Studies of Behavioral State in Aplysia

7 Pages·1991·3 MB·English

by  I Kupfermann

Reference: Biol. Bull. 180: 262-268. (April,
Studies of Behavioral State in Aplysia
IRVING KUPFERMANN, THOMAS TEYKE, STEVEN C. ROSEN,
AND KLAUDIUSZ R. WEISS*
CenterforNeurobialogy and Behavior, Columbia University College ofPhysicians andSurgeons:
New York State Psychiatric Institute: and *Department ofPhysiology and Biophysics.
Aft. Sinai School ofMedicine, New York, New York
Abstract. This paper reviews a series ofstudies on the For many years, studies that were difficult or impossible
neural organization and the cellular mechanisms under- in vertebrates could be approached by investigating the
lying behavioral states; in these studies, feeding behavior squid giant axon and the large somata ofgastropod neu-
inAplysiawasusedasamodel system. FeedinginAplysia rons. In recent years, the use ofcell culture, brain slices,
has similarities to motivated behaviors in other animals and othermethodologies hasmade itpossibletodo many
and is modulated by a number ofinteresting state vari- types ofcellular studies on vertebrate neurons that could
ables, including arousal. Food-induced arousal manifests previously be done only in mollusks. However, it is still
itselfin two categories offeeding behavior: (1) appetitive verydifficult to study the integrative functions ofthe ver-
responses(e.g.. head-up feeding posture and directed head tebrate nervous system and to relate cellular processes to
turning),whichorienttheanimal topotentialgoalobjects behavior. Forthis reason, the presence ofa relatively few
such as food; and (2) consummatory responses (biting, neurons in gastropod mollusks has assumed increased
swallowing), which obtain the goal object. The consum- importance.
matory responses are rhythmic and relatively stereotyped, We have been studying the marine mollusk Aplysia in
whereas the appetitive responses are highly variable. Our order to understand the neural organization and the cel-
evidence suggests that one consummatory response, bit- lular mechanisms underlying behavioral states. We have
ing, appears to be controlled by command elements in concentratedon feedingbehaviorbecauseourearlystudies
the cerebral-ganglion, such as neuron CBI-2, which are indicated that the feeding responses ofthese animals are
capable ofdriving the behavior. One component ofthe modulated by a number ofinteresting state variables, in-
appetitive behavior, head lifting, may be controlled (at cluding arousal and satiation (Kupfermann el a/., 1982;
least in part) by another cerebral neuron, C-PR. C-PR, Susswein etai, 1978). This paperisa reviewofourwork.
however, affects numerous systems in the animal, but all It emphasizes studies ofthe appetitive aspects offeeding,
the systems affected seem to be involved in the food-in- and is not meant to be a general review of feeding in
duced arousal state ofthe animal. We postulate that C- Aplysia.
PR is, insomeways,analogoustocommand neuronsthat
evoke behaviors. The C-PR, however, not only evokes a Feeding Behavior in Aplysia has Similarities to
behavior, but also evokes a central motive state which Motivated Behaviors in Other Animals
aids in insuring that behavior is efficiently expressed. To provide themselveswith adequate nutrients,Aplysia
has many ofthe same problems faced by most other an-
Introduction
imals. They must detect and locate appropriate food
Mollusks have long been used for studies that are de- sources. They mustapproach the food andorient ittothe
signed to investigate general neurobiological principles buccal orifice. They must then biteand swallowthe food.
rather than the details ofa single species. One important Finally, when a sufficient amount has been consumed,
advantage ofmollusks is the large size oftheir neurons. they need to stop feeding. These operations must all be
carried out in a mannerthat isefficient intimeandenergy
Received 7 August 1990;accepted6 November 1990. expenditure. One ofthe meansby which theanimals im-
262
STUDIES OF BEHAVIORAL STATE IN APLYSIA 263
too-
80-
\
Figure 1. Aplysiainthefeedingposture. Inthispositiontheanimal
showsdirected turningresponsestoseaweedapplied to the head.
prove the efficiency of their behavior is by regulating it
accordingtoparticularinternalstates. Theseinternalstates
are modulated byexternal and internal stimuli and by an
internal endogenous process associated with a circadian
activity rhythm. In higher animals, the constellation of
state variablesthat regulate feedingaretermed "hunger,"
and byanalogy, ahunger-like statealsoappearsto regulate
feedinginAplysia. Asin higheranimals, feedinginAplysia
isgreatlypotentiatedbypre-exposingtheanimalstofood;
i.e.. the animal exhibits incentive motivation. When a
quiescent Aplysia is first stimulated with seaweed, it be-
comesactivated aftera relatively longdelay(uptoa min-
Figure 2. Vectors indicating the magnitude and direction that the
headturnsin responsetotactilestimulibrieflypresented(open loop)to
different pointson therhinophoresandtentacles. The movementsturn
theheadinthedirectionofthestimulus. Intheopenloopcondition the
animal greatly overshoots the stimulus. If, however, the stimulus is
maintainedin place(closedloop),whentheanimalbeginstheresponse,
themovementisrepresentedbytheindicatedvectors,butastheanimal
turns,theresponseprogressivelydecreasesinmagnitudesothatthemouth
comes to be accurately centered over the stimulus. Data from Teyke
elal (1990b)
264 I. KUPFERMANN F.T Al.
BMN IlILllliLL
U ILL
B16 JJJIJJJJIIJUJU
C12
JlO mV
10
i
Figure 4. Example ofthemotorprogram dnven by CBI-2. CBI-2 was fired byaconstantdepolarizing
current (dark horizontal line). The rhythmic program incorporated neurons in the cerebral and buccal
ganglia. The buccal program is reflected in the activity ofan identified ARC muscle motor neuron. B16.
Another buccal motor neuron. BMN. illustrates that the program is present in numerous other buccal
neurons. CI2 is a cerebral ganglion neuron that controls movements ofthe lips, and it is one ofseveral
cerebral neuronsthatisrecruitedbythebuccal program that isdrivenbyCBI-2. CBI-2alsoshowsperiodic
synapticinputdrivenbythebuccalprogram.NotethatwhenCBI-2stopsfiring,theprogrambrieflypersists
andthen terminates. Thedataarefrom Rosen el al. (1987. 1988).
distance ofthestimulus from the mouth. If, however, the cal mass. The forward position is maintained during the
stimulusis maintained in position sothat it providescon- whole meal. (2)Thewholebuccal mass undergoesforward
tinuous feedbackduringthe movement (closedloop), the and backward movements. These movements occur on
food is accurately centered over the mouth (Teyke et al., a background ofthe maintained forward movement. (3)
1990b). Seaweed provides the animal with two distinct The radula rotates forward and backward. (4)The radula
types of stimuli: tactile and chemical. Surprisingly, the halves open and close. The latter two movements cause
stimulus that results in the animal turning toward the thefoodtobegraspedanddepositedintothebuccalcavity.
foodisthetactilecomponent. A purelychemical stimulus, The relativelysmall backward movement, which deposits
provided by an aqueous extract of seaweed, is not very the food in the buccal cavity during biting behavior, can
effective in eliciting turning. On the other hand, if the be distinguished from a larger backward movement
animal is first aroused with a chemical stimulus, a purely (swallowing) that is triggered by the presence offood in
tactile stimulus (provided by a glass rod) very effectively the buccal cavity, and which results in the food being
evokesaturningresponse. If, however, thetactilestimulus moved into the esophagus (Kupfermann. 1974). Biting
is repeated without intermittent chemical stimulation, the movements, which are elicited by food contacting the
turning response habituates until no response at all is perioral zone, thus consist ofa large forward component
evoked (Fig. 3). Thus, the chemical component of the of the radula. followed by a relatively small backward
seaweed maintains the arousal level ofthe animal, while movement. Swallowing, which is elicited by food in the
the tactile component directs the response. buccalcavity,consistsofarelativelysmall forward move-
When the animal turns toward the stimulus, contact ment and a large backward movement. The swallowing
with food to the region immediately around the mouth movementsareassociatedwith an inhibition ofthebiting
(perioral zone) initiates consummatory behaviors and a movements; i.e.. as long as food is present in the buccal
new set ofarousal responses. The consummatory arousal cavity, stimulation ofthe perioral zone neverelicitsalarge
is characterized by a progressive build-up ofthe rate and forward movement ofthe radula.
magnitude of the rhythmic biting response that occurs
when foodtouchestheperioral zone(Kupfermann, 1974; Biting Responses are Elicited by the Activity of
Weiss et al., 1982). Whereas the appetitive feeding re- Individual Neurons Located in the Cerebral Ganglion
sponses are highly variable, the consummatory biting re-
sponse is morestereotyped, although itconsistsofseveral In a number ofspecies, including gastropod mollusks,
components (Kupfermann, 1974; Weiss et al.. 1986): (1) stereotyped responses are elicited by the activity ofindi-
Thereisa forward movement (cocking)ofthewholebuc- vidual cells or small groups of cells (Kupfermann and
STUDIES OF BEHAVIORAL STATE IN APLYSIA 265
A Postural System B Consummatory System duced a robust and reliable rhythmic motor program of
the buccal ganglion (Fig. 4) (Rosen el al.. 1987). CBI-2
receives chemosensory input from the perioral zone. In
CBI-2 addition, when itelicitsabuccal motorprogram itreceives
rhythmic synaptic input from the buccal ganglion, and
MCC thus it fires in phase with the buccal motor program. If,
however, the synaptic feedback from the buccal ganglion
is blocked by placing the cerebral ganglion in seawater
CPR containing cobalt ions, the firing of CBI-2 still evokes
rhythmic activity in the buccal ganglion, in the absence
CPR ofrhythmic activity in CBI-2 (Rosen et al., 1988). For a
discussion ofrecentwork on thecentral patterngenerating
circuitry intrinsic to the buccal ganglion ofAplysia, see
Cardiovascular System D Defensive Systems Kirk(1989), NagahamaandTakata(1989),andSusswein
and Byrne (1988).
Usingasemi-intactpreparation,wefoundthatthefiring
L10 Bncell ofCBI-2 can evoke rhythmic movements ofthe buccal
mass and radula, and the movements are similar to the
repetitive biting responses seen in the intact animal. The
responses do not resemble swallowing or rejection. The
firing of two other cerebral to buccal interneurons also
evokescoordinatedbuccalganglionactivity, butthemotor
programs are different for each ofthe CBIs. Thus we hy-
pothesize that the CBIs in Aplysia, as in othergastropods
OPR CPR (Gillette et al., 1982; Benjamin and Elliott, 1989; Mc-
Crohan and Kyriakides, 1989; Delaney and Gelperin,
Figure 5. The various effects of firing C-PR on different systems 1990), may constitute a command system, the conjoint
associated with food-induced arousal. Foreach experiment, C-PR was
intracellularlystimulatedat20Hzfor5s.Forillustrativepurposes,mul- activity ofwhich drives consummatory feeding responses.
tiplefollowercellsoftheC-PRareshownforeachpartofthefigure,but
the data foreach trace were obtained in separate experiments. (A) Ex- Activity ofan Identified Cerebral Neuron Appears to
tahmaptlemsayofbtehepaerftfecotfstohfefpiorisntgurCa-lPcRonotnrodlifsfyesrteentm.pe(dBa)lEgffaencgtlsioonfCne-uPrRonosn, Elicit Elements ofAppetitive Arousal
cerebralganglionneuronsthatcontrolconsummatory feedingresponses
(biting command element, CBI-2, and the modulatory neuron, meta- Although stereotyped consummatory responses are
cerebralcell,MCC).(C)EffectsofC-PRonabdominalganglionneurons driven by a relatively few command-like elements, it is
that control the cardiovascular system (command element LIO. heart difficulttoimagine howthe highlyvariable responsesthat
exciterRBHE,andvasoconstrictorLBVC.(D)EffectsofC-PRonvarious constitute appetitive behavior could be similarly driven
neuronsthatparticipateindefensiveresponses[headwithdrawal neuron, by a small number ofneurons. Nevertheless, we set out
sBencrceetllio(nTenyekueroenlsa,l..R2198a9n)d;gPiLl1l]w,itChadlribarwaatliomno:to2rs,ne2u0romnVs,,Le7x;cedpetfe5nsmivVe to determine whether the nervous system contains neu-
forcellsR2 and PL1 in part D. Dataare from Teyke clal. (1990a). ronsthat can evoke appetitive feedingbehavior. Backfills
ofthe cerebral-pedal connectives revealed a small subset
ofcerebral ganglion neurons that send their axons to the
Weiss, 1978; Gillette el al, 1982; McClellan, 1986; Ben- pedal or pleural ganglia (Teyke et al., 1990a). The firing
jamin and Elliott, 1989; McCrohan and Kyriakides, 1989; ofthese neuronsrevealed asingle(bilateral)cerebral neu-
Delaney and Gelperin, 1990). To determine the critical ron that can influence the activity ofnumerous neurons
control elements forthe consummatory phase offeeding in theabdominal, pedal, andcerebralganglia. Wetermed
inAplyxia, we back-filled thecerebral-buccal connectives this neuron the cerebral to pedal regulator [to avoid con-
and located a population ofcerebral neurons that send fusion with the caudal photoreceptor (CPR) interneuron
their axons to the buccal ganglion. Several ofthese cells of crayfish, we abbreviate this neuron C-PR, although
hadbeen previously identified, includingthe serotonergic previously we did not use the hyphen].
metacerebral cells (MCCs) and ICBM mechanosensory The pedal ganglion in particularcontainsa large num-
cells (Rosen et al.. 1989a,b). In addition, two small pop- berofneuronsthatareexcitedbyC-PR(Fig. 5).Asmaller
ulations ofcells were found in anterior and lateral posi- number of pedal ganglion neurons are inhibited by C-
tions. Firing ofone ofthe cells (cerebral to buccal inter- PR. EachneuronthatisaffectedbyC-PRactivityreceives
neuron two, or CBI-2) within the anterior cluster, pro- input following the firing ofeitherthe left or right C-PR,
266 KUPFERMANN ET AL
I.
OPR
MCC
Figure6. ExampleofaprolongedexcitatoryresponseinC-PRandtheMCCtoabriefseaweedstimulus.
Calibration: 5 s, 20 mV. Datafrom Teykeetal. (1990a).
suggesting that C-PR is probably not directly involved in animal liftsits head intothe feedingposture(Teykeetal.,
thedirected head turningresponse, which isvery strongly 1990c). Thus, the total complex ofappetitive feeding re-
lateralized. Nevertheless, headturningdoesnotoccurun- sponses may consist of two components: a stereotyped
lessthe animal is first aroused, so that C-PR activity may postural head-lifting response anda more varied directed
enable head turning. Some of the effects of C-PR are turning response.
monosynaptic, whereas others are mediated by interneu- We have formulated a simple neural model (Teyke et
rons. Firing of many ofthe pedal cells that are affected a/.. 1990b) whose input-output functions are similar to
bytheactivityofC-PRcausesthe musclesoftheanterior- thebehavioral resultsconcerningthedirected headturning
dorsal region ofthe necktocontract(Teykeetal.. 1990a), component ofappetitive feeding behavior. The model is
which suggests that C-PR may evoke movements that based on reflex circuits and does not contain command
cause the head to be lifted into the feeding posture. Con- elements. By contrast, the head lifting response may be
sistent with a role ofC-PR in eliciting head-lifting in re- importantly controlled by a small number of neurons,
sponseto food, we found that seaweed appliedto theten- such asC-PR, that havecommand-like properties. C-PR,
taclesevokesstrongactivityinC-PR(Fig. 6). Furthermore, however, affectsresponsesotherthan head lifting. In fact,
preliminary studies involving extracellular recordings
fromthecerebral-pedalconnectives, supporttheideathat
B
C-PR is active just before and during the time that the
TIME (SEC)
Figure 7. Sequence ofmouth openings and closings during seven
repetitivebitingresponses, intwoanimalsthat havehadbilateralchronic
lesions (protease injected) ofthe MCCs. The sequence is based on a
videotaped analysisofbiting. Width ofthe mouth openingisexpressed
asa percentage ofthe maximum. A. An example, illustrating "stuck"
radula in a MCC lesioned animal, in which the radulastaysprotracted
foranabnormallylongduration. B. Responsesofanormalanimal(Bl),
and ofthesame animal (B2) following lesion ofthe MCCs. Data from
Rosen etal. (I989a).
STUDIES OF BEHAVIORAL STATE IN APLYSIA 267
20-- When C-PR isfiredat physiological rates, itsexcitatory
o
LJ effect on neurons involved in biting responses is never
l/l strong enough to drive the neurons at a rate sufficient to
15-- evoke biting. C-PR appears to function to increase the
aU:J D excitabilityofthese neuronswithoutdirectlydrivingcon-
summatory responses.
O3 10 By cutting various connectives we could localize the
MCC Lesion, Pre-Op ganglia that contain the interneurons that produce the
* MCC Lesion, Post-Op effects ofC-PR on the various non-postural systems. We
5-- D D Control, Pre-Op found that all oftheseeffectsare mediated by the activity
Q Q Control, Post-Op of the pedal-pleural ganglia. It may be significant that
these ganglia mediate the postural responses associated
012345678910111213
with food arousal. Thusappetitive arousal may involve a
SWALLOW NUMBER primary effect on a postural system, which, in turn, mod-
ulatestheactivityofthe numerousothersystemsthatwill
Figure9. MCClesion andcontrol groups mean interswallowinter- eventuallycomeintoplayduringfeeding. In thevertebrate
dvailfsf,ermeenacsesurweedredufnonungd.ingDeasttaionfroofmstRroipsseonfcsteailwlee(d1.98N9ao).significantgroup burlaaitni,oninodfeceodn,snceiuorusonnesstshaonudghatrotousbaelcaornecceornnceedntwriatthedregin-
thebrainstem in regionsintimatelyinvolvedwithpostural
we found that C-PR activity affects neurons involved in regulation (Hobson and Brazier, 1980). Because virtually
three other types of responses: defensive withdrawal re- all behaviors require a particular posture for their exe-
flexes (Fig. 5D), consummatory biting (Fig. 5B), and car- cution, the postural neural system may serve a primary
diovascular responses (Fig. 5C). The neurons involved in role in arousal in highly diverse species.
defensive responses were inhibited by the firing ofC-PR. Some ofthe effects ofC-PR, such as those on the ele-
and in semi-intact preparations we showed that the firing ments ofconsummatory responses, could enhance these
ofheadwithdrawal neuronsin responsetoastrongtactile responses. Other effects, such as those on Bn neurons,
stimulus to the head was reduced when the C-PR neuron maysuppressresponsesthatare incompatiblewith feeding
waspermitted to fire. The rapid depression ofwithdrawal behavior. We postulate that C-PR is, in some ways, anal-
responses following contact with seaweed may therefore ogoustocommand neurons, which evokebehaviors. The
be due either in part, or wholly, to an active inhibition, C-PR, however, notonlyevokesabehavior(head lifting),
ratherthan to low frequency depression, asappears to be butalsoevokesacentral motivestatethataidsin insuring
the case for habituation of the gill and siphon reflex to that behavior isefficiently expressed. A behavioral action
tactile stimulation (Castellucci el al, 1970). such as feeding is made up ofa number ofdifferent be-
Firing ofC-PR evokes complex mixtures ofexcitatory havioral acts(e.g., head lifting, biting, swallowing). Thus,
and inhibitory synaptic responses in abdominal ganglion aconsideration ofthewaysinwhich behavioralefficiency
neuronscontrollingthe heart and blood vessels(Fig. 5C). ismaximized raisestwofundamental questions. First, how
These effects could contribute to aspects ofcardiovascular are multiple responses ofthe organism coordinated with
responses that occur during food-induced arousal. one another, and second, how are the individual behav-
The cerebral ganglion neurons involved in consum- ioral acts which make up a behavioral action modulated
matory behaviors generally receive pure excitation when so as to optimize their speed and minimize energy ex-
C-PR is fired. These neurons include command-like ele- penditure? Our evidence suggests that one means ofco-
ments for biting (CBI-2) and the metacerebral cells ordinatingdiverse responsesdirected towardasinglegoal
(MCCs). The MCCs modulate the muscles and neurons is to affect diverse neuronal systems through the activity
that effectuate biting and account, in part, for the build- of a relatively few neuronal elements. Data presented
up ofthe speed and magnitude ofsuccessive bites, which elsewhere indicate that maximization ofthe efficiency of
occurs during consummatory arousal (Rosen el ai, individual responses is accomplished, in part, by the ac-
MCC
1989a). In contrast to the C-PR, the modulatory effects tivity ofsubordinate specialized neurons suchasthe
ofthe MCC are very restricted. It only modulates con- (Weiss et al.. 1978; Rosen et al.. 1989a). In addition, in-
summatory responses, and only the bite component. For dividual responses may be regulated by neuromodulators
example, ifthe MCCs are destroyed, there is no change thatoccurascotransmittersin motorneuronsinnervating
in thecapacitytoelicitthefeedingposture(Fig. 8)(Rosen themusclesthateffectuatefeedingresponses(Lloydeta!.,
et al., 1989a), but there is an increase in the bite latency 1985; Cropper et al., 1987a,b, 1988, 1990). The motor
and inter-bite intervals(Fig. 7, 8B). Inter-swallow intervals neurons are subordinate to the modulatory effects ofthe
are unchanged (Fig. 9). MCC, which, in turn, is modulated by C-PR. Thus the
268 I KUPFERMANN ET AL.
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