
et al., 1997). Neurone B51 fires during only some retraction
movements and makes movements more ingestion-like
(Nargeot et al., 1999b) (or
perhaps more swallowing-like) (see Evans
and Cropper, 1998) by amplifying firing of retraction-phase
neurones and driving radula closer motoneurones during retraction. Sensory
neurones such as B21 that respond to food touching the radula may also
contribute to biasing a switch between different types of movement. In
Lymnaea, the pattern produced by stimulating the modulatory SO
interneurone (Elliott and Benjamin,
1985b; Rose and Benjamin,
1981a) is different from that seen spontaneously or by stimulating
the N1 CPG interneurone (Elliott and
Andrew, 1991), suggesting that SO-induced activity represents an
alternative behaviour.
A fourth mechanism contributing to the choice between different movements
is modulation by different regulatory transmitters
(Kabotyanski et al., 2000).
The effectiveness of a modulator depends on the state of the network.
Stimulation of the cerebral serotonergic cells in Lymnaea may
activate the feeding pattern only in quiescent preparations. If a fictive
feeding pattern is already running, stimulation of the serotonergic cells can
either accelerate or reduce the feeding rate depending on the state of the
system (McCrohan and Audesirk,
1987; Tuersley and McCrohan,
1988).
The buccal octopaminergic interneurones (OCs) show particularly fascinating
modulatory effects. First, their activity will accelerate slow rhythms and
slow down fast rhythms. Such mechanisms may promote the stability of
particular rhythmic patterns. Second, the OC interneurones also reconfigure
the feeding pattern through their network of connections with the other
feeding interneurones and motoneurones. Third, they modulate the output of the
SO, a cholinergic modulatory interneurone also located in the buccal ganglia.
Finally, stimulation of the OC in a quiescent preparation produces fictive
feeding, but only well after the end of stimulation
(Elliott and Vehovszky, 2000;
Vehovszky and Elliott, 2001).
Many of their effects are polycyclic, i.e. they last over several repeats of
the feeding pattern.
Comparative pharmacology
Many neurotransmitters are utilised in the feeding network. The behavioural
role of a transmitter is often known since the functions of the neurones
utilising the transmitter have been determined.
In Aplysia, most of the motoneurones innervating the buccal
muscles are cholinergic (e.g. Cohen et
al., 1978) and a small number are glutamatergic
(Fox and Lloyd, 1999).
Cholinergic and glutamatergic motoneurones may innervate the same muscle
(Keating and Lloyd, 1999). At
present, it is unclear why different conventional transmitters should be used
by motoneurones. CPG neurones also release these two transmitters.
Acetylcholine (ACh) is released by the protraction-phase interneurones in
Lymnaea (Elliott and Kemenes,
1992; Vehovszky and Elliott,
1995; Yeoman et al.,
1993), and glutamate is released by the retraction-phase
interneurones in Lymnaea and Helisoma
(Brierley et al., 1997c;
Quinlan and Murphy, 1991;
Quinlan et al., 1995). Each
transmitter has excitatory and inhibitory receptors on follower cells, with
more than one kind of inhibitory receptor sometimes present on a single cell.
In Aplysia, some of the command-like neurones, as well as
protraction-phase interneurones, are cholinergic
(Hurwitz et al., 1999a).
Indirect evidence suggests that the chemoreceptors innervating the lips and
sensing the presence of food in Aplysia, Limax and
Pleurobranchaea are cholinergic, and for this reason the application
of cholinergic agonists to the cerebral ganglion induces repetitive feeding
bouts (King et al., 1987;
Susswein et al., 1996;
Morielli et al., 1986).
Serotonin is present in the giant cerebral cell in all species. Serotonin
modulates sensory neurones, interneurones and motoneurones as well as the
buccal musculature [Lymnaea (McCrohan and Benjamin,
1980a,b;
Yeoman et al.,
1994a,b,
1996); Aplysia (for
a review, see Kupfermann,
1997), Achatina
(Yoshida and Kobayashi,
1991), Helix
(Bernocchi et al., 1998) and
Pleurobranchaea (Gillette and
Davis, 1977; Moroz et al.,
1997; Sudlow et al.,
1998)]. Other monoamines, including dopamine and octopamine are
present in buccal ganglion cells and also modulate the pattern. In Limax,
Helisoma, Lymnaea and Aplysia, exogenous dopamine application to
the buccal ganglia induces fictive feeding
(Kabotyanski et al., 2000;
Kyriakides and McCrohan,
1989; Quinlan et al.,
1997; Wieland and Gelperin,
1983).
In Aplysia, one command-like neurone (CBI-1) is dopaminergic. The
buccal ganglia of Helix, Lymnaea, Helisoma and Aplysia all
contain dopaminergic neurones; in the latter two genera, they are
protraction-phase neurones that can initiate motor patterns
(Elekes et al., 1991;
Hernadi et al., 1993;
Kabotyanski et al., 1998;
Quinlan et al., 1997;
Teyke et al., 1993). In
addition, many peripheral neurones in the gut of Helix and
Aplysia may be dopaminergic (Hernardi et al., 1998;
Susswein et al., 1993). In
Lymnaea, octopamine antagonists (but not the dopamine antagonists
tested) block feeding responses
(Vehovszky et al., 1998).
Their effect may be explained in part by the presence of three OC
(octopamine-containing) neurones in the buccal ganglia
(Vehovszky et al., 1998)
which, when stimulated, produce fictive feeding after a significant delay.
Similar neurones are present in Helix
(Hiripi et al., 1998) and
Helisoma (N3a) (Quinlan and
Murphy, 1996). In Aplysia, exogenous dopamine and
serotonin modulate the rate and form of buccal motor programs
(Kabotyanski et al., 2000).
The cerebral ganglion also contains an identified histaminergic sensory
neurone that excites the giant cerebral neurone
(Weiss et al., 1986).
Studies on gastropod feeding were among the first showing that many
neurones synthesize and release both conventional neurotransmitters and
peptide cotransmitters. Many of the basic insights into the cellular
neurobiology of peptide cotransmitters come from work on these systems (for a
review, see Kupfermann,
1991). Insight into the function of cotransmitters has been
facilitated by the availability of parallel information on behaviour and on
network interconnections. Cotransmitters functioning in the feeding system
include SCPA and SCPB, FMRFamide, FRFA,
FRFB and FRFC, APGWamide, buccalin and myomodulin.
Cotransmitters are found in motoneurones, interneurones and sensory
neurones.
At the neuromuscular junction, the combined release of peptides and
conventional transmitters allows the separate regulation of muscle contraction
and relaxation (Brezina et al.,
2000; Church et al.,
1993; Evans et al.,
1999b; Fox and Lloyd,
1997; Vilim et al.,
1996a,
b,
2000), permitting the muscles
to be used through a broader frequency range of buccal movements. Co-release
of a conventional and of a modulatory transmitter has been demonstrated, with
the peptides generally released at higher firing rates. Peptide-releasing
interneurones include CBI-12 in Aplysia, which contains myomodulin
(Hurwitz et al., 1999a,
b), and buccal interneurones
SO and N1L in Lymnaea (Santama
et al., 1994; Vehovszky and
Elliott, 1995; Yeoman et al.,
1993). Mechanoafferents innervating the radula utilise SCP and
glutamate (Klein et al.,
2000). FMRFamide inhibits feeding in Helisoma and
Lymnaea (Kyriakides and
McCrohan, 1989; Murphy et
al., 1985) as a result of the action of a pleural ganglion neurone
projecting to the buccal ganglia [Helisoma:
(Murphy, 1990),
Lymnaea (Alania et al.,
2002)]. This connection is conserved in many species, including
Lymnaea and Helix, and even in the carnivorous predator
Clione (Alania, 1995;
Alania et al., 1999).
Nitric oxide (NO) plays a prominent role in a number of sites in the
feeding systems of many gastropods. In both Lymnaea and
Aplysia, lip chemosensors with peripheral cell bodies release NO, in
addition to ACh, and an increase in NO levels in the cerebral ganglion can
induce repetitive bouts of feeding programs
(Elphick et al., 1995;
Moroz et al., 1993;
Moroz, 2000). In
Lymnaea, gut motoneurone B2 excites other motoneurones via
both ACh and NO (Park et al.,
1998; Perry et al.,
1998). In addition, the serotonergic giant cell in the cerebral
ganglia also expresses the gene for nitric oxide synthase (NOS). Expression of
this gene may be controlled by a NOS pseudogene with an anti-sense sequence
(Korneev et al., 1998,
1999). In Aplysia, a
primary mechano-afferent neurone produces a slow, conductance-decreasing
excitatory postsynaptic potential (EPSP) onto the giant cerebral cell
via the release of both histamine and NO
(Koh and Jacklet, 1999). In
Limax, the procerebral (PC) lobe contains approximately
105 local interneurones that respond to food odours with coherent
oscillations. The frequency of the oscillations is affected by both NO and CO.
Many neurones in the PC lobe contain NOS
(Gelperin et al., 2000).
NOS-containing neurones also play a role in the regulation of feeding in the
carnivorous gastropods Pleurobranchaea
(Moroz and Gillette, 1996)
and Clione (Moroz et al.,
2000). In these animals, NOS-containing neurones are found
exclusively within the central nervous system, whereas in the herbivorous
gastropods many peripheral neurones also contain NOS. It has been suggested
that the differences in distribution of NOS-containing neurones may be related
to differences in feeding ecology since the carnivores eat large, infrequent
meals, whereas the herbivores graze for many hours per day
(Moroz et al., 2000).
Other transmitters, including 
-aminobutyric acid (GABA), which is
found in buccal and cerebral ganglion neurones in Lymnaea
(Hatakeyama and Ito, 2000),
Helix (Hernardi, 1994), Helisoma (Richmond et al.,
1991,
1994) and Aplysia
(Diaz-Rios et al., 1999), also
play a role in activating the feeding pattern, probably through the actions of
the GABAergic cerebro-buccal and buccal-cerebral interneurones. Injection of
GABA into the haemocoel of Clione also evokes feeding movements
(Arshavsky et al., 1993).
|
Modulation of feeding movements by changes in state |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
Food arousal
Food initiates a state of food arousal, in addition to driving feeding
movements (Kupfermann, 1974).
Arousal is mediated largely by slow, modulatory connections between neurones
(Kupfermann et al., 1991).
The neural circuitry underlying food arousal is partially parallel to that
generating feeding movements in that some neurones apparently have a purely
modulatory function. However, food arousal also partially arises from aspects
of neural function that are embedded within the same neurones that effect the
feeding movements.
The most prominent purely modulatory neurones are the giant serotonergic
cells, which are a constant feature in all the gastropods (although they are
known by different abbreviations, MCC, MCG, CGC, in different species).
Chronic recordings show that these cells fire during feeding behaviour
(Kupfermann and Weiss, 1982)
and also (in Lymnaea) during egg-laying
(Yeoman et al., 1994b). Their
axons project to the buccal ganglia and to the buccal muscles, where most of
the neurones and muscles are modulated by serotonin
(Kupfermann et al., 1991).
Both protraction- and retraction-phase muscles and motoneurones are modulated,
as is the sensitivity of mechano-afferents innervating the radula
(Alexeeva et al., 1998;
McCrohan and Benjamin, 1980a,
b;
Weiss et al., 1978;
Yeoman et al., 1996).
Evidence for the behavioural function of these cells comes from chemical
ablation experiments in Aplysia, in which radula retraction was
delayed and the strength of movements weakened
(Rosen et al., 1989). Other
aspects of the feeding behaviour, for example the latency to bite, were not
affected. In Lymnaea, laser ablation of these cells in the isolated
central nervous system slowed fictive feeding, with the biggest changes being
longer inter-bite intervals (Yeoman et
al., 1994a). Injection of the serotonergic neurotoxin
5,6-hydroxytryptamine into the intact Lymnaea reduced feeding after
12-18 days, at a time when the levels of serotonin were also reduced
(Kemenes et al., 1990). This
was mostly due to changes in latency to feed, with shorter bites and longer
interbite intervals. By contrast to the purely modulatory effects seen in the
herbivores, stimulating the MCG in Pleurobranchaea accelerates
ongoing feeding rhythms or causes short-latency motor output, suggesting that
the neurone has a command-like function
(Gillette and Davis,
1977).
In Aplysia, the MCC is strongly excited by neurone C-PR, which has
both mediating and modulatory functions and is activated by food. It elicits
head-lifting and also affects a variety of neurones whose activities are
changed when Aplysia becomes aroused by food. It has been suggested
that C-PR may function to elicit food arousal
(Teyke et al., 1990a). In
addition to driving the MCC, C-PR also drives additional purely modulatory
neurones in the pedal ganglion, which modulate body wall postural muscles that
are active during food arousal (Nagahama
et al., 1994). C-PR also excites some command-like CBIs that
initiate repetitive consummatory movements
(Hurwitz et al., 1999b). The
initiation both of an arousal state and of appetitive behaviours by the firing
of a single neurone indicates that the appetitive behaviours may represent a
motor read-out of the arousal state
(Kupfermann et al.,
1991).
Food arousal is also partially mediated via the same synaptic
connections mediating feeding movements. For example, command-like neurone
CBI-2 in Aplysia elicits repetitive bite-like activity and also
increases the excitability of CPG neurones
(Hurwitz et al., 1999a). The
mediating and modulating effects of CBI-2 may be partially via
different transmitters. CBIs release both ACh and peptides
(Morgan et al., 1997;
Wu-Morgan et al., 1998). In
addition, many of the motoneurones driving the buccal muscles release peptides
as well as conventional transmitters (e.g.
Church et al., 1993; Evans et
al., 1999b; Fox and Lloyd,
1997,
1999).
A major insight into the neural basis of arousal arises from the finding that modulatory cells affect several successive levels of processing: sensory neurones, other modulatory interneurones, CPG interneurones and motoneurones. Modulatory effects benefit from the feedforward organization, leading to a cumulative modulation. Examples of this are provided by the cerebral giant serotonergic cells, by the buccal ganglia SO and OC of Lymnaea and by the C-PR and CBI neurones in Aplysia.
Satiation
In Aplysia, Limax and Lymnaea, feeding is inhibited by
mechanical stimuli that result from filling the gut with food
(Elliott and Benjamin, 1989;
Kuslansky et al., 1987;
Reingold and Gelperin, 1980;
Susswein and Kupfermann,
1975a,
b). The inhibition is a
graded function of the degree to which the gut is filled
(Susswein et al., 1976). In
Lymnaea, gut dilation activates the mechanosensory OM cells, which
inhibit modulatory and pattern-generating neurones and also activate radular
retractor motoneurones (Elliott and
Benjamin, 1989). In Pleurobranchaea, satiation causes
food stimuli to initiate withdrawal movements, in part because food stimuli
inhibit cerebral ganglion command-like neurones, instead of exciting them
(Davis and Gillette,
1978).
Other stimuli associated with feeding contribute to the patterning of
feeding into meals. In Aplysia, gut stimuli arising from the
consumption of small quantities of food facilitate feeding
(Susswein et al., 1984b),
before the inhibition begins as a result of filling the gut with larger
quantities of food. Feeding in Aplysia and Limax is also
patterned into meals by the build-up and decay of sensory adaptation, which
occur when the lips are stimulated with food
(Horn et al., 1999;
Reingold and Gelperin, 1980;
Schwarz et al., 1988). In
addition, satiation affects the ability to arouse an animal, and this effect
can contribute to the patterning of feeding into discrete meals
(Susswein et al., 1978).
Changes in haemolymph glucose concentration do not affect feeding in
Aplysia (Horn et al.,
1998).
Behavioural hierarchy
Classic studies in Pleurobranchaea examined the choice made by an
animal in response to simultaneously presented stimuli that elicit different
behaviours. Initially, these studies showed that behaviours are hierarchically
organized, with feeding dominant over other behaviours, such as mating,
withdrawal and righting (Davis et al.,
1974a). The inhibition of withdrawal by feeding is attributed to
the action of `corollary discharge' neurones, which convey information from
the buccal ganglia to the brain (Kovac and Davis,
1977,
1980a,
b). However, it was later
shown that feeding and withdrawal both modulate one another and are mutually
inhibitory (Kovac and Davis,
1980a,
b). Interestingly, food
stimuli continue to inhibit withdrawal even after the animals are satiated,
indicating that the stimuli causing satiation specifically modulate feeding
behaviour by modulating the reciprocal inhibition between feeding and
withdrawal (Davis et al.,
1977). The relatively dominant position of feeding in the
hierarchy can also be modified by hormonal control. For example, the release
of hormones inducing egg-laying inhibits feeding
(Davis et al., 1974b).
Aplysia, like Pleurobranchaea, displays mutual inhibition
between feeding and defensive behaviours. However, the mechanisms underlying
mutual inhibition differ. In Aplysia, mutual inhibition arises
because stimuli that elicit one class of behaviour inhibit the other. Thus,
noxious stimuli elicit withdrawal responses and also inhibit feeding
(Kupfermann and Pinsker,
1968). A blood-borne factor found in satiated animals also
inhibits withdrawal responses (Lukowiak,
1987). In addition, food stimuli inhibit withdrawal responses even
in the absence of ingestion of food or of feeding movements
(Advokat, 1980). By contrast,
in Pleurobranchaea, both food and noxious stimuli can elicit either
feeding or withdrawal responses. The specific response elicited depends on the
previous feeding history and on the strength of the stimulus
(Gillette et al., 2000). The
choice between feeding and withdrawal arises via inhibition of
withdrawal responses by specific motor elements in the feeding system (Jing
and Gillette, 1995,
2000) as well as via
inhibition of command-like neurones that initiate feeding by neurones that
initiate escape responses (Kovac and Davis,
1977,
1980a,
b).
In Clione, Helisoma and Lymnaea, a pleural interneurone
that has been suggested to be activated by stimuli that cause withdrawal
projects to the cerebral and buccal ganglia and inhibits the feeding system.
This may provide a partial explanation for the coordination of the feeding and
withdrawal behaviours (Murphy,
1990; Alania, 1995;
Alania et al., 1999,
2002).
Interaction with sexual behaviour
Feeding in Aplysia fasciata is strongly modulated by the animal's
sexual state. As in most grazing animals, a major proportion (up to 25%) of
the animal's time is budgeted to feeding
(Susswein et al., 1983).
A. fasciata spend an additional 25-50% of their time mating
(Susswein, 1984), leaving
little time for other activities. The large blocks of time spent mating and
feeding suggest that these behaviours may compete for the animals' time and
are mutually inhibitory. Removing food should then cause an increase in
mating, and removing mates should facilitate feeding. Removal of food indeed
causes increased mating (Nedvetzki et
al., 1998; Susswein,
1984). By contrast, isolation from potential mates inhibits
feeding, indicating that sexual stimuli facilitate feeding rather than
inhibiting it (Botzer et al.,
1991; Ziv et al.,
1989).
In Aplysia, conspecifics signal their presence via
peptide pheromones (Painter et al.,
1998; Susswein and Benny,
1985) that are sensed by the chemosensory rhinophores
(Levy et al., 1997), and the
presence of putative pheromones in the water at concentrations of
10-9 moll-1 facilitates both the appetitive and
consummatory components of feeding
(Blumberg and Susswein, 1998;
Blumberg et al., 1998).
Facilitation of appetitive behaviours occurs in part by exciting the neurone
C-PR (Teyke and Susswein,
1998). Thus, C-PR is a site of convergence in the control of
feeding by food and by pheromones. The seemingly paradoxical facilitation of
feeding by pheromones may be a mechanism for helping to synchronize mating
(Nedvetzki et al., 1998),
which occurs in large groups in which animals are constantly exchanging sexual
roles (animals can mate as males, as females or as both simultaneously) and
partners (Ziv et al., 1989).
If animals eat at times that should be devoted to mating, their mating
patterns would be severely disrupted. The facilitation of feeding by
pheromones in conditions of sexual arousal causes animals to eat vigorously
and effectively and, consequently, to become thoroughly satiated. Feeding will
then be relatively inhibited, allowing animals to devote the rest of the day
to effective mating, which is not impeded by feeding.
Feedback as a result of feeding movements
The nature of feeding movements changes as a result of feedback. In
Aplysia, radula mechanoafferents can switch movements from being
bite-like to being more similar to swallowing. In addition, increasing the
resistance against which animals must pull induces animals to cut the food
instead of swallowing it (Hurwitz and
Susswein, 1992). In Limax, the load on the radula is
monitored by the medial tooth. An increase in load causes a decrease in bite
rate (Reingold and Gelperin,
1980).
|
Modulation of feeding by learning and memory |
|---|
|
TOPSummaryIntroductionStructure of the feeding...Feeding movementsNeural circuitry organizing...Modulation of feeding movements...Modulation of feeding by...Concluding remarks: why are...References |
|---|
).
A later study demonstrated inhibition of locomotion towards a food odour if
ingestion of the food had been paired with a bitter taste
(Sahley et al., 1981a). Using
this learning paradigm, it was possible to show that a variety of phenomena
affecting learning in vertebrates (second-order conditioning, blocking and the
effect of pre-exposure to the unconditioned stimulus, UCS) also affect
odour-learning in Limax (Sahley
et al., 1981b). Later studies developed an appetitive conditioning
paradigm in which the responses to an initially aversive odour were increased
by pairing the odour with an attractive taste
(Sahley et al., 1990). Neural
correlates of learned inhibition of feeding are retained in a reduced
preparation (Gelperin and Culligan,
1984). In addition, a reduced preparation can be trained
(Culligan and Gelperin, 1983).
Since the primary mechanism of learning seems to be a change in processing of
an odour stimulus, subsequent studies have focused on the effects of training
on odour processing (e.g. Teyke et al.,
2000).
An important study has shown that separable memory processes follow learned
inhibition of feeding in Limax
(Yamada et al., 1992).
Long-term memory can be disrupted by cooling before the memory is
consolidated. For approximately 1 week after memory consolidation, the ability
to disrupt the memory by cooling can be reactivated by exposure to the food
conditioned stimulus (CS). A similar ability to disrupt memory only when it is
re-activated has been reported in mammals
(Nader et al., 2000). In a
later stage of memory, cooling can no longer disrupt memory even after it has
been reactivated (Yamada et al.,
1992).
Another early study showed that pairing food with intense, prolonged shock
in Pleurobranchaea causes the animals subsequently to withdraw from
the food instead of eating it (Mpitsos et
al., 1978). Studies examining the effects of differential training
showed that the training is moderately specific to the taste of the food
stimulus paired with the shock (Davis et
al., 1980; Mpitsos and Cohan
1986a
