Dissolution of the Pheromonal Bond: Waning of Approach Response by Weanling Rats’

(ficccived 3 July I c)70 1

I)ISSol.I‘I’IoU 01. ‘1’111~ I’III~KOR1ON:\I. BOSI)

I I3 II! CAECAL EMPTY NO

CONTENTS GOAL CHOICE BOX

21 22 23 24

r

i 25 26 27

AGE OF PUPS IN DAYS WHEN CAECAL CONTENTS REMOVED

;I slrlking correlation

rcsponx lo rnatcrn;il

396

TABLE I

APPROACH BEHAVIOR OF 30 DAY OLD PUPS WHOSE CAECAL FUNCTION HAD BEEN INHIBITED. TO THE ANAL EXCRETA OF STANDARD DAY 16-21 I.ACTATING FEMALES

PUPS

Choice Anal Excreta of Empty Goal

N Lactating Female Box No Choice

Caecectomized Sham operated

Diet S raised in hlillA room

Diet S raised in isolation

Purina diet raised in Purina room

before parturition. This diet was composed by Teklad Mills, Madison, Wisconsin, and consited of in g/kg: 584.5 sucrose. 21 1.0 casein, 104.5 celluiose, 50.0 oil, 40.0 salt, and 10.0 vitamin supplement. Five of the litters were kept with their mothers in a colony room with 20-40 lactating females eating Purina Laboratory Chow, allowing the sucrose diet reared young to experience the odor emitted by those lactating females. Five other litters reared with mothers who were ingesting the sucrose diet were isolated in a separate room.

On Day 30, all of the young were separated from their mothers for 3 hr and then tested in the olfactory discrimination apparatus for an approach response to the odor of the anal excreta defecated in a 3 hr period by a Purina colony mother, 16 -21 days postpartum. The data collected from these three groups were analyzed con- sidering each litter as a single statistical unit [ I].

Results

Table 1 shows the results of both studies. In the first study, caecetomized pups approached the maternal phero- mone on Day 30, while control pups did not (x2 = IO, df = 1, p<O.OI). Interference with caecal function by direct removal clearly extended the time during which the pups remained responsive to maternal pheromone.

In the second study, Purina colony reared pups did not prefer the maternal odor on Day 30 while the pups eating the sucrose diet in the Purina room did (Mann-Whitney U test, U = 1.5, p<O.Ol). Therefore, suppression of caecal development by dietary means also extended responsiveness to the maternal odor. In addition, pups weaned onto the sucrose diet in the Purina colony room approached the colony maternal odor on Day 30 significantly more than the isolated litters weaned on the sucrose diet (Mann- Whitney U test, U = 0, p<O.OOS).

I)ISCIISSION

interference with the maturation of caecal function in the weanling pup extends the period of time that they will approach the familiar maternal caecal odor. These data indicate that the role of caecal odor development in weanlings is critical for the cessation of attraction of the caecal odor of a lactating female.

Although the present data identify the maturation of the

caecum as being critical for approach response cessation. we must speculate about the actual mechanism by which the development of the synthesis and cmlssion of this odor by the weanling causes the reduction in their attraction to the maternal odor. The cessation of the approach response may be explained by considering the mechanism by which the attraction is established and the particular significance of an individual’s own odor.

Leon. Galef and Behse [ 131 have suggested that an odor becomes attractive to young pups by means of a famil- iarization process. Young rats will approach a familiar stimulus, such as the pervasive maternal pheromone, per- haps because of their inherent tendency to avoid un- familiar, and to approach familar stimuli in their environ- ment [4.18]. The maternal odor may therefore be ap- proached in an unfamiliar test environment because it IS the most familiar and therefore. thy Itrast aversive aspect of the situation.

At the time of weaning, the young develop their own caecal odor which, given that the young are innoculated with the maternal enteric biota and initially ingest the diet their mother has been eating, probably resembles closely the familiar caecal odor of their mother. The weaned rats may therefore be capable of producing their own. partiou- larly salient, familiar odor.

The pheromonal bond is characterized by 3 close synchrony between the onset of maternal pheromone emission. which occurs at the time when pups are capable of leaving the nest, and the cessation of pheromone emission which occurs at the time when the pups become independent of the mother. While under the care of the mother, the young not only receive her physical protection and nurturance. but are marked with her caecal odor, the communicative value of which lingers in her absence [ I I I. The value of the maternal scent may be to confer a familiar olfactory environment around the young. which may decrease neophobic responses by the animal in the maternal environment by decreasing the novelty of that en- vironment. When the mother ceases to emit the maternal pheromone in the fourth postpartum week, the young now begin to emit their own similar odor, which might serve to maintain the familiarity of the weanlings’ immediate surroundings. Such a mechanism would facilitate the independence of the weanlinps by eliminating their de- pendency on the mother for providing a familiar olfactory

environment

I~ISSOLI;TIOU 01: IlIt. I’Hf~K041ONAL BOKD 3Y7

Sevrral investigators have suggested that the importance familiar. and hence aversive. envlromnrntal sllmuli with

of an animal king surrounded by its own odor lies in its which they arc innundated. Their ability to deal effzorivcl)

confidcnc,c value to the mdividual [ S,7 I ] If one restates with thclr environment would thcrct, be t‘acililatcd. This

that concept m the trrms that we have been utiliring. the process may find an analogy tn Ihe conc‘cpt of an

onset 01‘ productIon of an Individual’s own odor may be ectohormonc. in which a chemical suhstancc IS rclezscd into

par(icularly effective In increasing the familiarity of the the external environment. inducing ;t bchavloral or physic,-

mimedlatc environment of thr animal. When young rats logicrll response in the emitting individual. In this Case. the

hccomf capable of productng an odor that ~111 familiari,:e etnittsd odor tna! reduce t~rlvironitir’iit;II novlrlt) and

thclr surrounding\. one \~ould cxprct that familiar odor to thereby reduce phobic rcsons2s I,, lhc IntlIvidual in ils

dzcreayc thc:lr Inhrrcnt neophohlc rcsponscs to the un- immcdiatc surroundings.

REFERENCES

Ahhc!,. II. and I:. Ilo\vard. Statistical procedure in dc- vel~~pmrnt;d studies OII spccic\ \vith multiple oft’sprine. DvI,/ P~~&~/Jw/. 6: 330 335. 1973. l%ablck!. .A.. I. O~t;itlolovi. .I. I’art’xk, J. Kolrir. and H. Hihr. I \II‘ of r;id~oi\otopc tcchnqucx for dstcrmining the \\camng ~‘crl~xl ili I~\l~crtm(.nt:~l ,~nitn;~l\. WI,~~siolo,yia hollrf~iosk~l’. 19: 4.5; 10;. 1970. Hahick!. ,\., J. I’.lrixk. I. Ost.tdlilovri and J. Koldr. Initial solid IIKNI Illt.lkr dlld gro\r lh 01’ !'c,ullg rats in nc\ts <If diffcrcnt \,/1‘\. /‘/l\W~l10,41u. holrc~l,M~slol~ 22: 557 -566. lY73. Barnclt. S. ,\. I\perirnont\ on “neophobia” in wild and I;ilx~ratur)~ ~115. /jr. ./. /‘~l~c~l~ol. 1Y: 19.5 -201. I YSX. F\\t,r. R. I f:/l~hq~ o/ .Ih~r~m/\. New York: Plenum t’rcu. 196X. (;3lc‘l. IS. (;.. Jr.. .~nd 51. 31. (‘lark. Mother’s milk and adult prc’\cnc’c: rxo factors tlctermining initial dietary selection h) \veanlin: rat>. .I. ~tu/J. plixrtr,l. f’s~~clrol. 75: 34 I -357. 197 1. (;aIcf. IS. C;.. Jr. & I’. IV. Ilcnderson. Mother’s milk; A dctcrminunt of the feeding prct’?rcncer of u,esnlin:: rat pup\. .I. CC,,,,,,. /Jll~W~l. I’\I~c~irol. 78: 2 I3 -2 IY. 1972.

14.

IS.

16.

17.

IX.

19.

20.

21.

22.

23.

24.

25.

26.

Leon. 51. ~ntl Il. Molt,. Sl,ltcrnal phcromonc: di\crtmm.itioll by preue;lnltnc albino rats. Pl!>mrio/. &,/MI.. 7: 26.5 267. 197 I. Leon. bl. and II. \loltz. ‘I hc devcl~lpmcnt of the phcromonal bond in the albino rat. I’li~.Col. Hdrcll 8: 683 -6X6. 1972. l.utton, c‘. and I.. Clievallier. ~‘opropha~ie chL’7 Ic rat bltlnc. .1. WI!~\id. h-is. 66: 219 -228. 1973. hlickclson, 0. Intestinal synthcsi\ ~11‘ vtt:miin\ in the non- ruminant. 1’ir.s IlontI. 14: I- 95. 1956. Slitchell, II. I.xpcrimcntc on neophohia in wild and laborator) rate: d rccvalu;~tion. .I. uu?rP. /‘lr>.\r~jl /‘\1~c~lrol. 90: I90 I Y 7. 1976. h~lolt/. Ii.. I. Leidahl and I). Rou,l.md. l’rol~>ngation of pheromonal ctnisGon in the rii;~tern;~l rat. fV1.1 sir)/. fklral~. 12: 409 -4 I?. 1974. 51~1~. II. and I). Rc~l~hinr. \l;ltern31 hchavior of primip~lroux and multipar~u~s rats. .I CWW~. 1111 rsiol. /‘\I,( 1101. 60: 4 I7 42 I. 1965. Mykytouyu. II. Reproduction 01 m;mim;1ls m rclatiun to environment;tl odors. J. HcPw~. I,‘c~/.. 19: 433 446, 1973. Raihoud, Y.. ;I. B. Dickinson. 1.. Sacqu~11. II. (‘ttarlicr 2nd (;. Xloquot. l‘hc microllora of the .ditnentary tr:lct 01‘ the rat. ,Itttrls Irtsf. Pasreur. I’clri\. I1 0: X6 1 X76. I Y6h. Kosenhlatt, J. S. The hasi\ ut \ynchr~)n:, in the heha\loral intcrclction hctwccn the mother and her offspring in tltc I;lbor:a tory rat. In: Iktwr~rimtris 01 /ti~o//1 lh~lw~ ior. cditrd 1, 13. 51. I,os\. \!ol. 3: I ondon: .Clcthucn. IOh. pp. 3 45. Rosenblatt. J. S. and I). S. Lchrmztn. Jl;rtcrn;rl hchavior (11’ 111~ l:iboratory rat. In: .Ilurcr~ral Hclla~~ior irr .Ilatvt~mlc, edited 1,~ II. IL. Kcingold. t+\~ York: Wiley. 1963. pp. N 57. Smith. Il. W. The dcvclopmcn t of the tlor;l 01’ IJ~C ;Ilimcnt~r) tr3ct in young animals. .I. fu/lr. /kIl I. 90: 495 5 13. I Y65. \Viesncr. 1%. I’. ;rrld U. hl. Shard. .Ilulf~t~~/ lM~ut~ii)r itr l//c- /&ll. I.drnl)lir:!h: Oliver ;~nd Ih)!.d. 1933.