ERIC EJ872843: A Paradigm for Operant Conditioning in Blow Flies ("Phormia Terrae Novae" Robineau-Desvoidy, 1830)

1.2 MB·English

by  ERIC

JOURNALOFTHEEXPERIMENTALANALYSISOFBEHAVIOR 2010,93,81–89 NUMBER1(JANUARY)
A PARADIGM FOR OPERANT CONDITIONING IN BLOW FLIES
(PHORMIA TERRAE NOVAE ROBINEAU-DESVOIDY, 1830)
MICHEL B. C. SOKOLOWSKI1, GE´RALD DISMA1, AND CHARLES I. ABRAMSON2
1UNIVERSITE´ DEPICARDIE-JULESVERNE
2OKLAHOMASTATEUNIVERSITY,STILLWATER
Anoperantconditioning situationfor the blow fly (Protophormia terrae novae) is described.Individual
fliesaretrainedtoenterandreenteraholeastheoperantresponse.Onlyafewsessionsofcontingent
reinforcement are required to increase response rates. When the response is no longer followed by
food,therateofenteringtheholedecreases.Controlproceduresrevealedthatrateofrespondingisnot
asimpleoverallresultoffeedingorofaging.Thefliesenteredintotheholeonlyiftheresponsewas
requiredtoobtainthefood.
Keywords: associativelearning,operantconditioning,blowflies,apparatus
_______________________________________________________________________________
The majority of studies on learning in previously include mazes (Bicker & Spatz,
dipterans have been done in the context of 1976; Fukushi, 1985, 1989), shuttle boxes
classical conditioning of proboscis extension (Diegelmann, Zars, & Zars, 2006; Leeming,
where one or more pairings of a conditioned 1985; Leeming & Little, 1977; Putz & Heisen-
stimulus (CS) with an unconditioned stimulus berg, 2002; Wustmann, Rein, Wolf, & Heisen-
(US)subsequentlyleadstoanextensionofthe berg, 1996) and situations where leg position
proboscis to the CS in anticipation of the US orforceexertedinstationaryflightispunished
(Chabaud, Devaud, Pham-Dele`gue, Preat & (Booker & Quinn, 1981; Brembs & Heisen-
Kaiser, 2006; Nelson, 1971). Work has also berg,2000;Gong,Xia,Liu,Feng,&Guo,1998;
been done on olfactory avoidance by pairing Mariath, 1985; Wolf & Heisenberg, 1991).
an odor with electric shock, this odor being Operant chambers are available for several
subsequently avoided by the flies (Tully & invertebrate species including crustaceans
Quinn,1985;Waddell&Quinn,2001).Species (Abramson & Feinman, 1990), stingless bees
of Musca, Drosophila and Phormia have all been (Pessotti, 1972), honey bees (Grossmann,
used as model systems to study various aspects 1973; Sigurdson, 1981), snails (Balaban &
of behavior including learning, memory (Da- Chase,1989),Aplysia(Downey&Jahan-Parwar,
vis, 2005; Fukushi, 1976, 1979; McGuire, 1972) and cockroaches (Rubadeau & Conrad,
1984), and motivation (Dethier, 1976). 1963). The only procedure we know where a
In contrast to classical conditioning, there dipteran used a behavior in an arbitrary way
are few studies of operant conditioning in was developed by Wolf, Voss, Hein and
dipterans (Brembs, 2003). Operant condition- Heisenberg (1992). In this study, a drosophila
ing would require the insect to operate some successfully controlled the angular position of
manipulandum or use a behavior in a new or avisualpanoramabychoosingtheorientation
arbitrarywaytoobtainreinforcement(Abram- of its posture.
son, 1994). The various techniques used Since the beginning of JEAB, most pub-
lished experimental articles about condition-
ing concerned a narrow list of species.
ThisresearchwassupportedbyagrantfromtheSocie´te´
Picardepourl’EtudeduComportementAnimal(http:// Figure 1 shows the range of species covered
speca.free.fr).Thisarticlewaswrittenduringthecomple- by the journal from 1958 to 2008. The vast
tionbythefirstauthorofaFulbrightscholarshipprogram majority of articles concern birds (97.4% of
at Oklahoma State University. Thanks to Franc¸ois Ton-
these were pigeons), rodents (97% were rats),
neauandJohnKraftfortheirencouragement.Thanksto
humans, and various primates. These species
threereviewersfortheirhelpfulcomments.
AddresscorrespondancetoMichelSokolowski,Univer- make up 97.9% of the total published articles.
site´ de Picardie Jules Verne - Unite´ ‘‘Dynamiques des Mammals such as horses, cats, dogs or por-
Syste`mes Anthropise´s’’ (JE 2532), Dpt de Psychologie,
poises comprise 1.42% of the total articles,
CheminduThil,F-80025Amiens,Cedex1,France(e-mail:
fishes and reptiles 0.5% of the total articles,
[email protected]).
doi:10.1901/jeab.2010.93-81 and finally invertebrates 0.13% of the total
81
82 MICHEL B. C. SOKOLOWSKI et al.
Fig. 1. RangeofspeciescoveredbyJEABfrom1958to2008.Speciesfrom5successiveyearshavebeencombined.
Onlyempiricalarticleswithdatahavebeenconsideredintheanalysis.
articles. Despite the importance of insects in constructed from transparent plastic kitchen
the animal kingdom and what they can tell us boxes (‘‘Mepal moduul’’ 320 ml, 12.5 cm 3
abouttheevolutionoflearning,wefoundonly 7.6 cm 3 6.3 cm) with the inside dimensions
two articles with insects, one with the honey reduced to 3 cm 3 4.5 cm 3 12 cm with two
bee (Grossman, 1973) and the other with horizontal partitions. Twenty-four 2-mm diam-
cockroaches(Rubadeau&Conrad,1963).The eter holes were drilled in either side of the
cockroach article contained no data on which cage for air circulation.
to evaluate its effectiveness. The home cage also served as the experi-
The present article describes an operant mental chamber. The subject remained in the
conditioning paradigm developed for an home cage throughout the remainder of its
invertebrate, the blow fly Protophormia terrae life.Whenthecageswerenotconnectedtothe
novae. An individual blow fly enters a small training apparatus they were stored between
hole to receive food. We decided to focus our 20and25uC.Becauseyoungadultsdonotfeed
attention on P. terrae novae because of its before2daysold,theexperimentbeganwhen
importance as a myiasis pest of livestock such the flies were 3 days old. The flies stayed alive
as sheep (Wall & Shearer, 1997) and its use as for approximately 2 weeks.
an object for life history studies (Collatz,
1997). We were also interested in whether Apparatus
lawful data can be obtained from a traditional Figure 2 provides an overview of the appa-
operant situation using a nontraditional or- ratus. The experimental chamber with its
ganism. We were aided in our design by the associated circuitry is shown on the left with
large size of P. terrae novae that can approach the 5-ml glass syringe and stepper motor used
7–12 mminlengthandbythelargeamountof todeliversucrosereinforcementshownonthe
information on its natural history and feeding right. The experimental chamber is easily
preferences (Norris, 1965; Whitworth, 2006). connected to, and removed from, the rein-
forcement mechanism with two brass screws.
Circuit diagrams are not provided in this
METHOD
articlebecausetheyarestandardcircuitsused,
Subjects
for example, to detect when an infrared light
Six adult blow flies (Protophormia terrae beam is broken and to turn on various lights
novae), were reared from maggots obtained and the stepper motor.
from a local supplier. When the larvae The operant response consisted of moving
pupated,theywereplacedindividuallyintheir in and out of a 7-mm hole. The hole was
own ‘‘home cage.’’ The home cage was created from a larger hole 1.3 cm diameter 3
A PARADIGM FOR OPERANT CONDITIONING IN BLOW FLIES 83
Fig. 2. Photographoftheexperimentaldevice.Aplasticboxcontainingthefly(totheleft)isscrewedtoastepping
motormechanismlinkedtoaglasssyringe.Theboxwiththeflycanbeeasilyscrewedinplace.
1.5 cmlongwhichwasreducedtotherequired the 0.1-mm diameter needle of a 5-ml glass
size bytwoplasticplates.Therationalebehind syringe. The tip of the needle was cut to be
reducing the size was to allow the fly to enter flush with the bottom of the hole. After each
the hole only in the horizontal plane thereby session,theholewascleanedwithalcohol and
minimizingvariationsintopographythatcould water. The syringe was activated automatically
influence performance. Moving in and out of with a stepper motor controlled by ITC Com-
theholewasdetectedwithtwoinfraredemitter step and Powerstep interface connected to a
and detector pairs (Honeywell SEP8736 and 486DX2-50 PC computer through the printer
SDP8436). The two infrared lights were posi- port. The software was written in Borland
tionedin theform of a cross to ensure that all Pascal (MS DOS).
entrancesintotheholeweredetected.
Entryinto theholewassignalled with twelve Procedure
1.8-mm diameter light emitting diodes (six Sessionswereconducteddailyforeachfly.A
yellow and six green, in alternation) placed session began by carrying a subject’s home
equaldistancearoundthecircumferenceofthe container to the conditioning device and
circle(2.5 cmdiameter,seeFigure 3).Oneach screwing it in place. Figure 4 shows the home
sideofthecircle,sevenlinesofsix5-mmlight- cage connected to the training device. Each
emittingdiodeswerearrangedinalternationof animal received one session per day through-
green and yellow (but not used in this out its lifetime. Each session ended after 15
experiment). The purpose of the lights was to responses or 1 hr. Our principal purpose in
provide discriminative stimuli. Figure 3 shows limiting the session length was to obtain some
theresponseholeanddiscriminativestimuli. baselinedataonthelongevityoftheflieswhen
The reinforcer was 0.086 ml of 5% sucrose confined to the apparatus and to collect data
solutiondeliveredatthebottomoftheholeby oncontinuousreinforcement(CRF)schedules
84 MICHEL B. C. SOKOLOWSKI et al.
Fig. 3. Photographof the hole that constitutes the operant response. Note the two plastic plates that restrict the
orientationintothehole.Entryintotheholeisdetectedbyphotocells.Twelvelight-emittingdiodes(yellowandgreen)
arearrangedaroundtheholeandserveasdiscriminativestimuli.
that can be used later for experiments on alternated the phase every 3 days. We used
schedules of reinforcement. A session began twoadditionalcontrolflies(F1andF2),which
by turning on the yellow and green lights that remained under baseline conditions through-
were positioned around the response hole. out their life. The rationale behind the use of
When the animal entered the hole the lights thesetwoanimalswastodetermineifentering
were turned off. theholeincreasedintheabsenceofreinforce-
In operant conditioning studies it is stan- ment and as the fly ages.
dard practice to study a few animals over a Phase A consisted of the baseline condition.
long period of time (Sidman,1960).This type During this phase, each entrance to the hole
of design focuses on a detailed analysis of an activatedthesyringe,butitwasnotfilled,andso
individual’s behavior, and is the most popular the fly received the same amount of vibration
design in operant conditioning. We used an from the stepper motor as in phase B, but
ABdesignwithtwoflies(fliesF3andF4),with withoutfood.Atthebeginningofthesessions,a
Acorrespondingtothebaselinelevelinwhich drop of 1.29 ml sucrose solution (equivalent to
each response was not followed by reinforce- thetotal amount received per sessioninphase
ment, and B corresponding to the condition- B)wasmanuallyputinsidetheboxatarandom
ing phase in which each response was rein- place.Asweknowthatsugarmayelicitwalking
forced. For flies F3 and F4, we stayed 6 days at (Dethier,1957),thegoalofthisprocedurewas
the baseline level before switching to the B tomeasuretherateofholeenteringelicitedby
phase, which continued until the fly died. For sucrose solution alone. The yellow and green
two other flies (F5 and F6), we used an ABA lights were on except during a 3-s timeout
design. For fly F5, the first two phases were followingeachexitfromthehole.
performed over 6 days, with one day devoted During phase B, each access to the hole was
to a return to baseline. For fly F6, we followedbyareinforcer(CRFschedule).After
A PARADIGM FOR OPERANT CONDITIONING IN BLOW FLIES 85
Fig. 4. A photographoftheflychamberconnectedtooperantdevice.
the reinforcer was consumed, and the fly which substantially increased during the sec-
backed out of the hole, a 3-s time-out (yellow ond phase of the experiment when food was
and green lights off) was scheduled with no contingent upon entering the hole. Note that
responses being reinforced. This procedure the change appeared only after several ses-
was instigated to prevent small movements of sions, suggesting that the contingency took
the fly being recorded as a response. In some time to be effective. Whether this was
addition, the delay had the benefit of requir- due to some inhibitory conditioning learned
ing the animal to back out and then reenter during the first phase is not known at this
theholetherebyprovidingresponsefeedback. time.Asthecontingentreinforcementsessions
Following the training session no additional continued, the rate of responding increased
food or water was provided. until the end of the animal’s life.
Two alternative explanations other than the
effect of reinforcement for the increase in
RESULTS AND DISCUSSION
responding observed during the contingent
Figure 5 shows the rate of hole entering for condition are that 1) as the fly ages its hole
two flies that received no reinforcement for entering behavior increases as a result of
entering the hole during the first phase but maturation and 2) hole entering behavior
whose hole entry was reinforced during the increases as a result of sucrose stimulation
secondphaseoftraining(i.e.,ABdesign).The per se. Figure 6 shows the results for flies F1
twofliesshowedsimilarpatternsofbehavior.A and F2 who were only exposed to the baseline
very low rate of responding was observed condition. No systematic or substantial in-
during the unreinforced baseline condition, crease in response rate was observed during
86 MICHEL B. C. SOKOLOWSKI et al.
Fig. 5. Response rate (responses/min) as a function Fig. 6. Response rate (responses/min) as a function
ofexperimentalsessionsfor2fliesF3andF4involvedin ofexperimentalsessionsforthe2controlfliesF1andF2.
the AB design. The vertical dotted line shows the switch Noreinforcerwasgiventotheseflies(baselinecondition
from the baseline level (‘‘A’’, open circles) to the writtenas‘‘A’’).F1remainedalivefor10consecutivedays,
continuousreinforcementschedule(‘‘B’’,closedcircles). andF2for16days.
These2fliesworkedfor14consecutivedays.
the lifetime of these subjects nor did hole withineachcondition.Thisneededtobedone
entering increase with repeated consumption becausethelifespanoftheblowflyisshortand
of sugar solution. F1 showed a small increase wehadnowayofpredictinghowmanysessions
from session 1 to session 10, but it was not could be conducted, or conditions employed,
comparable to the large one observed with before an individual fly died. Figure 7 shows
experimental flies when the response was the performance of fly F6 across conditions.
reinforced. Contrary to F1, F2 showed a Althoughtheresponseratewaslowduringthe
regulardecreaseinresponserate.Thehighest first contingent phase (B), it was reduced
rate was obtained the second day, and a zero furtherbyextinction(A)andincreasedduring
rate was obtained after 12 days. the second contingent condition (B).
Inorder toobtain some information on the It has been suggested that the small brain
effect of extinction, we returned a fly to the and short life span precludes insects from
baseline condition following contingent rein- learning a wide range of behavior (Dethier,
forcement (i.e., ABA design). Figure 7 shows 1962; Mayr, 1974). Our data show that
that the behavior of fly F5 was similar to the dipterans are capable of a wider range of
behavior of flies F3 and F4 that received a learned behavior than previously demonstrat-
baseline condition followed by contingent ed (Brembs, 2003; Dukas, 2008). The devel-
reinforcement. When fly F5 was returned to opment of an operant conditioning paradigm
the baseline condition its rate of entering the for Protophormia terrae novae is the first step to
hole decreased. Unfortunately, fly F5 died quantitativelystudy operant conditioning phe-
after only one extinction session. nomena in this economically important spe-
To gather additional data on the effect of cies and opens a promising field for compar-
extinction we reduced the number of sessions ative investigations on learning phenomena
A PARADIGM FOR OPERANT CONDITIONING IN BLOW FLIES 87
sumed by fliespersession intheexperimental
condition (phase B). Although this procedure
provides equal access to the solution across
experimental and control phases, it does not
exactly reproduce the periodic access to the
reinforcer in the experimental condition. The
possibility that hole entering might be a
byproduct of periodic consumption cannot
be completely ruled out. A yoked control
could be used, but as Church (1964) has
shown, the comparison of different subjects
canbeasourceofadditionalproblemsifthere
are individual differences in the effectiveness
of the reinforcer to elicit the response. A
better control procedure may consist of
providing the fly with a choice between two
holes, only one providing reinforcement, with
the response rate expected to be higher for
the active hole. However, this procedure
requires substantial changes in the hardware
and software. As our preliminary data are
encouraging, these developments will be the
next goal in our fly learning analysis.
Contrary to most dipteran instrumental
Fig. 7. Response rate (responses/min) as a function conditioning studies where negative reinforce-
ofexperimentalsessionsforthe2fliesF5andF6involved ment or punishment procedures are common
in the ABA design. The dotted vertical line shows the (Booker&Quinn,1981;Brembs&Heisenberg,
switch to the next condition (Baseline, open circles,
2000; Gongetal.,1998; Mariath, 1985; Wolf &
written as ‘‘A’’ or CRF, closedcircles, written as ‘‘B’’).F5
Heisenberg, 1991), we used positive reinforce-
stayed 6 days in each condition before a switch, and F6
only3daysbeforeachangeinreinforcerdelivery. mentwithsucroseasthereinforcer.Ouruseof
a nutritional positive reinforcer suggests that
life history studies using operant conditioning
traditionally studied using operant methodol- can now be performed with the blow fly.
ogy (Skinner, 1956; Staddon & Cerutti, 2003). Operant learning with food reinforcement
The apparatus functioned very well. Only a may increase food consumption and fitness
few sessions ofcontingent reinforcementwere butatacostrelativetoenergyconsumptionand
required to increase response rates. When the neural activity. Such a cost produced by an
responsenolongerproducedsucrose,therate abilitytolearnmayironicallydecreaselifespan
of entering the hole decreased. Moreover, (Laughlin, 2001; Mery & Kawecki, 2004). It is
within the individual chambers serving also as knownthatmatingshortensthelifespaninflies
conditioning boxes, we were able to detect and the question naturally arises whether
these changes in individual behavior (Dunlap, learned behavior also influences life history
1935) without any direct manipulation of the traits (Collatz & Wilps, 1985). Since it is
flies. As the control flies revealed, rate of relatively easy to study the behavior of a fly
responding was not a simple overall result of duringitslifetime,ourapparatusalsoopensthe
feedingorofaging.Thefliesenteredthehole doortonewstudiesoflifehistorytrade-offs.
only if the response was required to get the Finally, as Phormia have been used for a
food. numberofyearsasamodelinsectforthestudy
However,atthisstageofresearch,thesefirst of aging (Collatz, 1997) our situation is ideal
results need to be considered carefully. At the for such studies because now it is possible to
beginning of the session during the control study the maintenance of learned behavior
phase (phase A) we gave in the chamber, but (and specially of operant behavior) through-
outside the response hole, an amount of out its aging process (Fresquet & Medioni,
sucrose equivalent to the total amount con- 1993).
88 MICHEL B. C. SOKOLOWSKI et al.
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