VOL. II, No.
3 SEPTEMBER, 1927
rTI
THE QUARTERLY
11 R\EVIEW
> T 11
of
ANIMAL BEHAVIOR AND INTERNAL DRIVES
O
BY CURT P. RICHTER
Psychobiological
Laboratory,
PhippsPsychiatric
Clinic,JohnsHopkinsUniversity
NE of themostfundamental
action. We believe,however,that spon-
of all the phenomenawhich
characterizeanimal life and
distinguish it from plant
life is the spontaneousmotilityof the
animalorganism. A fewplants,to be sure,
especiallycertainformsof marinevegeta-
tion, do move about, but these few are
exceptionsin the plant kingdom. The
activityof animals, on the other hand,
although it varies widely in form and
extentfromspeciesto species,is an ordi-
naryphenomenon whichone alwaysantici-
pates under normal circumstances. We
may ask, then,what it is that setsoffthe
diverseperformances which animals dis-
play. Ordinarilywe think of most of
their activityas being due to some form
of externalstimulation. We know, how-
ever, that all animals, fromthe lowest.
uni-cellularorganismto man, are active
even when all externalstimulihave been
eliminated. And since this spontaneous
motility,just as any otherkind of motil-
ity, must have a definitecause, it must
be due to some natural factor within
the organism. Many workershave cho-
sen to call it "voluntary" activity,pre-
sumably because of the common belief
that the "will" to do is the originof the
QUlAR. REV. BIOL., VOL. II, NO. 3
BIOLOGY
taneousactivityarisesfromcertainunder-
lying physiological origins. We shall
attemptto show fromstudieschieflyon
the white rat what some of these origins
are, and how they fit into the general
biological pictureof the animal's life.
The investigationsdescribedbelow have
been made by Ging H. Wang, Elaine F.
Kinder, Tomi Wada, and the present
writerin thePsychobiologicalLaboratory
ofthePhippsPsychiatricClinicduringthe
past six years. Some of the experiments
have alreadybeenreportedelsewhere,but
we have takenthis opportunity to collect
also numerousobservationsthat are as
yet unpublished. Of the extensivework
on animal "drives" done by Hoskins
(i92.5), Moss (I924), Slonaker (I924,
I92X5, I92.6), Stone (I92.4, I92.5, I92.6),
Szymanski(i92.0, i92.2.), and Tracy(i92.6)
we shall incorporatein this review only
that partwhich bearsdirectlyon our own
methodof approachor on our own experi-
mentalfindings.
PERIODIC NATURE OF SPONTANEOUS AC-
TIVITY-TWO-HOUR RHYTHM
We may begin our reviewwith the rat
confinedjust afterfeedingin a small cage
307
308 THE QUARTERLY REVIEW OF BIOLOGY

of the typeshownin figurei. The walls activitywithineach activeperiodis slight

and floorof the cage are absolutelybare
and the room in which the experimentis
performed is kept constantlyilluminated
and freefromall disquietingnoises and
odors. If we observe the animal for a
while we see that it moves about most of
the time, doing many things. It sniffs
and claws at the walls of the cage, it
climbs,and gnaws and scratches;but from
all these observations,however interest-
at the beginning,but increases as the
period advancesand reachesits maximum
usually near the end (Richter, I92vf2).
Typical recordsobtainedfromtwo rats in
triangularcages are shown in figure2.
The recordin figure3, obtained froma
guinea pig in the same type of cage, is
representativeof a similarrhythmfound
in otheranimals.
H ad the motility been irregularand

FIG. I. PHOTOGRAPH OF CAGE USED IN STUDYING GROSS BODILY ACTIVITY

The cage is triangularin shape, I. incheshigh and iX incheswide. Each corneris supportedon a rubber
tambourthroughwhich all movementsare transmitted to a recordingMareytambour. The timeis recorded
on the smokedpaperin halfhourintervalsby meansof an eightday clock.

ing at firstsight,we learnnothingofwhat non-periodic we shouldhave accomplished

makesit active. If, however,we arrange
the cage so that everymovementtherein,
even the slightest, is recorded over a
periodof tento twelvehourson a smoked
drum,a remarkablefact comes to light:
this diffusegross bodily activity occurs
rhythmically,active periods alternating
withperiodsofalmostcompletequiescence.
The active periods occur at intervals
varyingfromone to two hours. More-
over, the recordsshow furtherthat the
nothingin our investigationof its origin.
On the contrary,however,it is verysig-
nificantthat such well definedperiodsof
activity,recurringat such regularinter-
vals, are foundwhen externalconditions
are as nearly constant as is practically
possible. This fact would indicate that
the motilityrhythmmustbe set up from
within the animal in some organ which
functionsat a similar frequencyof one
and a half to two hours.
ANIMAL BEHAVIOR AND INTERNAL DRIVES 309

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HO

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3IO THE QUARTERLYREVIEW OF BIOLOGY
ORIGIN OF THE TWO-HOUR-ACTIVITY
A review of the periodicity of the
differentviscera,eliminates at once the
heart and lungs and the sex glands, since
the two formerorgansfunctionat a fre-
quency much higher and the latter at a
frequencymuch lower than that of the
bodily activityrhythm. In the stomach,
however, we know that active periods
alternatewith quiescent intervalsevery
hour and a half to two hours. In I904
Boldireffwas able to show that contrac-
tions occur in the walls of the empty
stomach,but severalyearselapsed before
FIG. 4. DIAGRAM SHOWING THE METHOD
Carlson (I9I6) demonstrated the periodic
natureof this activity. Carlson,working
with guinea pigs, dogs, and monkeys,
foundthat fromone to two hours aftera
meal, when the stomachis nearlyempty,
contractionwaves begin passing down-
ward over the stomach walls. These
waves, small at first,gradually become
largerand largeruntiltheyfinallyinvolve
the whole lower half of the organ, and
the gastricmusculatureoftenpasses into
a conditionof semi-tetanus.Then, quite
.uddenly, the contractionscease and an
inactive interval of an hour or more
ensues. Afterthis period of quiescence
the small waves begin again, and the
RHYTHM
entire process is repeated. Thus one
period follows another as long as the
stomachremainsempty.
Gastricmovementsin both animalsand
man have been studiedby means of the
apparatus shown in figure 4 (Martin
and Rogers, I927). A balloon attached
to the end of a tubeis passed throughthe
oesophagusinto the stomachand inflated,
and a manometeris fastenedto the other
end of the tube. The contractionsof the
stomach change the pressure on the
balloon, so that someof the air is pushed
up intothetube,and thelevel ofthewater
in the manometeris changed. As the
OF RECORDING THE HUNGER CONTRACTIONS OF THE EMPTY STOMACH
(Martinand Rogers,I927)
water rises and fallswith the contraction
waves, the movementis recordedby a
floatingpointer on a smoked drum. A
record obtained by this method with
similar apparatus is shown in figure5.
The recordwas taken in this laboratory
on a humanadultduringa nightofnormal
sleep. The portionpresented,-thatpor-
tion registeredbetween I1.30 and 2.30,
when the last meal had certainlybeen
assimilated,-illustratesvery clearly the
cyclic nature of the movementsof the
emptystomach.
Accordingto the recentobservationsof
Rogersand Martin(i9z6), the stomach
takes the shape shown in figure6 A at
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 3II

the heightof each of the single contrac-

CORRELATION BETWEEN THE TWO-HOUR
tionsnearthe end of the activeperiodand ACTIVITY RHYTHM AND THE HUNGER
that shown in figure6 B when it is
RESPONSE
inactiveand relaxed. With each of these
largewaves, then,we see that the lower In order to test this hypothesiswe
part of the stomach contractsto such recorded simultaneouslythe bodily ac-
an extent that the lumen practically tivity of the animal and the intervals
disappears,whereas the upper part may at which it sought food and ate. This
show a contractionwave nearthe middle.experimentwas performed in the type of
CannonandWashburn (I9i2) andCan- cage shown in figure7. The largercom-
non (I9i5) have shown that with these partmentwas simplythe usual triangular

FIG. 5. RECORD OF STOMACH CONTRACTIONS OF A HUMAN ADULT TAKEN DURING AN UNINTERRUPTED SLEEP

largecontractionsthe sensationof hunger

arises,and fromthe work of Rogers and
Martin we know that these "hunger" SSifbbwiLst ;-;.ZbwW

contractionsare set up in the lower third

1<<;~~~~~~~~~~~~~~~~~

FIG. 6. A. SHAPE OF THE STOMACH AT THE HEIGHT OF A

CONTRACTION WAVE. B. SHAPE OF THE RELAXED
STOMACH

(Roentgenographicobservationsby Rogers and

Martin, i92.6.)

of the stomach. The hungersensationis FIG- 7 PHOTOGRAPH OF COMBINED FoOD AND

not produceduntil the end of the active
periodis nearlyreached,when the waves
have becomeverylarge, but even thenit
increasesin intensityto someextentwith
the magnitudeof the contraction,and it
disappearsentirelywhen the contractions
cease. The inference, therefore,is quite
logical that the two-hour periodsof gross
bodily activityin the rat are associated
withperiodsofgastricmovement andhave
to do with the hunger responses of the
animal.
ACTIVITY CAGE
The two compartments are supportedon separate
sets of tamboursso that the activityin each is re
cordedseparately.
activity cage shown in figurei; the smaller
compartment contained a cup filled with
a powdered food mixture (McCollum
diet). The corners of each cage were
supported on rubber tambours and so
arranged that the activity in the two
cages was recorded separately. In this
way the curve in figure8 was obtained,
3I THE QUARTERLY REVIEW OF BIOLOGY

where the activity in the large cage is
registeredon the firstline,and that in the
food-box on the second, with the time
in hours below. It will be seen imme-
diatelythat the animal always entersthe
feeding-cageand eats once during each
approaches the food-box except to eat,
and that the vibrationsrecordedin the
activity cage for a short time after it
leaves the food-boxare producedalmost
entirelyby an extensive cleansing per-
formancewhich always follows feeding.

FIG. 8. RECORD SHOWING THE RELATION BETWEEN GROSS BODILY ACTIVITY AND FEEDING PERIODS

Activityin the largecage is givenon the upperline, and entrancesinto the food-boxon the lower. Time
in hoursis indicatedbelow therecord.

A1 i i i I
Time in hours

Activit

1t0MQCL,h contracotions

Acti vitj

Stomach contracQticn s

FIG. 9. SCHEMATIC REPRESENTATION OF THE RELATION BETWEEN PERIODS OF GROSS BODILY ACTIVITY AND STOMACH
CONTRACTIONS

A. Simpleactivitycage withoutfood. B. Double cage withfood

activityperiod,thatit entersusuallynear In theseexperiments the activityperiods,

the end of the period and rarelyat the
beginning,and that it does not enter
during a quiescent interval. Moreover,
we have foundthroughprolongedpersonal
observation,that an adult animal rarely
recurringinvariably with the entrance
into the food-box,are even moreregular
than theywere in the earlierwork when
no foodwas available. With this greater
regularity,the quiescent intervals are
 ANIMAL BEHAVIOR AND INTERNAL DRJVES
much longer, so that the lapse between
periods is three to fourhours instead of
one to two, as foundin the activitycage
with no food-box attached. The sig-
nificanceof the lengthenedintervalswill
be discussedbelow.
We may now attemptto show in more
detail how the grossbodily activity,the
feedinghabits, and the stomachcontrac-
tions seem to be correlated. The simul-
taneous records of activity and feeding
suggest that a close relationshipmust
exist betweenthe periodsobservedin the
simple activity cage and the hunger
"drive" of the animal. Fromthe experi-
mental data compiled above we know
thatthemotilityrhythmand the stomach
contractionrhythmhave three features
in common:the frequencyof both varies
between one and two hours; the active
phases of both begin at slight intensity
and increasegradually,reachinga maxi-
mumnearthe end; and in both the active
periodends abruptlyand is followedby a
quiescent interval. If we representthe
two rhythmsas in figureg A, drawinga
diagrammatic activity record directly
above a diagrammaticrecord of gastric
movement, so thatthe activephasesof the
two coincide, we find that the small
stomach contractions occur simultane-
ously with the beginningof the motility
period, and that as the magnitudeof the
contractionsincreasesthe animal becomes
more and more active. But how can we
justifyour representation in termsof the
hungerresponse? It is veryprobablethat
as long as the animal experiencesthe
hungersensationwhich accompaniesthe
stomach movements,it seeks for food,
unsuccessfully, ofcourse,in thesinglecage
without food-box. When the gastric
a firstplace. Furthermore,its throat is
contractionsstop, however, the hunger
disappearsand the animal becomesquiet
again.
On this basis one might expect that
3I3
when foodwas available all the time,the
rat would enterthe food-boxas soon as
the contractionsbegan. Actually, how-
ever,we know that it movesabout in the
main cage for some time beforeit ap-
proachesthe food-box. How, then, can
we explain this preliminarydiffuseac-
tivity? Here again, as in figureg A, the
relationshipmay be represented schemat-
ically. In figure g B, a record taken
simultaneously fromthe activitycage and
the food-boxis shown in diagramon the
firstand secondlines, and a stomachcon-
tractionrecordon the third. Thus we see
that the small contractionsgive rise to
thediffuse activityin thelargecage. The
animalseemsat firstsimplyto be annoyed
and becomes more and more restlessas
the contractionsgrow larger,until the
"'main" contractions setin and thegeneral
discomfortbecomes centralized in the
hunger sensation. This stimulus domi-
nates the behaviorof the organismand it
enters the food-box to eat. When its
appetitehas been satisfied,it passes into
a period of quiescencewhich lasts until
the stomachhas become emptyand the
contractionshave startedup again. And
since time is requiredforthe contentsof
the stomachto be digested,the interval
between contractionperiods is three to
fourhoursinsteadof one to two hoursas
observedin the earlierexperiments.
We had hopedto establishthisrelation-
ship in moredetail in the rat by meansof
recordstaken simultaneously of stomach
contractions and gross bodily activity,
but all of our attempts to introduce bal-
loons into the stomach of thisanimal were
unsuccessful. It is verydifficult to keep
it frombiting a hole in the tube in the
apparentlytoo small to admit even the
finest tube without a severe asphyxia
resulting. Because of this failure, we
turned our attention to other animals
3I4 THE QUARTERLY REVIEW OF BIOLOGY

fromwhich Carlson and his associates rat, but they are just as regular. The
had already obtained good records of cage used in these experimentswas cy-
stomachcontractions. lindricalin shape,two feetin diameterand
Since the stomach tube can be intro- three feet high. The circular bottom,
ducedand fastenedveryeasilyin the bull- made of cardboard,and small enough to
frog, we experimentedon this animal, fitinside the wire wall withouttouching
of Patterson
usingthe technique (i9i5). it at any point, was supportedon tam-
The tube and bulb were pushed into the boursso that all movements of thepigeon
stomachthrougha smallhole made in the were recorded on a smoked paper. A
skinbeneaththe throat,and the frogwas wooden rod pushedthroughthewirewall
placed in an activitycage enclosedin a half-wayup, pivotedon a nail at one end
box which could be almost completely and supportedon a tambourat the other,
darkened. Water from a faucet dripped servedas a perchfromwhichactivitycould
throughon the animalat all timesin order also be recorded. Figureio, a recordof the
to keepit in good condition. In thisway activityon thebottomof thecage whenno
food was available, shows that the bird
lefttheperchaboutonceeveryzo minutes;
and by attaching a recordingfood-box
filledwith corn,we foundthateverytime
it jumpeddown it invariablystoppedto
eat. Rogers (I9I6) has demonstrateda
thirty-minute averagerate for the active
periodof thecropof thepigeon,observing
at the same timethat it was mostrestless
when its crop was contracting. We at-
FIG. IO. RECORD
OF A PIGEON,
SHOWING
KEPT IN
THE
A LARGE
PERIODIC
CAGE
ACTIVITY
WITH
tempted,therefore,to record simultane-
A PERCH ously the crop contractions and the
The birdspentmostof its time on the perch,but activityin the largercage, but the bird
at quiteregularintervalsit jumpeddownto thefloor always managed to expel the tube no
fora fewminutes. This recordshowstheactivityon
thefloor. Timeis givenin hoursbelow therecord. matterhow carefullyit had been inserted
and fixed.
we obtainedstomachcontractionswhich We sought our relationshipnext in
showed no periodicityat all. In one experiments on the humaninfant. Wada
individual, in fact, both the frequency (i 92) foundthatin a childtenmonths
and the amplituderemainedconstantfor old, during a continuous uninterrupted
eighteendays. The lack of periodicity sleep lastingeight hours,the activity,as
partlydefeatedthepurposeof the experi- recordedby a tambourand springplaced
ment,but not as muchas thefactthat the beneaththe crib,was definitely periodic,
frogsremainedperfectly still at all times, theintervalbetweentheperiodsaveraging
never making even the slightestmove- forty-five minutes. This seemedto offer
ment. us an excellent opportunity,especially
The pigeon seemedmorepromisingfor sinceCarlsonand Ginsburg(I9I5) had
our purposes, since we had previously found that the stomach tube could be
foundits activityto be definitely periodic. passed quite easily into infants. Our
The intervals between the periods are plan was to take simultaneousrecordsof
somewhatshorterherethantheyarein the the stomachcontractionsand the activity
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 315

periodsduringsleep. In six babies used results. The students swallowed the

for these experimentswe succeeded in stomach tube at ten o'clock in the
passingthe tube without too much diffi- evening, just beforeretiring,and simul-
culty,buttheneitherthebabieswould not taneous recordswere taken throughout
go to sleep,orelse thetubewas completely the nightof the stomachcontractionsand
blocked by strongspasms of the cardiac bodily movements. Besides diffuseac-

~~~
-

FIG. II. SIMULTANEOUS RECORD OF GROSS BODILY MOVEMENT AND STOMACH CONTRACTIONS OF A HUMAN ADULT
TAKEN DURING DEEP SLEEP

FIG. i. l CAGES USED FOR STUDYING FOOD-HABITS

FIG. 1L.- CAGES USED FOR STUDYING FOOD-HABITS

sphincter. After many unsuccessfulat- tivities such as turning over, smaller

temptsthis method of attack had to be
abandoned.
Meanwhile, Wada, taking records on
medical studentswhile they slept, suc-
ceededin obtainingsome veryconclusive
movementswere recordedwheneverpos-
sible. Adult activityduringsleep,just as
infantactivity,provedto be periodic,but
the intervalbetweenthe periodsis much
longer, varyingbetween two and three
 3I6 THE QUARTERLY REVIEW OF BIOLOGY

hours. The stomach contractions, of conclusive, would seem to uphold our

course, are also rhythmical,much more
so than they are during the waking
state. And the periods of these two
phenomenacoincideverywell; when the
stomach is quiescent the gross bodily
activity is reduced to a minimum,but
during the contractionperiods frequent
movementsoccur, the largest coinciding
with the "main" hunger contractions.
The recordin figureii illustratingthis
factis similarto thoseobtainedby Wada.
The bodymovements indicatedon the top
theorythat the two-houractivityrhythm
in theratis dependenton gastricfunction.
FEEDING HABITS OF THE RAT
Startingfromour observationson the
relationbetweenactivityand the feeding
periods of the rat, we decidedto extend
our investigationto a study of its food
habits, with special referenceto their
regularity. For thispurposecages shown
in figureI2. were constructed.They con-
sisted of individual compartments large

FIG. I3. RECORD SHOWING THE FEEDING PERIODS OF AN ADULT RAT

intervals
at half-hour
Time is registered

enough for the animals to take plenty

o T
of exercise,with a small tunnelon one
side at the top leading to the food-box.
0
0k5
This tunnelwas built in an inconvenient
positionin orderto discouragethe rat as
Age ir dcQys I much as possible fromenteringit except
I1 i I when driven by hunger. The food-cup
75 85 95 105 1Ii
12S
was placed at the end of the tunnelunder
FIG. I4. GRAPH SHOWING
FEEDING PERIODS
THE REGULARITY
OF AN ADULT RAT FROM
OF THE
the wire cloth floor,and a hole was made
DAY TO DAY in the floorjust large enoughfor the rat
The numberof periodsper day is given on the to insertits head. Whenever it reachedin
ordinatesand the age of the animalin days on the
abscissae. for food, the balance of the cup on a large
tambourwas disturbedand a mark was
line in this figurewere recordedby means made on a smokeddrum.
of a tambour and spring attached from The records obtained in these cages
beneathto the springof the bed. Since bringout clearlythegreatconstancyofthe
onlylargemovements such as turningover feedinghabits of the rat. The recordin
are registeredin this way, it can be seen figureI3, taken on an adult animal from
that just beforethe "main" hungercon- 8 p.m. to 8 a.m., shows that the feeding
tractionsset in, the subjectbecame very period recurredabout once every three
active, and again almost simultaneously hours throughoutthe day, and when the
with the largest contractionwave there experiments were extendedover a longer
was an even greateramountof activity. time, it was foundthat the rhythmper-
The resultsof most of our supplemen- sisted very constantlyfromday to day
tary experiments,therefore,while not (See fig. I4). Similar experimentson
 ANIMAL BEHAVIOR AND INTERNAL DRI VES 3I7

otheranimalsconfirmed theseresults. A GENESIS AND DEVELOPMENT OF THE FEEDING

rat may eat seven times a day or it may HABITS
eat eight or ten times,but in any case it
maintainsa constantaveragefromone day But how does the activityproducedin
to thenext. The degreeof variabilityof this way become associated finallywith

-60

0 100 2.00 300 400 500 600 700 800 900

LeenQth
of intervalin minutes
FIG. I5. FREQUENCY CURVE OF INTERVALS OF VARIOUS LENGTHS BETWEEN FEEDING PERIODS IN FOUR ADULT
MALE RATS FOR TWENTY DAYS

thefeedingresponseis shownveryclearly
by the curve in figurei5, compiledfrom
recordstaken on fouranimals fortwenty
successivedays. The abscissae represent
the length of the intervalsrecordedbe-
tweenfeedings,and the ordinatesindicate
the numberof times each intervalwas
recordedfromany one of thefourindivid-
uals. The curveis evenlybalanced with
a modeof two hundredand fiftyminutes,
or approximatelyfour hours. The few
longerintervals,we believe,may be iden- .:~~~~~~~~~~~~~~~~~T
.. S.:... :..

tifiedentirelywith periodsduringwhich
the rat, like the human being, slept in
spite of the stomachcontractions.
From the above experimentsit seems
fairlywell established, then, that the
hungercontractionsstimulatethe organ-
ism to activity,but what the details of
themechanismare we are not preparedto
discuss. We do believe, however, that
somehow,with each new hunger con- FIG. I6. PHOTOGRAPHS OF CAGES USED IN RECORDING
tractionperiod,impulsesare sent up the ACTIVITY OF NEW-BORN RATS
afferentnervesfromthe stomach to the
brain and out to the stripedmuscles,to the eating process? We cannot assume
releasetheenergystoredup there. that the new-born animal seeks food
318 THE QUARTERLY REVIEW OF BIOLOGY

when the contractionsbegin. Indeed it hoursat a time,and thenreturned to their

would seemmoreprobablethat the rela-
tionshipis built up by the usual trial and
error method. In order to solve this
problemone must learn more about the
activityof the veryyounganimal. Does
it show the periodicmotilityof the adult
individual?
The activityof the new-bornrat was
recordedfromthecages shownin figurei6.
mothersfortwelve hours.
Records obtained in this way showed
that the motilityof the rat immediately
after birth is continuous rather than
periodic (See fig. I7). For the firstten
days it remainsconstant;then a rhythm
begins to appear, and by the sixteenth
day clear-cutand very regular intervals
arepresent. This resultis consistentwith

late

alday old

4 dayls old

13OdaCysoldl

FIG. I7. RECORD OF THE ACTIVITY OF A NEW-BORN RAT Two, FOUR, THIRTEEN, AND SIXTEEN DAYS AFTIBRBIRTH
Up to the tenth day the activity is continuous, then it gradually breaks into periods, which, by the seven-
teenth day, stand out very clearly in the records.

The bottom of the cage consistedof a the factthat thenew-bornof someanima

wooden frame 6 inches square with a
sheet of rubberdam stretchedtaut across
it. The rubberwas coveredwith pieces
of flanneland the sides of the cage, made
of paper, were pasted on the wooden
frame. Everymovementof the animalin
the cage was transmittedthrough the
rubbermembraneto a lever which re-
corded on a smoked paper drum. The
youngratswereleftin thecagesfortwelve
species show stomach contractionswith
almost no indicationof periodicity(Pat-
terson,I9I4). On the basis of this
knowledge,then,we maypicturehow the
diffuseactivity of the new-bornrat re-
solves itselfinto a searchforfood.
In its almostcontinuousmotility,the
very young animal sucks at everything
with which its mouth comes into
contact,-the feet and legs of its litter
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 3I9

mates,the straw of the nest, hair on its
mother's body, and, eventually, the
mother'steats. When it sucks at any-
thingotherthantheteats,nothingresults;
the stomachcontractionspersistand the
activity continues as before. When it
sucksat the teats, on the otherhand, an
entirelydifferentsituation arises; milk
teats through the interventionof the
mother,but largelyby the trial and error
methodthereis graduallyestablished,on
a conditionedreflexbasis, an association
betweendiscomfortdue to stomachcon-
tractions,feeding,and subsequentrelief.
In theadultrat,thepreliminaryrestlessness
which occurs during the time of small

IRcabbit- I day old

~~~~~~~~~...............
... ..... ....
....

K rtten -I day ola

-i I -- ---- I''' '

B
FIG. i 8. ACTIVITY RECORDS OF NEW-BORNANIMALS
A, rabbitand kitten. B, chicken. Time in hoursbelow the record

fillsthe stomach,the contractionscease, contractions is diverted at once into

and the animalgrowsquiet. Then as the
stomachbecomesemptyagain, theprocess
will be repeated. The animalmayhappen
uponthe teatsat the verybeginning,or it
may reach them aftera prolongedactive
interval. In either event, the excursion
always ends with the feeding process.
The young doubtlessfrequentlyfindthe
specificfood seekingactivitiesas soon as
the main contractionsbegin.
It is interestingin this connectionthat
the new-bornguinea pig, rabbit, kitten,
and chick, unlike the rat, show periodic
activity at birth (See fig. i8 A and B).
But how may this fact be broughtinto
relationwith the view developed above?
320 THE QUARTERLY REVIEW OF BIOLOGY

It is importantto note thatwhile the rat FURTHER OBSERVATIONS ON THE PERIODIC

embryoniccon-
is still in a comparatively NATURE OF SPONTANEOUS ACTIVITY.
ditionat birth,theseotheranimalsare all FOUR-DAY ACTIVITY RHYTHM IN THE
fairly well developed and coordinated. FEMALE
The rat, for several days after birth,
progresses muchas a wormdoes, crawling So much for the three to four-hour
andwrigglingitsway about; thenew-born activityrhythmapparentin recordstaken
guinea pig, on the other hand, actually during twelve to twenty-fourhour
walks almost at once. In keepingwith periods. Our observationsmust now be

. .X.! D~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
.>'...tr,-y_
*....
|sc
!E
2 az~~~~~~~~~~~~~~~~~~ .1 jI .F. : >.S . sS11
| .. . .

.;::.
P:r s _l -lill 1 1111 _~~~~~~~~~~~~~
| 11 _ _

. l i N . _ _ _ _
r

_~~~~~~~~~~~
'..,.e '\e.
j eXi;St _H
twffie>x bet;P$w _ _ _ _

_ i _ .' S A
_
_ _ A
F-i_
F < 3 _ _~~~~~~~~~~~~~~~~~~~~~~~~~~~
_~~~~~~ 11
| _
_

.< < ... ........ .

FI.i.APRTSUE ESRIGSOTN:sR O N iGATVT

The ivin com artetwt h
odcpadwtrbtl,adt-cco ee n eno n
ee,cnb
sidewof th patto,adtervligdu_nteohrsd. (ihe n ag 9-.

their periodic bodily activity,the more extendedover days and weeks insteadof
highly developed individuals probably hours. The small triangularcages are
show periodic stomach contractionsat impracticalfor this purpose because of
birth. We have as yet done no experi- the lengthof time requiredto count the
mentsto test this theory,but we hope individual marks on the smoked drum
soonto observein detailthefeedinghabits record. Activityforlong periods can be
of these animals to determinehow the measuredmore simply and much more
habits differfromthose of the rat with accuratelyin the type of cage shown in
regardto theirgenesisand development. figureI9, which consistsof a small living
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 32.1

compartment just large enoughto accom- rhythmdescribedabove. In the female

mnodate a food-cupand an adult animal,
and a revolvingdrumto which the animal
has freeaccess at all times. By meansof
a cyclometerconnectedwith the axle of
the drumby an excentriclever,all revolu-
tions, clockwise and counterclockwise,
are recorded. A detailed descriptionof
the complete apparatusand method em-
ployed is given elsewhere (Richter and
Wang, i926; Richter,i926; Wang, I927).
rat the activityfalls into a regularfour-
day cycle, most femalesrunningeight to
ten miles every fourth day and but a
fraction of a mile on the three days
intervening. In the recordin figurezo,
in which activitymeasuredin the number
of revolutionsis indicated on the ordi-
nates, and the days of the experimenton
the abscissae,the regularfour-daypeak is
very evident. Since this rhythm,which

14,000. 4 4
44

1O00 4 4
4

4 4
0 ~~~~~~~4 4

-
76000--

2 3~~~

~~~~~a3 2~~~~~~~~~~~~~~~2

76 86 96 106 1Q 126 136 146

FIG. 2.O. RUNNING RECORD OF A NORMAL FEMALE SHOWING THEF FOUR-DAY CYCLE

The rat, like many other small rodents, was described independentlyby Wang
seemsto enjoy runningand spendsmuch (I9z"3) and Slonaker(i9z4), occurs in an
of its time in the drum. Although the environmentfree from any cyclic dis-
daily activity averages betweenfive and turbance,it, too, must have its origin
tenmilesformostof theanimals,as many within the organism. But what organ
as twenty-seven mileshave been recorded functionsin the rat at a four-dayrhythm?
for one individual in twenty-fourhours.
Here again, casual observationof the FOUR-DAY ACTIVITY RHYTHM AND THE
OVULATION CYCLE
runningactivitydiscloses nothingof its
origin. Continuous records over long Observationsof the ovulation cycle of
periods of time, however, reveal a fact the rat madeby Long and Evans(i9z2)
far more striking than the tri-hourly answer this question at once. These
3ZZ THE QUARTERLY REVIEW OF BIOLOGY

workershave shown, by the methodsof the sex "drive" of the animal. Wanghas
Stockardand Papanicolaou(I9I7), that foundthat femaleswill mate fora short
the lengthof the oestrouscyclein the rat timejust beforeand just afterthe peak of
is four days, with individual variations runningactivityis reached,while at all
above andbelow thisaverage. As is well- othertimestheyare completelyindifferent
known, this was determinedby histo- or even averse to the male. The exact
logical studies of cast-offcells scraped relationship between running activity,
with a small spatula from the vaginal vaginal smears, and sex activity, as
mucosa. Duringthe dioestrumnucleated worked out by Wang, is shown in figure
epithelialcells and leucocytesare present, 27i. Recordstakeneverysix hourson all

4000 _

-o 3,000-

F_-

1'000{-
s 2p00

R 9unnm acttVt,
11eCat _ m
Scs t'ehavior
CornifieceSe e-
thellol cellm
Nucleacted epi ____ _
thelial ce-lsls
Leuc,ocytes
Snmenr fincdine

el I I I
Tlim 1 I I I I . 1 ,I I I I
noo 11 noon noon noorn noon noon
0 1 2 3 4 5
FIG- 2I. EXACT TEMPORAL RELATIONSHIP BETWEEN RUNNING ACTIVITY AND THE OVULATION CYCLE, ESTABLISHED
BY MEANS OF Six HOUR RECORDS

(After Wang, I923)

whereasduringthe periodsof oestrusand threephenomenashowed that the great

ovulation only cornifiedcells appear.
Wang and Slonakerhave been able to
show by meansof simultaneoussmearand
activityrecords,that the peak of running
activity every fourthday just precedes
ovulation. This is undoubtedlyone of
the most interestingcorrelationsthat
have been made in animalbehavior.
The question arises then, as to the
relationbetweenthe runningactivityand
burstin runningactivityrecordedon the
day of oestrusis confinedalmostentirely
to the six-hour interval which imme-
diately precedesthe appearanceof corni-
fledcells in thevaginal smear.
Obviously, therefore,the spontaneous
activityis dependenton ovarianfunction.
The degreeof dependencecan be demon-
strateddirectlyby numerousexperiments
performed on animalsin which theovaries
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 32.3

were not functioning.Pre-pubescence, of experiments in which a normalfemale

senility, pregnancy,pseudo-pregnancy,had constantaccess to a cage containinga
lactation,and castrationall show a clear- vasectomizedmale. In theseexperiments
cut effectin the activity readings. In a sex-box attached to the usual living-
figurezz, a typicalnormalrecordis pre- cage connectedwith the revolvingdrum,
sented to show the low runninglevel was so arrangedthatthefemalecould pass
beforepubertyand the suddenpubescent freelyback and forthto visit the male,
burst. but the male could not get into the living
Pregnancycauses a 6o to 95 per cent cage and revolvingdrum. This separa-
decreasein activitywhich lasts through tion was achievedquite simplyby means
14P000

(I)

2120,00
0
[-
1,'00 $1 tt p 8

(6,00Q

4,00a

?1 31 4 1 61 TI 81 91
Agein days
'FIG. 2.2.. RECORD SHOWING THE BURST OF ACTIVITY AND APPEARANCE OP THEFFOUR-DAY CYCLE AT THE
TIME OF PUBERTY

(AfterWang)

the entiregestationand lactation period of a board partitionwith a hole just

(Slonaker,i925; Wang, 192.3. See fig. largeenoughto admitthefemale,but too
2.3). Pseudo-pregnancy, produced when small for the male. A typical record
the tip of the uterusis stimulatedwith a obtainedin thisway is shownin figure25.
glass rod introducedthroughthe vagina, In orderthat we mightdifferentiate run-
resultsin an immediatedecrease which ning activitychangescaused by the extra
persistsfor fifteendays (Wang, I92.3. compartmentfromthose caused by the
See fig. z4), and sterilecopulation per- presenceof the male, we attached the
formedby a vasectomizedmale has the sex-boxa week beforethemale was intro-
sameeffect (Slonaker,i92.5). duced. The recordshows that the mere
Similarresultswere obtainedin a series addition of the sex cage produced no

QUAR. REV. BIOL., VOL. II, NO. 3

 324 THE QUARTERLY REVIEW OF BIOLOGY

effect. When the male was placed in it,
however, there was an immediate and
prolongeddecreasein activitywhich per-
sistedfor eight to ten days afterhe was
removedagain.
Figure 26 shows the effectof complete
removalof the ovaries: the activitydrops
strated most strikinglyby the effectsof
ovarian implantationin spayed animals.
Wheneverthe grafts"take," the activity
begins to increase almost immediately,
and it grows graduallyhigher until the
normal runninglevel of the female is
reached. Then, if the graftedovary is

2?o,ooa

18,0001

14,00

07

5EIwooo

-~8000

40000-
4ooo--

gaooo

Aq,in Ca
70 80 90 t00 10 120 130 140 150 OO 170 180 190
FIG. 2 3. RECORD SHOWING THE EPBEcT OF PREGNANCY AND LACTATION ON SPONTANEBOUS ACTIVITY
The four-daycycleis absentduringpregnancy
and lactation,appearingagain a shorttimeafter the litter
is weaned. (AfterWang.)

(6o to 95 percent) to a flat,low level and removed,the activitydrops about 6o to

the four-daycycle disappearscompletely.
When an animal is spayedbeforepuberty
its activityalways remainslow and non-
rhythmical (Wang, 1923; Slonaker,1924).
Finally the dependenceof the running
activity on the ovaries may be demon-
95 per cent, just as it does in the normal
femaleafterspaying.
These experiments show definitely that
the high runninglevel is dependentupon
some substance secretedby the ovaries
into the blood stream. The questionnow
 ANIMAL BEHAVIOR AND 1NTERNAL DRIVES 325

arisesas to what part of the ovariespro-
duces this substance. Bugbee and
Simond(i926) have thrownsomelighton
thisproblemby experiments in which the
extractfrompigs' follicleswas injected
level of normal animals and the genital
tractresumesits normalcondition.
Wang also has obtained these results
by the injection of follicular extracts
(Unpublished results. See fig. 27). He

80.000 1

0
18,00

16,000-

I4,000-

5--
~0

Ep,o0-

4,000-

2,000-

Age,in doss
70 80 90 to0 II& 120 130 140 150
FIG. 24. EFFECT OF PSEUDO-PREGNANCY oN ACTIVITY
(After Wang)

into spayedrats. Such a procedurepro- foundthat the smearchangesare usually

duces the same effectthat successfulim- detectedseveraldays beforethe activity
plantationof an ovary would have pro- changesbecomewell defined,and in many
duced,-the activity shows a marked instancesthe activityand smearchaniges
increasefromthe low spayedlevel to the occur independently of each other. Ac-
 a)~~~~C
Cs
OQ)
0 a~~) 0
0~~~~
14,00 )

0 a

V.)'
12,OOQ--

5= 10,000-
0

96,00 A 8
4-b

4,00a
t~ ~~ 4
2U00L

73 83 93 103 113 153 133 143 1753 i3 17G

Q-
6,O
FIG. 2.5. RECORD SHOWING HOW THE PRESENCE ATMAi
OF AFFETS TEE AcrIVITY oFOmAxRB
THE

I('>0003

z
14,000

l2p000

I10,00oa
4-3

8,000-

4,"000-

2,000-

e infdLj
97 107 117 127 137 147r 157 167 177 187 197 20

FIG. 2.6. REscoRD SHOWING THEa EFFECT OF THE CompLETEaREMovAL oF BOTH OvARIEs

32.6
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 327

cordinglyhe has concludedthattheremay appear and disappear with very little

be in the ovarian secretionone specific
substancefor furthering the growth and
developmentof the genital tract and
another for the productionof activity.
in which
And on the basis of experiments
he traumatizedthe ovaries (Wang and
Guttmacher,
i9z7),
this suggestion
comeseven moreplausible. It was found
quite by chance that a small remnantof
ovaryleftin the bodyproducesverystrik-
relationto the changesin activity.
The questionas to how and where the
secretionacts to producethe activityhas
not yet been answered. We thoughtat
firstthat, just as the threeto four-hour
rhythmwas set up by stomachcontrac-
be-
tions,so thefour-daycyclemighthave its
originin the contractionof some similar
hollow viscus in the sex-apparatus,prob-
ably the uterus. Contrary to our expecta-

12P-000.

10,000-

,y0 0

tooo
FE4,000-

r,)

35 45 55 65 75 85 95 6
lOS l1
A9gein days
FIG. 2R7. RECORD SHOWING THE EFFECT OF DAILY INJECTIONS OF FOLLICIN ON THE RUNNING AcrIVITY OF A
SPAYED FEMALE
wasadministered
theperiodoverwhichtheextract
Theshadedareaindicates

ing changes in both smear and activity tions,however,Wang foundthatremoval

findings. The activity,exceptfora drop of the uterusaffectsneitherthe level of
of shortdurationimmediatelyfollowing activitynor the four-daycycle (fig. 28),
the operation,usuallyregainsits original and Hoskins (i9z5, II) has recentlycon-
level, but the four-daycycle is entirely firmed theseobservations. The secretion,
absent. Coincidentwith thehighirrhyth- then,musttake effectin somepartof the
mic activity level, the vaginal smears centralnervoussystem,eitherby simply
usuallyshow cornified cells,theindication increasingthe irritability
of the centersin
of oestrum in the normal animal. In the brain and spinal cord, or by actually
some individuals, however, the other stimulating thosecenters. Althoughdefi-
types of cells, as well as cornifiedcells, nite evidence is lacking at present,we
3X8 THE QUARTERLY REVIEW OF BIOLOGY

are inclined to hold to the latter possi- mal runninglevel (Richterand Wislocki,
bility. I9z7). And transplantation of ovaries
brings about an even greater increase
SPONTANEOUS RUNNING ACTIVITY OF THE (Wang,Richter,and Guttmacher,
I92.5).
MALE The activitythen reaches the high level
In the male the spontaneousrunning of the female,and, what is moreinterest-
activitydoes not show the four-daycycle ing, it also shows the four-dayrhythm
of the female,and the generalaverageis (See fig. 30). When the graftsare re-
somewhat lower. However, it is de- moved the castrateeffectsappear again.
That the relationof runningactivityto
the sex "drive" is not so clear-cutin the
16,00
male as it is in the female,is demon-
stratedin a seriesof experimentsin which
14,00Q 9 each male was removedfromthe running
cage fora half hour each day and placed
with a femalein "heat" in a large stock
to cage. We foundin this way that males
0 showinga low runningactivitytook no
interestin the femalesand made no effort
to copulate,whereas males with a high
running activity copulated frequently.
Contraryto the effecton the females,
4icoo however,copulation,even when repeated
o as many as thirtytimes, produced no
ci5 i
noticeable change in the runninglevel
of the male on the followingday. An
4.800Q- activity curve of one of these animals,
typicalof the entiregroup,is presentedin
figure
3I.
Nothingis knownregardingthe mech-
anism involved in the production of
..,,/g 49'ndcLysl the activityof the male. That the re-
50 60 70 80 90 moval of the seminal vesicles produced
FIG. 2
8. RECORD SHOWING THAT REMOVAL OF THE
a no morenoticeableeffectthan did the
UTERUS AFFECrS NEITHER THE LEVEL OF THE RUN- removal of the uterus in the female is
NING ACrIVITY NOR THE APPEARANCE OF THE CYCLE
shownin figure32.. We are tryingto dis-
cover on what part of the testes the
pendenton the sex glands,forwhen the activityis dependentby a methodsimilar
animal is castrated the activity drops to thatusedbyStockardand Papanicolaou
about 6o per cent to the low level of the in the female. We have been extirpating
spayed female(fig. z9). Hoskins (i9z5, the testesin some animals at a peak of
IV) was able to demonstrate no changein activity and in others at a depression
activitywhen testeswere transplanted to with the expectationthat detailedhisto-
the castrate,but we have foundthat the logical studiesoftheseorgansmaydisclose
activityimmediatelyincreasesto the nor- what partsare responsibleforthe fluctua-
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 329

12)000

o poo d

o 8,000-

-~4,000

2,00u

fLe. in~
daty
145 155 165 175 185 196 205 021 225 23;5 245 2255

FIG. 2.9. SPONTANEOUS RUNNING ACTIVITY OF A MALE, SHOWING THE EFFECT OF CASTRATION

14Q00- 0

45)

12,000 d

I0;I0000-

",8,000-

- .000-

Owl

30 40 50 610 X70 80 90 100 It10 1o 130 140 150

FIG. 3O.RECORD SHOWINGTHEBEFEBCTOF IMPLANTATION0OFOVrARIE3INTO A CASTRATEDMALB,

tions in activity. Although we have It must be borne in mind beforewe

obtainedno conclusivedata the approach pass on to a discussionof otherrhythms
is promising. that the work reportedabove has simply
330 THE QUARTERLY REVIEW OF BlOLOGY

demonstratedto what extent the overt OTHER ACTIVITY RHYTHMS

bodily activity is dependent on the sex
hormone. None of our experimentshas With a knowledgeof the cyclicfluctua-
shownthat the hormoneactuallyproduces tions in activitywe may learn a great
the activity. Veryprobablya numberof deal about changes which occur in the
other organs are equally important,so different organs within the body, when
that the elimination of any one of them outwardly or without sacrificeof many
would be to
sufficient bringaboutthe large animals nothing could be learned. The
decreasein activitywhich follows spaying discoveryof the four-dayactivityrhythm
or castration. We have tried removing in the female rat, for instance, would

16,000,

14,000.,

I ,000.

0 10000.

4-,000-
,
8pOOQ

2,000.

AC ii7 dcYs
50 60 -to 80 90 100 110
FIG. 3I. EFFECT OF COPULATION ON THE RUNNING ACTIVITY OF A MALE

the thyroid,hyperthyroid, and the pitui-
tary,but in so far as our operationswere
successful,they produced no change in
activity. Removal of the adrenals, on
the other hand, causes a decreasein the
runningaverage, although the sex cycle
still remains(See fig.33). It can be seen,
then,that we still do not have complete
knowledgeof the mechanismwhich de-
terminesthe composite picture of the
spontaneousactivity.
have led veryquicklyto the discoveryof
the oestrous rhythmhad it not been
already detected by othermeans. This
same principlemay be applied in a search
forcyclicchangesin otherinternalorgans,
since we have found periods of activity
longerthan fourdays in both males and
females afterthe sex organs have been
removed. There are at least two other
fairlywell-definedrhythms,one of from
seven to ten days (fig. 34), and one of
 ANIMAL BEHAVIOR AND INTERNAL DRIVES 331

fromsixteento thirtydays (figs. 35 and associatedwith some specificperformancc

36). Besides these two rhythmsa num- just as the three to four-hourand the
ber of othersvaryingbetweenfortyand four-daycycles are? It may be that,
one hundredand twentydays have occa- coincidingwith these slowerfluctuations
sionallybeenobserved bySlonaker(i92.6) of runningactivity,changesin such pur-
and by us. Figure37 shows the activity suits as burrowing,climbing, gnawing,
record of one animal in which a small fighting, and other specific
nest-building,
remnantof one ovaryremained. activities can be demonstrated. How-

i(6,000

14,000A

12,000 ts

Te
00

6,~0001~

4,000.

2,000.

Aeiri
ye
29 39 49 ro9 69 79 b9 99 109 119 129 1a9
FIG. 32.. RECORD 01FTHE RuNNING ACTIVITY 01F A MALE, SHOWING THE EFEC-r OF REMOVAL OF BOTH
SEMINALVESICLES
Therecord inno way,so faras we have beenabletodetermine,
differs from animal
thatofa normal

The questionarisesnow as to the origin ever, beforewe take up the question of

and significanceof these rhythms. The
other internalglands, the thyroid,the
parathyroid,the pituitaryand the ad-
renals, suggest a possible source. We
have been removingeach of theseorgans
at variousphases of activitybut we have
beenunable as yetto make a studyof the
histologicalsections.
So muchfortheoriginoftheserhythms.
What is their significance?Are they
thesemorecomplicatedbehaviorpatterns,
we mustconsiderbrieflysomeofthepurely
physiologicalmechanismsin order that
we maycomprehend the completeactivity
picturepresentedby the organism.
OVERT RESPONSES OF A PURELY PHYSIO-
LOGICAL NATURE
For this reasonwe have studieddrink-
ing, urination,and defecation,to deter-
332. THE QUARTERLY REVIEW OF BIOLOGY

30.000-

28,000-

26.000

24,00Q

0 0
22,00Qe

20,00Qc- C5-)

OC18,000- ON7-M

40 51

12.Q00-
000
334.REORDSHOIN
FIG. EPET O TH RMOVL O BTH DREAL

-1400Q.

00
(0,0

46000-

2kOOCL

40 50 60 7 80 90 100 110 20o 130

FIG. 33. RECORD SHOWING THE, ErFFCT OF THE RE,MOVALoF BOTH ADRENALS
 ANIMAL BEHAViOR AND INTERNAL DRIVES 333

mine whether these functions,too, are and an invertedwateringtubewas placed

periodic. Recordsof the timeintervalat at the end away from-the cage. The
which these threeresponsesoccur show bottomof this recesswas made of a piece
thattheyare all rhythmical. of aluminumpivoted at one end and sup-

D 01
0

22P00 0 D i ^

54 i 64 y 4 84 94- 04 114 Z24 134 144

FIG. 34. ECORDS FROM Two CASTRATED MALES AND ONE SPAYED FEMALE, WHICH SHOW RHYTHMS VARYING PROM
5 To 8 DAYS
These rhythmshave beenobservedin normals,but theyarefoundmostoftenin castratedor spayedanimals
probablybecauseofthemuchlowerrunningactivitylevel.

8,000

2k000.
52 9 02
0 62r68
12002 2 12 S

9eir dc.J5
52- 6a, 7~ 82 9~ JO- 112 1I a 132 14~
FIG. 35. RECORD OF A NORMAL MALE SHOWING A i6 TO 21ODAY CYCLIC CHANGE IN THE RUNNING ACTIVITY LEVEL

thanthefour-day
The cyclesaremuchmoreirregular cycle,buttheyareclearlypresentnevertheless.

Thirst was studied by means of the
cages shown in figure38. A recesslarge
enoughforthe animalto enterand drink,
but too small for it to lie down or turn
around,was built on one side of the cage
portedon a tambourat the other,so that
wheneverthe animal enteredto drink a
mark was recordedon a smoked drum.
The records,as may be seen in figure39,
show that the rat drinksabout ten times
 16,000

14,0001

'2,000 0

0 10poo.

6,00

4,0001

2,000.

A in days
87 97 107 1I7 121 (37 147
FIG. 36. RECORD OBTAINED PROM A NORMAL MALE SHOWING ONB VERY STRIKING CYCLE oF TWENTY-NINE
DAYS DURATION

The activitymountssteadilyfortwelvedays, thendecreasesagain equallysteadilyfor the nextseventeen

days. Such regularcyclesoftenappearin the midstof an otherwlseveryirregularrecord.

16,00

14,000--

9 12,000-

s-10,000.

8,00O.

71(0 9 116 136 15G 176 190 2-1G -20 256 27(C 296 316
FIG. 37. GRAPH SHOWING CYCLES OF MucH LARGER DURATION,-90 TO i2.o DAYS
This recordwas obtainedfroma femalewith one ovarycompletelyremovedand the otherpartiallycut
away. The animaldid not show the low activityof the spayedanimal. On the contraryit showed cyclic
duringwhichit reacheda level nearlyas high as thatpresentbeforetheovarywas traumatized.
fluctuations,
334
 ANIMAL BEHAVIOR AND 1NTERNAL DRIVES 335

a day at intervalsof two and a quarter mentsof the time interval,nor can we
hours. The periodicityof the thirstre- show how these rhythmsvary with age
sponseis quite as remarkableas that of and sex.
thehungerresponse,in view ofthecurrent Thesephenomenamustreveal the perio-
conceptionthat the rats eat and drinkat dicityof the bladderand rectum,but so
veryfrequent and irregularintervals. farwe do not know in what organthirst
Urinationand defecationwere recorded is localized. Possiblythroughourknowl-
in the apparatusillustratedin figure40. edge of its periodicitywe may obtain
The small cage with a '-inch meshwire- someclue as to its origin.
cloth bottom,restedover an 8-inchpar- The resultsof all of the experiments
affinedtin funnel. When the rat def- discussedabove have shown how largely
ecated, the fecesslippedthroughthewire the spontaneousactivitiesof the rat are
floorinto thefunneland on to an inclined periodic in nature, and are associated
trough of fine-meshed wire below. As
TABLE I
theydroppedfromthe end of this trough
theystrucka small paper disc fastenedto ACTIVITY PERIODICITY ASSOCIATED ORGAN

Urination Z-3 hour Bladder

n
)aterin Drinking
Defecation
2-3 hour
3-5 hour
?
Rectum
Eating 3-4 hour Stomach
Mating Y 4 day Ovaries
Nest-building ? ?
Cag( Gnawing ? ?
Burrowing ? ?
Fighting ? ?
Migrating ? ?
7 days ?
Torb oLur i 8-zz days ?
40-,lo days ?
FIG. 38. DIAGRAM OF THE CAGE USED IN RECORDING ? ? Adrenal
THE THIRST RHYTHM ? ? Pituitary
? ? Thyroid
the end of a tambour,and the processwas ? ? Parathyroid
recordedas in figure4I. Urine was also
collected in the funnel but it passed with periodically functioning organs.
directly through the wire trough to From these results,we see the animal as
anotherpaper disc attached to another an organismcarrying withinitselfvarious
tambour. A recordof urinationis shown mechanismsdischargingat differentrates,
in figure42.. to a great extent independentlyof one
From simultaneousrecordsof urination another. By way of summarywe have
and defecationobtainedby this method, listed in Table I the different
activities
it was found that although these two according to their periodicityand the
functionsare veryregular,they are quite organwith which theyare assoc.ated.
independent. Urination occurs approxi-
CONSTRUCTIVE ACTIVITIES
matelyeverytwo hours;defecation,every
five hours, but the group of animals With this work on the simplerforms
studied up to the presenttime is not of spontaneousbehavior as a basis, we
sufficiently large to permitaccuratestate- may now single out for study the more

QUAR. REV. BIOL., VOL. II, No. 3

336 THE QUARTERLY REVIEW OF BIOLOGY

of quantitatively studied. We may ask,

complicatedand specificperformances
therat,suchas burrowing,gnawing,nest- then,what it is that makes the rat build

---
FIG. 39. RECORD SHOWING THE THIRST RHYTHM OF AN ADULT ANIMAL

Time in hoursbelow

Cci

0 0oooo
0 oo0 o 00o O 0O a0 0 0 0 0 0

-
'/ Trough
c , r

FIG. 40. DIAGRAM OF TH1E APPARATUS USED IN RECORDING URINATION AND DEFECATION RHYTHMS

=~~~ -_
I T I I I I I I 1 1 1 1 I I [ I If I i t -X

FIG. 4I. RECORD OF THE DEFECATION RHYTHM OF AN ADULT RAT

Time in hoursbelow

building, and social activities. At the nests. In order to answer this question
present time nest-buildingis the only we must arrangeour experimentso that
constructive activity which has been nest-building is practicallythe onlyoutlet
 ANIMAL BEHAViOR AND 1NTERNAL DRIVES 337

for the animal, and all other activities vals tell us nothingabout the mechanism
are either kept constant or eliminated. involved. Observedover long periods
Such a situation in which spontaneous of timeundercontrolled will
conditions,
nest-buildingcan be measuredhas been it also be periodiclike the runningac-

FIG. 42. RECORD SHOWING THE URINATION RHYTHM OF AN ADULT RAT

Time in half-hourintervals

workedout verysatisfactorily by Kinder

(I92.7), in two differenttypesof cages.
In thesecages the activityis measured
in termsof the numberof stripsof crepe
paperusedeach day by the rat in building
its nest. The method of presentingthe
paper differed in the two typesof cages.
In the firsttype 6oo strips,I inch wide
and 6 inches long, were scatteredeach
day evenlyoverthe floor,and the animals
builttheirnestsby pushingthe stripsinto
heaps. In cagesofthesecondtype,(fig.43
A and B) 2O5ostrips, iS incheslong, were
hungoverthesidesso thatthe animalhad
to pull down one stripat a timeand take
it to the nest. With these cages Kinder
foundthat if the nests are removedeach
day ratsof all ages will build a freshnest
withinthe followingtwenty-four hours.
That the activityis presentand equally
strongin both sexes is shown by the
recordsof the daily nest-building activity
of a male and femalegivenin figure44 A
FIG. 43. PHOTOGRAPHOF ONE TYPE OF CAGE USED
and B. Moreover,nest-building is prac- IN MEASURING NEST-BUILDING AcTIVITY
tically independentof experience,since A shows thecage assembledwithoutnest-building
youngrats thirtydays old raisedin saw- material. The walls are of galvanizediron and the
dust build perfectnests out of the crepe top of wire cloth. The diameterof the cage is 36
inchesand theheightI8 inches.
paperthefirsttimeit is presented to them. B shows the arrangement of the stripsof crepepa-
But what is it that drivesthe rat to build peroverthe sidesof the cage. The stripswerehung
so thattheratscould reachthemcomfortably onlyby
nests? Again observationsforshortinter- standingon theirhindfeet. (AfterKinder,I92.7.)
338 THE QUARTERLY REVIEW OF BIOLOGY

tivity? Here Kinderfoundthat the four- in commonthatindicatestheoriginof the

day rhythmof the femaleis presentjust
as it was in the runningactivity(fig. 45),
but it has a verydifferentrelationto the
cycle. Nest-buildingis greatestin the
dioestrousinterval of low runningac-
tivity and lowest during oestrus when
the runningactivityis highest. At par-
activity:every phase can be understood
mechanism
as a partoftheheat-regulating
by means of which the body-temperature
is maintainedat a constantlevel. The
activityincreasesin low temperatures and
decreasesin high temperatures.It is high
when there is a tendencyfor the body

A MALE
u-o300

20

U.
0

AGE INrAYS45 so 55 60 0 75 85 90 94
DATh .+ I4 )cc 4 i4 24 Jctrz

B. F E MALE
REO300

100

SMEAR
RECORD 46 5t 56 61 66 '71 76 8
AGEIN DAYS 41 Z6 May6 16
DATE r
Apr I6

FiG. 44. DAILY RECORDS OF THE NEST-BUILDING ACTIVITY OF A, A MALE, AND B, A FEMALE, OVER A PERIOD OF
50 DAYS

turitionand duringlactationthenestsare temperatureto decrease,beforepuberty,

very large, but the controllingmecha-
nismis obviouslynot an essentialpart of
the reproductiveactivitysince the males
oftenbuilt nests as large as those of the
motherrats.
Kinder found that all phases of the
nest-building
phenomenon haveonefeature
during the inactive dioestrousinterval,
during pregnancy and lactation, and
during starvation;it is low at oestrus,
when the animal is very active and the
body temperature tendsto increase.
We may regardnest-buildingas a part
of the heat-regulating
mechanism,just as
 ANIMAL BEHAVO1R AND INTERNAL DRIVES 339

350

300

250

?.- 200
LO

Ii-

Ii0
50

0 ~~~5~
'~
'7000

6000
U)

2
0
1-

FIG. 45. RECORD SHOWING THE RELATIONBETWEENNEST_BUILDINGAND RUNNING ACTIVITY

(AfterKinder)
340 THE QUARTERLY REVIEW OF BIOLOGY
we considerthe growth of fat and hair
duringcold weather a part of the more
primitivephysiologicalmanifestations of
heat conservation. Nest-building, like
the buildingof sheltersand the wearing
of clothing,is a much more highly de-
veloped methodof maintaininga normal
bodytemperature, but it is nevertheless
an
expressionof the same impetusthat pro-
~~~~~I_~
Hw~~~1
FIG. 46. MULTIPLBa AcrIVITYCAGER
duces the increasein fat and hair in more
primitiveanimals (Martin, C. J. i9oi).
The mechanismof thedriveinvolvedhere,
therefore,is verydifferentfromthat pres-
ent in either the hungeror the sex ac-
tivities.
Allied to nest-buildingin the rat are
probablyburrowing,the tendencyof the
animal to wedge itselfinto small spaces
with contacton all sides,and its desireto
huddletogetherwith severalof its mates.
These activitiesalso tendto conserveheat,
in contrast to running,climbing, and
jumping,which contributeto the main-
tenance of a constant body-temperature
throughheat production.
The various performances which, al-
though associatedwith otherdrives,may
be consideredas contributing to the heat-
regulating process, can be grouped as
follows:
Nest-building
Burrowing
Huddlinginto small
conservebodyheat
spaces
Huddlingtogether-
socialcontact
Running
Climbing increase
heatproduction
Jumping
Thus far we have investigated the
different activities of the rat separately
undermoreor less isolated and controlled
conditions. We believe that it is possi-
ble, however,to studythe animal under
normal conditions,when it can indulge
in anyof the activitiespresentin its usual
outdoor environment.For this purpose
we have constructed thesetofcagesshown
in figure46, in which a record can be
obtainedofthe timespenteach day by the
ratin climbing,running, burrowing,gnaw-
ing eating, drinking,and mating. This
cage makes it possible to accountforthe
activity of the animal each day during
every minute of the twenty-four hours.
The large triangular central cage and
all of the smaller cages at the side,
except the revolving drum and the
climbing tower, are supportedon tam-
bours. Runningactivityis recordedboth
graphicallyand with a cyclometer; climb-
ing activity,by countingthe numberof
times the animal goes up and down the
towereach day. Both theentranceto the
 AN1MAL BEHAViOR AND 1NTERNAL DRIVES 34I

tower and the top part are supported any perspectiveon either the constancy
on tambours,so that a record is made and fluctuations or the importanceof the
on smokedpaper each time the animal different activitiesin the life of the rat,
startsup the tower and when it reaches but we do know that in this cage the
the top. runningactivityin the drumis reducedin
Because of the fact that we had only everycase to a few hundredrevolutions
one cage we were not able to gather per day. It is veryinterestingalso, that
enoughdata to be of statisticalvalue, but in thesecages wherethe animalhas many
we have made sufficient observationsto different diversionsthe frequencyof its
know that with some refinement of this eatingperiodis greatlyreduced. It enters
method the behavior of the rat can be the food-boxonce everyfiveor six hours,
thoroughly studied in the laboratory. and sometimeseven less frequently,but
Certainlywith this type of cage we can whetherit actuallyeats less foodwe have
obtain a normal environmentfor the not yet determined.
animal, in so far as it has an outlet for That even the most complicatedform
drives,and if we can oftherat'sbehaviormaybe studiedin this
most of its different
judge how normalthe environment is by cage is broughtout by the followingob-
the type of rat that it produces,the suc- servations. In experiments on one animal
cess of the method is unquestionable. a liberal supply of building material,-
An individualbroughtup in the multiple sticks, rope, stones, and cloth,-was
cage is farmoreintelligentthanone raised placed in the large central cage. This
in theordinaryrunningcage. Withinthe animal had habituallydepositedits feces
multiplecage the animal shows all kinds in the water-cup. Usually the waterwas
of constructive and imaginativeactivities, changedeveryday, but on one occasion,
rarely,if ever,seenin an ordinarylabora- by some neglect,it was not changedfor
toryrat, and on occasionswhen it escapes several days, so that the resultingodor
it avoids recapturewith extraordinary became very unpleasant. At this point
success. We may note in passing that the animal startedto cover the hole over
were rats of this environmentused for the water-cup. It firstremovedpart of
experiments on extirpationof thedifferent the upper layer of the cardboardbottom
areasin thecortexofthe brain,muchmore of the large centralcage, and draggedit
noticeabledefectsin behaviormightpossi- into the water-box. It placed the card-
bly be demonstratedas a result of the board over the cup and smoothedit down
injuries than have appeared thus far in on all sides until the hole was perfectly
the rat kept under the usual laboratory covered. Then fromthe bottom of the
conditions. centralcage it liftedstoneslargerthan its
Individualdifferences are quite striking head threeinches into the drinkingcage
in the multiplecage ifwe may judgefrom and placed themoverthecardboardcover.
our small numberof animals. One rat Besidesthe large stonesnumerouspebbles
will spendmostofits timein theclimbing and stickswere used until the water-box
tower, passing up and down as many as was completelyblocked. The animalhad
thirtyor fortytimes a day; anotherwill cut offits only water supplyby this per-
spend all of its time in the sex box; and formance. Sincewe wishedto seewhat it
anotherwill gnaw all day long. None of would do when it became very thirsty,
our recordshave been taken over suffi- the materialwas leftundisturbedand no
cientlylong periodsto permitus to give otherwaterwas given. Afterthreedays,
 34Z THE QUARTERLY REVlEW OF BIOLOGY

the animal pushed all of the sticks and offeredfor the frequencywith which
stones fromthe drinkingcage into the adult rats closed the entrance to the
large centralcage, tore up the cardboard running drum shortly after they were
seal, and drank its fill of the polluted placed in the cage. In one instancethe
water. This observationis certainlycom- openingwas plugged up so tightlywith
parable to those made in the field. Had nest-buildingmaterial that a knife had
our apparatus been working better just to be used to open it up again.
at this time we should have obtained Many similarexamplescould be given
a completebiological recordof this very to demonstrate that in our artificallycon-
interestingincident. structed environmentpractically every
Anotherperformance likewiseconstruc- variety of behavior observable in a
tive but less complicatedwas frequently natural environmentis obtained. And
observed. The rats plug up the entrance with a record of the way in which
to any of the smallercageswheneverthey the animal spends its time beforeand
have been frightenedon enteringthem. aftersuch episodesmuchmorelight will
This is the only explanationthat can be be thrownon theirorigin.

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