PhystologyandBehav,or, Vol l l , p p 543-553 Brain Research Pubhcatlons lnc , 1973 Prmtedm the U.SA.

Presurgical Rearing Environment Alters Exploration, Fluid Consumption, and

Learning of Septal Lesioned and Control Rats

P E T E R J DONOV1CK, R I C H A R D G B U R R I G H T AND M A R K A SWIDLER l

Departme~tt o] Psychology, State Unil'erslO' o f N e w York at Bmghamton, Bhlghamton, N e w York 13901

(Received 1 F e b l u a r y 1973)

DONOVICK, P J , R G BURRIGHT AND M A SWIDLER Presurgtcal rearing envwonment alters exploranon, flutd consumption, and leatnmg o] septal lestoned and control rats PHYSIOL BEHAV 11(4) 543-553, 1973 -Rats were reared m etther enriched, social cages or restricted mdwidual cages from 25 days of age until they underwent septal or control surgery two months later Rearing condlnons differentially altered septal and control behavior as measured by (11 exploration tests; (2) fluid consumption of water, saccharin, and quinine; and, (3) the learning of a spatial alternation task

Septal lesions Early experience Exploratmn Flmd consumption Sodium saccharin Spatial alternation performance

Water Quinine hydrochlorlde

AS R E C E N T L Y reviewed by Fried [ 7 ] , septal lesions have been s h o w n to af fec t a wide range of behav io r For example , lesmns enhance the learning of an act ive avoM- ance p rob l em [ 13 ], impa i r classic response i n h i b i t i o n tasks [ 1 1 , 1 2 ] , and al ter c o n s u m m a t o r y b e h a v m r [4,9] and sensory react iv i ty [ 1, 15, 17 ]. In work ing wi th these p rob- lems we have no t ed the typical septal effect , bu t also a wide range of var iabi l i ty wi th in lesioned and con t ro l groups Since septal lesions a l ter the degree, r a the r t han the man- ner, of response to st~muh ,t b e c o m e s i m p o r t a n t to more fully u n d e r s t a n d those variable which mf luence the Individ- ual responsiveness of a l e smned or non le s loned an imal Obviously , the p ro b l em can be a p p r o a c h e d by invest igat ing the early exper ience of the Individual , his genet ic h i s to ry , and the l n t e r a c t m n s of b o t h these factors wi th specific e n v i r o n m e n t a l c o n d i t i o n s While it has been clearly shown tha t the genet ic [8] and exper ien t ia l ( e g , [ 2 ] ) h i s to ry of the o rgamsm affects a wide range of behavior , l i t t le Is k n o w n a b o u t the effects of such m a n i p u l a t i o n s on the behav io r of the organism fo l lowing brain damage.

To begin to examine exper ien t ia l in f luences on the behav io r of lesioned and non le s loned animals we m a m p u - lated the p o s t w e a n m g e n v i r o n m e n t of no rma l rats for 60 days Since there was no previous l i te ra ture d , rec t ly rele- vant to the p rob l em, insofar as s u b s e q u e n t bra in damage is conce rned , we fo l lowed the example of Benne t , D m m o n d , Krech and Rosenzwelg [2] We m an i pu l a t ed the exper ien-

tlal h i s to ry of two groups of animals such t ha t one group ( the so-called enr iched g roup) was al lowed same sex social in t e rac t ions as well as the o p p o r t u n i t y to explore and al ter a relatively complex e n v i r o n m e n t . The o t h e r g roup was reared unde r more res t r ic ted condatons wh ich p roh ib i t ed any di rec t social in t e rac t ions and reduced exp lo ra to ry poss lbiht ies Septal lesions or con t ro l ope ra t ions were t hen pe r fo rmed and a series of behawora l m e a s u r e m e n t s were ob t a ined which have been prevmusly s h o w n to d f f fe ren tmte be tween septal lesioned and con t ro l animals These in- c luded m e a s u r e m e n t s of exp lo ra t ion , c o n s u m p t m n and learning of a spatml a l t e rna t ion task It was found tha t the presurglcal h i s to ry of the an imal d l f fe ren tml ly af fec ted the behav io r of the les ioned and non les loned animals on these various behaviora l measures Individual di f ferences , how- ever, were no t marked ly reduced

METHOD

A 12 l reals

For ty-s ix male a lb ino rats, supplied by the Charles River C o m p a n y , were used m this expe r imen t . They were 25 days of age and wmghed a p p r o x i m a t e l y 43 g at the s tar t of the s tudy. Five animals died dur ing the e x p e r i m e n t One died dur ing the init ial 60 days of m a i n t e n a n c e , two dmd dur ing surgery, and two add i t iona l shor t ly a f te r surgery. Two rats

~We thank Came Burchardt and Michael Laughhn for thmr assistance This research was supported m part by NIMH Grants MH 15821, MH 13058, and the State University of New York Research I,oundatlon A prehnunary report on some of these results was presented at the Psydlononnc Scmnce Meeting, St Lores, M~ssoun, November, 1972

543

544 DONOVI( 'K, BURR1GHT AND SW1DLFR

failed to meet our his tological criteria tsee be lowl Thus the final da ta analys~s ~s based on 39 anuna l s

Pte vtoglcal 3lain tc'na~ c c

Upon recmpt f rom the suppher, ammals were weighed and randomly assigned to an enriched {E) group or restnLted (R) group The weanhng anllnal~ were then placed m appropr ia te cages m a v lvarmm which was mare- tamed on a 12 hr hght - 12 h r d a r k r e g ] m e , w l t h t e m p e r a - tures between 21 and 24"C Food (Purina lab chow) and water were available ad hb for bo th groups dur ing the entire presurglcal per iod

Ammals for the enriched group were mamed~atel} (at 25 days o f age) placed in socml cages conta in ing four to six ammals each and mainta ined thele un td s taged at 85 days of age The enriched env l ronment , l l ] us t ra tedm Fig I w i th a single adul t aminal , consisted o f a 58 \ 48 x 36 ~m ~age with three per fora ted galvamzed ~heet-metal ~all~ and a hardware-c lo th door winch allowed the rats v>ual a~cess to

/

a large part ot tile v~varmm Inside the ,.age throe wele two stable and secure p la t fo rms made of p ine w ood A ramp f rom the f loor led to the first p l a t fo lm , which was ¢) cm above the f loor and e x t e n d e d m a L-shape a round two walls of the cage Yhe second p l a t l o rm, placed against the t turd wall, was at a level of 20 cm above the floor of the cage & ramp ~onnec ted the first and second p l a t t o rms and a ladder c onne c t e d the f loor to the second pla t for ln L a c h p l a t f o l m wa~ 10 cm w~de and 30 c m a l o n g a w a l l In each cage there were two 1 tit capaci ty m a s o n lars placed on thmr s~de.s and part ial ly tilled with paper ai~d wood shavings , one was on the f loor and the second was ~m the lowel p l a t fo rm lmtml ly , all the w e a n h n g tats m a cage could , and did, en ter a single lar at the ~anle l ime Ping-pong balls, newspape r , and s t y r o f o a m p~eces were svat lered a round the cage, a chain was s u s p e n d e d f rom the ce lhng kach of the five e n r i c h m e n t cages con ta ined these t ea tu res and thereb} provided the i nha b i t a n t s a varied phTyslcal and socml e n v i r o n m e n t In addi t ion , the ]ats tn lhc enr iched g roup weie hand led three tmles a week dur ing the p res tugery t ea>

biG l Lnrlched presurglcal maintenance ~.age u~cd for maintaining four to sl\ rat~ |roill 25 85 da~ ~ of age

P R E S U R G I C A L REARING, SEPTAL LESIONS, BEHAVIOR 545

lng period During the handl ing sessions the antmals were taken f rom the living cage, one at a t ime, and placed toge ther in a large box wi th wood shavings, paper , and s ty rofoam pieces The expe r imen te r then cleaned the hwng cage and replaced the animals, one at a t ime, in to the home cage. Each animal was then fed several Cocoa Krisples f rom the expe r imen te r ' s hand This was the only dietary differ- ence be tween enr iched and restr icted anlinats

Animals in the restr icted group were placed m individual s tandard labora tory rat cages (24 x 17 x 18 cm) The f ront wall was wire mesh covered with a p lywood visual barrier and the remaining three walls were sheet metal Thus, these rearing condi t ions res t r ic ted visual input , but were other- wise similar to our s tandard labora tory ma in tenance of adult ammals. The restr ic ted animals were no t handled for the entire 60-day presurgical ma in tenance period The f loor of the cage did allow some light to en te r and the cages were opened for food rep len i shment

Surgery, Histology and Data A nalys;s

At 85 days of age, half of the enr iched and half of the restr ic ted subjects were randomly assigned to the septal surgical group, the o ther half was assigned to the con t ro l opera t ion group

Surgery was comple t ed with all animals receiving s o d m m pen tobarb i t a l anesthesia (40 mg/kg) supp lemen ted wi th local appl icat ion of hdocame hydroch lo r lde Septal lesions were p roduced electrolyt ical ly by passing 1 5 ma anodal D.C. current for 20 sec th rough the unxsulated tip (approxi- mately 0 5 mm) of a stainless steel pin to a rectal ca thode A Balt imore s te reotaxlc ins t rument , with a modif ied head holder , was used to posi t ion the e lec t rode The modif ica- t ion consis ted of a nose clamp to lmmob thze the head and maintain the surface of the skull in a horlzontaI plane The headholde i d)d not make use of earbars and thus mtra-aural

damage was not incurred The tip of the lesmn elect rode was lowered 5 5 mm from the surface of the dura at an angle of 25 ° toward the mldline at a point 1 0 mm anter ior to bregma and -+2.5 mm lateral to the mldhne . Control- opera ted animals unde rwen t the same procedures except e lect rodes were not lowered.

Upon comple t ion of the exper iment , all animals were overdosed with sodium pen tobarb l t a l and mtracardtal ly perfused with isotonic saline fo l lowed by 10% Formal saline Septal lesioned brains were fixed in 10% Forma lm for at least seven days and then sec t ioned using frozen tts- sue techniques . Each sect ion was 40 u thick and, generally, every t en th sect ion th roughou t the lesion was m o u n t e d for staining Sections were stained with a m e t a c h r o m a t m coun- ter stain for nuclear and fiber regmns (Donovlck, sub- mi t red) and microscopical ly examined to de te rmine the ex ten t of the damage produced by each lesion

A general examina t ion of all our data suggested that nonparametrxc statlstmal techniques were most appropr ia te for data analysis Therefore , Kruskall-Wallace H's, Mann- Whitney U's, and Cht-squares were employed for be tween group compar i sons Correct ions for tied scores were no t used, a l though ties were of ten present Each individual analysis is, therefore , relatively conservative

Postaurgtcal 31amtenance and Testing

Immedia te ly fol lowing surgery all animals, regardless of rearing condi t ions , were re turned to comple te ly s tandard , individual labora tory rat cages They were mainta ined m these cages for the dura t ion of the expe r imen t wi th food and water ad hb except where no ted below Table 1 gives the chronological design of the expe r imen t , which ex t ended approx imate ly 115 days after surgery until the antmals were 200 days of age All rats were weighed weekly th roughou t the postsurgery phases of the expe r imen t

TABLE 1

O V E R A L L I )ESIGN

Days o! Age 25 84 85 99 105 138

Days Postsurgery - - 14 20-53

Treatnlent Rearing ('ondHmn Surgery ~ k xplore I Consume I

139 145

54 60

Handle

146

61

k \plore II

153 192

68--107

T-Maze

193--200

108-115

Consuniell

GROUPS Conlple\ knv kS In = 91 10 rain ad hb

(multiple) test single

LNRICHLD I C In = 11 ) tube

Smlple knv RS (n = 10) 10 nun ad hb

(lsola ted ) test single

RLSTRI('Tt' D RC (n = 91 tube

1 lind Available T Water None Water see

ad lib ad hb Table 2

5 nllrl

daily

5 Inln

da l ly

Water

ad hb

t 0 nun

test

10 mm

test

Water

ad hb

8 trials

per day

8 trials

per day

Water

0 5 hr/day

ad hb

water

ad lib

water

Water

ad hb

*All animals housed mdp, ldually m standard ~ages postsurgery, n/group after histology +Food was available ad hb throughout the study

546 DONOVICK, BURRIGHT AND SW1DLER

I'IG 2 LxploratJon

Explora t ion Tests 1 and H

Two weeks after surgery all animals were individually tested for 10 rain m a dimly lit room in the explora t ion apparatus shown in Fig 2 As can be seen in the figure, the apparatus was symmetr ica l and consis ted of a large, white , complex chamber and a large, gray, simple chamber (each 58 x 46 x 45 cm high) A small (9 x 20 x 20 cm high) detachable start box could be placed be tween the two large chambers In the complex chamber was a dish of sand, a dish of sunf lower seeds, a spout on one wall f rom which water was available, a half gallon milk car ton tunnel open at bo th ends, and two pla t forms (14 x 8 x 15 cm high, and 13 x 7 x 9 cm high) connec ted to each o the r by a ramp ladder. a ramp ladder also led from the f loor to the higher of the two platforms. The complex chamber had black and white vertically str iped walls and a white f loor divided Into four quadrants (23 x 28 cm) The start box and simple chamber were painted flat gray, the floor of the simple chamber was also divided into four quadrants

All animals were placed in a start box for 10 mln prior to testing The start box was then shd be tween the two large chambers Both sides of the start box were raised s imultaneously, allowing the animal access to bo th cham- bers. Latency to leave the start box, tline spent in the simple env i ronment (start box plus gray chamber) and tune spent in the complex env i ronment were recorded In addi- t ion, we recorded the number of squares traversed m each of the two chambers , the number of crossings from one chamber to the o ther , and the contac ts with sunf lower seeds, sand, water spout , and bo th pla t forms. Fnt rances to the tunnel , incidences of gnawing on any object , and inci- dences of cl imbing on to the p la t forms were also recorded Each animal was tes ted twice, the first test occurred two weeks after surgery The second explora tory test was 45 days later, fol lowing C o n s u m m a t o r y Test I (see below) and one week of dally handling Both exp lora to ry tests and intervening procedures were the same for all animals.

Upon examina t ion of the con tac t data (concerning sun- f lower seeds, water spout , sand, tunnel , gnawing, p la t forms)

)est|ng apparatus

obta ined during explora t ion Tests 1 and I1, it became clear that the groups differed in their contac ts with the items While dif ferences among subjects did occui in the relative f requency of contac t ing individual i tems, such d l l te rences did not appear to dlscrllninate among the lour groups All contac t data were therefore pooled to provide a single, total f requency of contac ts for each animal

Copz~ummato O' Te~t 1 and 11

Table 2 shows the design for this por t ion of the exper iment All lneasureincnt ot fluid consumptlol~ was comple ted using a single Richter tube with a I00 Inl capacity Throughout Consummato ry Test I all animals had ei ther a single tube of water or a single tube of e i ther 0 1~2, sodium saccharin or 0 025'7 quinine h y d r o c h l o n d e avail- able 24 hr each day The order ol fluid presen ta t ion was water, saccharin, water, quinine, and water , each presenta- tion was for seven days except that quinine was only avail- able for five days. Fluid c o n s u m p t i o n was again measured near the end of the expe r imen t bo th during and fol lowing exper ience with the water deprivat ion schedule used during the spatial a l ternat ion training (see below)

Spat ia l . 1 ltertmt~oJ~

Training in a spatial a l t e rnahon task was carried out in a T-inaze (center alley 76 cm, arms 61 cm) with two drops of water as a re lnforce inent Approxmaately nine weeks after surgery all animals were placed on a 23 5 hr water- deprivat ion schedule The rats were then given two days, with five trials each day, to explore the T-maze On all explora tory trials bo th water cups were baited with water and the animals were allowed to explore until they found bo th rewards Animals were then given four training days on the spatial a l ternat ion problem (there were four trials per day) before they were switched to eight trials per day for the remainder of testing The reward on trial one each day was on the left side for all animals and was then alter- nated on each successive trial The rats were run until they

P R E S U R G I C A L R E A R I N G , S E P T A L LESIONS, B E H A V I O R 547

TABLE 2

MEASUREMENT OF FLUID CONSUMPTION

Period 1 2 3 4 5

Consume I (20-53 Days Postsurgery)

Single Water NaSac Water QHC1 Water

l luld ad 0 1% ad 0 025% ad

Tube hb ad lib hb ad lib lib

Duration Idays) 7 7 7 5 7

Single Last day

t lind 4 wk water

Tube deprivation

schedule

Duration (days) 0 5 hr

Consume II (108-115 Days Postsurgery)

Water

ad

hb

reached a c r i t e r ion of seven ou t of eight cor rec t responses on two successive days, or for a to ta l of 25 days wi th eight trials a day Tota l t ime to comple t e eight trials was r ecorded for each animal .

Af te r each daily session all an imals were given 0 5 hr of wate r in the i r h o m e cage All animals , Inc luding those who had reached cr i te r ion , were m a i n t a i n e d on this l imi ted wate r schedule unt i l the s tar t of tes t ing in C o n s u m m a t o r y Test II.

RESULTS

H:stolog.l'

Microscopic e x a m i n a t i o n of the his tological mater ia l revealed tha t all bu t two of the septal les ioned animals had damage c o m p a r a b l e to t ha t previously r epo r t ed [ 4 , 5 ] . Typ- ically, lesions were bi la tera l and res t r ic ted to the p recom- mlssural s e p t u m (see Fig 3) The smallest lesions spared the lateral septal nucleus , bu t b i la tera l ly des t royed the media l nuc leus The largest lesions comple t e ly de s t royed the p recommlssu ra l s e p t u m and invaded the ex t r eme ante- r lor s e p t u m and p roduced m i n o r damage in the an t e r io r dorsal cor tex The largest lesions also e x t e n d e d pos te r io r ly and des t royed t issue in the f imbria l nuc leus and, on occasion, the nuc leus t r iangular ls No damage was seen in the p reop t lc nuclei Two animals failed to mee t his tological cr i ter ia for acceptab i l i ty . One animal had a les ion res t r ic ted a lmost exclusively to one side of the sep tum. The o t h e r had a massive in fec t ion which des t royed m u c h tissue in the an t e r io r po r t i on of one h e m i s p h e r e The da ta f rom these two ammals were no t inc luded in the da ta analyses There was no a p p a r e n t co r re l a t ion b e t w e e n the size or locus of the relatively large septal lesions p roduced here and the behaviora l changes observed in les ioned animals

Exploration Tests I and I1

On the first test , two weeks a f te r surgery, enr iched

con t ro l s exp lored the i r e n v i r o n m e n t more vigorously t han animals in the o t h e r groups These d i f ferences were no t as a p p a r e n t w h e n the exp lo r a t i on tes t was repea ted approxi- mate ly five weeks later , fo l lowing C o n s u m m a t o r y Test ing I and a week of daily hand l ing , however , these d i f ferences had by no means to ta l ly d i sappeared La tency to leave the s tar t box and t ime spen t m the whi te comp lex c h a m b e r are ind ica ted m Table 3. Table 4 shows the n u m b e r s of whi te squares and to ta l squares t raversed, and the n u m b e r of t imes the an imal crossed f rom one c h a m b e r to the o ther . Tota l con tac t s wi th all measured media and the n u m b e r of t imes animals ac tual ly c l imbed o n t o e i the r p l a t f o r m are recorded In Table 5 (All of these tables display medians , ranges, and appropr i a t e Kruskall-Wallts H-values.)

On the first test , con t ro l animals left the s tar t b o x m u c h sooner t h a n les ioned animals , bu t Irrespect ive of lesion group, animals reared in the enr iched e n v i r o n m e n t spen t more t ime in the whi t e c h a m b e r t han did those reared in the res t r ic ted e n v i r o n m e n t (Table 3) Once ou t of the s tar t box , enr iched con t ro l s exp lored the i r e n v i r o n m e n t more vigorously t h a n o t h e r an imals , t hey no t on ly moved t h r o u g h the test e n v i r o n m e n t more readily (Table 4) , b u t they also made more con tac t s wi th all objec ts in the com- plex (whi te ) c h a m b e r (Table 5) It is In teres t ing to no te tha t the enr iched septal group spent a lmos t as m u c h t ime as the enr iched con t ro l group in the whi t e c h a m b e r , howeve r the enr iched septal g roup made fewer con tac t s and tra- versed fewer whi t e squares than the enr iched con t ro l rats

When re tes ted , mos t animals left the s tar t box sooner t han they did on the first test (Table 3) Once again, con- trols were fas ter t h a n les ioned animals , and enr iched were fas ter t han res t r ic ted animals. It is s t r ik ing t ha t on this, as well as on mos t o t h e r exp lo r a t i on measures , regardless of the median , the ranges o f scores observed for b o t h lesioned groups spanned the ranges of the scores for b o t h con t ro l groups.

On this second exp lo ra to ry tes t b o t h res t r ic ted groups marked ly increased the a m o u n t of tame they spen t in the

548 DONOVICK, B U R R I G H T AND SWIDLER

1 IG 3 Photomicrograph of the septat lesion m Rat 72-140 Tins v, a typical e\ample oI a large septal lesmn as produced m fin e,

labora Iorv

whi te c h a m b e r , consequen t ly , we now fall to see a slgmft- cant H-value on this measure (Table 3) Most animals explored and moved be tween the two chamber s more read- ily on this second test (Tables 4 and 5 ) As expec ted , these changes were seen best in the res t r ic ted groups However , not ice tha t the enr iched con t ro l s ac tual ly t raversed fewer whi te squares and made fewer to ta l con tac t s on this second test

One of the most in te res t ing exp lo ra to ry measures , which we have not yet discussed, is the n u m b e r of t~mes animals actually c l imbed o n t o the p la t fo rms m the com pl ex (wMte) c h a m b e r As seen in Table 5, none of the animals reared in

the res t r ic ted e n v i r o n m e n t d m l b e d o n t o the p la t fo rms dur- ing e i ther test F u r t h e r m o r e , on Test l, only three of nine enr iched septals c l imbed o n t o the p la t fo rms , whereas seven of eleven enr iched cont ro l s did so By Test II, on ly one of the enr iched septals bu t all of the enr iched cont ro l s got off the g round Animals depr ived of the o p p o r t u m t y to explore heights or those who had received septal lesions subsequen t to such exper ience ahnos t to ta l ly failed to direct ly explore this d lmensaon of the i r e n v i r o n m e n t

Consummatory Test 1 ,rod ll

When fluid re take was first measured three weeks af ter surgery, the expec ted increase m dally fluid in take , normal - ly observed in rats wi th septal lesions, was on ly seen in the res t r ic ted septal group In fact, as seen in Table 6 and Fig 4, the animals in the res t r ic ted septal g roup exh ib i t ed the classic c o n s u m m a t o r y pa t t e rn of rats wi th septal lesions [1,5] In all phases of the e x p e r i m e n t the res t r ic ted septal group d rank more water than any o t h e r g roup Fur the r , while all animals increased thei r daily fluid re take when the water con t a ined sodium sacchar in and decreased thei r in take when quin ine was added these changes were mos t p r o n o u n c e d m the res t r ic ted septal group Rats wi th septal lesions who were reared m the enr iched e n v i r o m n e n t showed only slight e n h a n c e m e n t of the react ivi ty observed in con t ro l animals , there were no appa ren t d i f ferences be tween the two con t ro l g ioups on these measures Inter- es tmgly, the enr iched septal group originally consumed the same a m o u n t of water per day as the con t ro l groups But, by Period 5 of C o n s u m m a t o r y Test 1 (seven weeks af ter ~urgery), the enr iched septals were consuming approxi- mate ly 11 6 m l / l O 0 g body weight of wate r per day compared to 9 7 m l / 1 0 0 g for enr iched cont ro l s and 9 3 m l / 1 0 0 g for res t r ic ted con t ro l s

After the first phase of c o n s u m l n a t o r y test ing, ammals were re tes ted on the exp lo ra t ion task and then placed on a 23 5 hr wa te r -depr iva tmn schedule in p repa ra t ion for t ram- mg on the spatml a l t e rna t ion task (see be low) A measure- men t of wate r re take dur ing the 23 5 hr pet lod was made prior to t ra in ing and then again af te r c o m p l e t i o n of the a l t e rna t ion task On the depr iva t ion schedule , all animals consumed app rox ima te ly 3 6 m l / 1 0 0 g body weight dur ing the 30 mln tha t water was avadable in Period 1 of Consum- m a t o r y Test II When r e t m n e d to ad lib water avaI labihty 15 weeks aftel surgety, the daffy in takes of septal lesioned groups weie greatly increased above the first measu remen t per iod This con t ras t s wi th the general decrease observed m a prior s tudy when animals were ma in ta ined on a con t lnu- o u s a d l i b food and w a t e r s d l e d u l e [4] Indeed, as s h o w n m Fig 4, the restr ic ted septals consumed an average 18.6 m l / 1 0 0 g body weight as compared to the two con t ro l g ioups which consumed a p p l o x t m a t e l y 10 m l / 1 0 0 g body weight Again, the lnore l ecen t postsurglcal lnstorTy includ- ing single cage hous ing and man ipu l a t i on of available fluids, appeared to fu r the r enhance the d i f ferences be tween the enr iched septals and the two con t ro l groups A~ can be seen m Fig 4, the enr iched septals, while d r ink ing cons iderab ly less water than the res t r ic ted septals, consumed a b o u t 14 5 m l / 1 0 0 g body wmght (H = 22 9 dJ = 3, p < 0 001 , all four groups, to ta l Period 2 of ( ' o n s u m m a t o r y 1I test ing) dur ing thls final c o n s u m m a t o r y measu ren len t per iod Clearlk even t h o u g h it was 115 days past thmr surgery, a marked effect of thmr rearing tns to iy was still apparen t . This hlstorTy ~as also apparen t in the average body weight of animals in the

P R E S U R G I C A L R E A R I N G , S E P T A L L E S I O N S , B E H A V I O R

T A B L E 3

EXPLORATION TESTS I AND II TIME MEASURES* (SEC)

Kruskal-Walhs

GROUPS ES (n = 9) R S ( n = 10) E C I n = 11) R C I n = 91 H-Values~-

549

TESTI

Start 59 145 11 15

Latency (15 320) 18 595) ( 1 - 2 0 ) ( 3 - 6 0 )

26 6 b

\Vh~t e 340 191 360 45

Tnne 15 450) (0 460) ( 2 5 5 - 4 4 2 ) (13 470)

13 0a

TEST II

Start 18 53 5 3 9

Latency 15 600t ( 1 - 5 6 0 ) ( < 1 - 1 7 ) (4 13)

27 3b

Wlute 221 362 5 400 313

Time 10-531) ( 4 0 - 5 5 8 ) (115-423~ (204 472)

6 4

Median land rangel start latencles, and trine spent m the white (structured) chamber (~ec) +H-value~ snzmficant at a0 01 bo [)01

T A B L E 4

EXPLORATION TESTS I AND II GENERAL ACTIVITY MEASURES*

Kruskal-Wallls

GROUPS LS (n = 9) RS (n = 10) EC In = 11) RC (n = 9) H-Valuesi

TEST I

Crossings 4 1 18 3

( 1 - 1 7 ) ( 0 - 7 ) ( 3 - 2 9 ) ( 0 - 1 0 )

27 lc

Wtute 23 2 52 6 Squares ( 1 - 3 9 ) ( 0 - 2 l ) (21 61) ( 0 - 2 2 )

30 5 c

Total 46 8 89 26

Squares (6 78) ( l - 2 5 ) ( 2 6 - 1 2 1 ) 14-64)

29 7 c

TEST II

Crossings 18 75 24 16

( 0 - 5 4 ) ( 0 - 3 2 ) (17 31) ( 1 0 - 2 1 )

17 0c

White 70 28 41 4 1

Squares ( 0 - 8 6 ) (2 80) (26 81) (17 50)

7 8a

Total 99 42 100 65 16 0 b

Squares ( 0 - 1 5 5 ) ( 2 - 1 3 6 ) (82 113) (38--89)

*Median number (and range) of crossings between white and gray chambers, white squares traversed, and total squares traversed

+H-values significant at a0 05 b0 01 cO 001

550 D O N O V I C K , B U R R I G H T A N D S W I D L E R

T A B L E 5

EXPLORATION TESTS I AND II SPECIFIC ACTIVITY MEASURES ~

GROUPS

Kruskal-Wallls

FS (n = 9) RS {n = 10) FC (n = 11) RC In = 9) [|-Values+

TEST 1

Total 15 0 5 36 4 70 lb

Contacts ( 0 - 2 7 ) l0 23) (25 54) (0 15)

ON 0 0 1 0

Platforms (0 1) 10-0) (0 4) (0 0)

TEST 11

Total 20 20 14 21

Contacts ( 0 - 3 6 ) (0 37) (5 31) (10 30)

14 1 a

5 2

ON 0 0 9 0 27 9 b

Platforms ( 0 - 6 ) (0 0) ( 3 - 2 2 ) I l l - 0 )

*Medmn number (and range) of total contacts, and ON platforms, l e , instances when an ammal chmbed onto rather platform

+H-values slgmflcant at a0 01 b0 001

T A B L E 6

CONSUMMATORY FES'I I I~LUID INTAK[e (ml) ~

Flmd Water 0 1'; NaSac 0 025 ' ; QHCI

Weeks Postsurgery 3 - 4 5 6 7 8 4 5 6 7"

GROUPS

['S In = 91 1/)3 9 8 112 164

1 9 5 - 1 4 8 ) ( 75 1171 176 163) 1126 2 4 7

R S ( n - 10) 12 2 1 0 4 1 6 0 19 3

( 8 7 - 2 4 3 ) 185 198) 1107 2 4 5 ) 1129 3 0 4

3 6

104 7 8 )

o 5

I C~n = I1) 9 4 8 6 9 0 146 4 6

( 7 4 123 t ( 7 3 - 2 0 0 ) 163 2 1 6 ) (95 2541 I 0 5 651

R C I n = 9 } 104 8 5 9 8 14 8

183 1221 ~73 9 7 ) ~73 1091 1104 213

4 7

(q~ (I 5 61

*lVledlan (and range) of mean dafl~ retake (ml l /bodvwelght {100 g) ~5-da~ exposure period Sit-values slgmflcant at a0 05 b0 01 cO 001

Mann-Whltne~ U {RS vs R(') = ~H-value 0 (~5<p~l) I Mann-Whlmey U ~RS v s EC) =

20, p = 0 05 21 5 , p < 0 02

Kruskal-\Valhs

H-Values ~ 8 6 a l l 8 b l g 2 c 7 7e III 2 b

P R E S U R G I C A L REARING, SEPTAL LESIONS, BEHAVIOR 551

27

23

2 I -

x 1 7 -

E uJ 1 5 - Y <~ I - z 1 3 -

0 ~J 2: I I - ".,

= 9 - =~ =

C~J " -

I X 7 - r~ (.9

I I

\ \

\ \

\ \

I I

24 HR. H20 INTAKE /BODY WT.

16 WKS. POST-SURGERY

FOLLOWING 4 WKS. ON 23.5 HR.

WATER DEPRIVATION SCHEDULE.

A

RESTRICTED -~- - z~ - - - R S (n=lO) 1. SEPTAL J

\ & m ES(n=9) (PRE-SURG. REARING) 7~ 0

~' . , .~..~'n, . - - - Rc(n=9) }CONTRO?~r.,,.,=,,,

I 2 5 4 5

DAYS POST H20 DEPRIVATION SCHEDULE

6 7

- 2 5

121

- 17

1:3

9

5

HG 4 Mean dally water mtake 16 weeks postsurgery Expressed m terms of retake (ml) per 100g bodyweJght for two-day blocks on Days 2 -7

various gorups (,Table 7) There were very shght dzfferences m the b o d y weights when the animals were first received, and there was only a very minor d i f ference be t w een the enr iched and deprived groups at the t~me of surgery Throughou t the remainder of the expe r imen t there was a large and consxstent dafference be tween the cont ro l and septal lesioned groups Within bo th surgical condltzons, however , the animals wxth the enr iched h~story, on the average, weighed more than those f rom the restr icted condi t ions

Spatial Altet natzon Training

Seven weeks af ter surgery all subjects were placed on a 23 5 hr water-depr ivat ion schedule , and training on a simple spatml a l ternat ion task in a T-maze began In this case, lrrespectxve of rearing cond]txons, rats w]th septal lesions were highly ]mpalred in their pe r fo rmance (~2 = 19 47, df= 3, p < 0 001) Only one of the 10 restrxcted septals and one of the nine enr iched septals reached cr i ter ion pe r fo rmance m the 25 full days of training In cont ras t to the perfor- mance of the lesioned rats, e]ght out of nine restr icted

552 DONOVICK, BURRIGHT AND SW1DLER

TABLE 7

MEAN BOD'~ WI~,IGHI (G)

Freatment Receipt Surgery Consume I ('onsunle 11

Nearest Pd 1 2 3 4 5 I 2

25 85 11() 117 124 129 138 190 197 Days of Age

GROUPS

f~S (n = 9) 45 350 429 443 459 440 478 48{1 5(/6

E(" (n - 11 ) 40 350 462 485 499 493 52() 539 564

RS In = 10) 44 342 405 415 434 384 43(~ 448 474

RC In=91 44 347 452 469 489 483 511) 519 554

control ammals and eight out of 11 enriched cont ro l ammals learned the task (medmn days to cri terion were 12 and 1 I, respectively) .

Differences m the behavior of enr iched and restr ic ted control ammals were suggested by (1) the minor d i f ference in the num ber of animals m the two groups reaching crlte- n o n , (2) time to comple te each session, and, (3) observa- tions of the exper imenters . The enr iched controls were, on the average, s lower to comple te the eight training trials per day than any of the o ther groups In fact, four of the enr iched cont ro l ammals refused to move through the run- way for two or three days, only one enr iched septal balked on one day and one restrscted cont ro l balked for three days These ammals were given 30 60 mln, depending on the t empe ramen t of the exper imenter , to comple te the mght trials The refusal to move through the runway ss an interest ing contras t to the exploratson tests, where all enriched controls explored vigorously and as a group were, by far, the most active explorers The dif ference in perfor- mance m these two measures suggests the ~mportant d~stinc- t ion made by Kavanau [10] be tween e x p e r i m e n t e r - a n d subject -mot ivated explora t ion However, despite the stub- bornness of many of the enr iched controls , they did not tend to show the pe r fo rmance impai rment of the septal group~

DISCUSSION

The present investigation shows qmte clearly that early exper ience determines , in part , the effects of septal lesions on behavior Thus, the c o n s u m m a t o r y changes normally associated wi th septal lesmns were best seen in ammals reared in a res tr ic ted env i ronment , a condi t ion mos t closely approximat ing standard labora tory housing condi t ions In view of the data presented by Sorensen and t larvey [14] , wh,ch indicate that decreased brain ace ty lchohne found m rats with septal lesion correlates with increased fluid con- sumpt ion , and the findings of the Berkeley group (e.g , [2] ) concernmg changes in brain ace ty lchohne with rearing condi t ions , it is t empt ing to speculate that the restr icted env i ronment and lesion effects summate to produce at least some of the changes in fluid consumpt ion However, this is

clearly a complex p h e n o i n e n o n First, while it is t iue that , as a group, the restr icted septals drank more water through- out the ad hb testing period, it is also apparent that the~¢ were most sensitive to the quali ty of the available fluid Not only did they increase their intake more than o the r groups when saccharin was the only available fluid, but they also suppressed thmr intake more when the unpalatable quinine solut ion was presented Fur ther , while the enr iched septal group originally drank no inore water than ei ther cont ro l group, after fur ther postsurgical manipula t ions this group of septals drank more water than the controls It is possible that this change in fluid intake was related to the ef tects of Individual housing but this s tudy was obviously not designed to investigate those effects p e r s e Certainly. post- surgical exper ience , in general, should be expec ted to inf luence behavior [ 1 (~ 1

However, not all aspects of the effects of septal lesions were as responsive to piesurglcal env i ronment manipula- tion Ammals with septal lesions, regardless of rearing lnstory, showed the expec ted (e g , [3] t deficit in perfor- mance on the spatial a l ternat ion task The lack of differ- ence be tween the two lesioned groups cannot be simply a t t r ibuted to the long tmle period be tween the presurglcal t r ea tment and the al ternat ion testing since the two lesioned groups clearly showed water consumpt ion d i f fmences after a l ternat ion t rammg Further , the explora t ion data show that there may be a dissociat ion be tween those aspects ot behavior wtuch were measurably af fec ted by exper ience and those which were nol In lhlb co n t ex t though, it IS unpor t an t to again stress that the test ing env l ronment can be most critical m d e t e r n n n m g t h e o u t c o m e Thus, whereas previously we [6] round that the hghtmg condi t ion was most ~lnportant m de te rmining the general m o t o r activity in an open-field maze lor bo th septal lesioned and contro l rats, the present investigation suggested the impor tance of s u b j e c t - vs exper imen te r -mot iva ted exp lora t ion ( l e , explora t ion vs a l ternat ion testing) in at least the enriched contro l group

Finally, it would appear that we can begin to dissociate funct ions of the septal region not only on anatomical bases [3 ,5] , but also with respect to their dependency upon early exper ience If our tlndIngs may b e g e n e r a h z e d , we can con-

P R E S U R G I C A L R E A R I N G , S E P T A L LESIONS, B E H A V I O R 553

c lude t h a t the s o m e t i m e s labile and c o n t r a d i c t o r y resul ts of brain damage , wi th no a p p a r e n t a n a t o m i c a l g r o u n d s for dxstmct~on, m a y be a t t r i bu t ab l e to unobse rved d i f fe rences

in the h i s to ry of the a mma l . Historic and genetac in f luences m a y be e xpe c t e d to in te rac t wi th brain damage

REFERENCES

1 Beatty, W. W and J S Schwartzbaum Enhanced reactivity to quinine and saccharin solutions following septal lesions in the rat Psychon Sct 8: 483-484 , 1967

2 Bennet, k L , M C Diamond, D Krech and M R Rosen- zwelg Chemical and anatomical plactlClty of brain Science 146: 610-618 , 1964

3 Donovlck, P J Effects of localized septal lesions on hlppo- calnpal EEG activity and behavior in rats J comp phystol Psychol 66: 569-579 , 1968

4 DonovJck, P J , R B Bumght and P L Glttelson Bodywmght and food and water consumption m septal lesioned and oper- ated control rats Psychol Rep 25: 303-310, 1969

5 Donovlck, P J , R G Burrlght and E Zuromskl Locahzatlon of quinine aversion w~thln the septum, habenula and inter- peduncular nucleus J comp ph)'stol P~vchol 71: 376-383, 1970

6 Donovlck, P J. and K Wakeman Open-field luminance and "Septal Hyperemotlonallty," Atom Behav 17: 186 190, 1969

7 Fried, P A Septum and behavior A review Psychol Bull 78: 292-310 , 1972

8 [ uller, J L Genetic aspects and regulation of food intake Adv psychosom Med 7 :2 24, 1972

9 Harvey, J A and H F. Hunt Effect ofseptal leslons on thirst in the rat as indicated by water consumption and operant responding for water reward J comp phystol Psychol 59: 49 56, 1965

10 Kavanau, J. L Behavior of captive white-footed mice Science 155: 3770, 1623-1639, 1967

l l McCleary, R A Response specificity in the behavioral effects of hmblc system lesions in the cat J comp phystol Psychol 54: 605-613, 1961

12 Schwartzbaum, J S and P. J. Donovlck Dlscrmunatlon reversal and spatial alternation associated with septal and caudate dls- funtlon m rats J comp phystol Psychol 65: 83-92 , 1968

13 Schwartzbaum, J S, R H Green, W W Beatty and J. B Thompson Acqulsltmn of avmdance behavior following septal lesions in the rat J. comp phvstol Psychol 6 3 : 9 5 104, 1967

14 Sorensen, J r , J P and J A Harvey Decreased brain acetyl- chohne after septal lesions in rats correlation with thirst Phystol Behav 6: 723-725, 1971

15 Wakeman, K A , P J Donovlck and R G Burrlght Septal lesions increase bar pressing for heat in ammals maintained m the cold Plo,stol Behav 5 : 1 1 9 3 - 1 1 9 5 , 1970

16 Wayner, M J , I Greenberg, R Tartagllone, D Nolley, S. Fraley and A Cott A new factor atfectmg the congtunptlon of ethyl alcohol and other sapld fluids Phystol Behar 8: 345-362, 1972

17 Zuromskl, L S , P J. Donovlck and R. G Burrlght Bar pres- sing for illumination change in albino rats w~th septal lesmns J comp physlol Psychol 78: 83-90 , 1972