Effect of post-weaning social experience with normal females on the behaviour of adult male staggerer mice interacting with normal females

145

Behavioural Processes, 23 (1991) 145-l 52 0 1991 Elsevier Science Publishers B.V. 0376.6357/91/$03.50

BEPROC

00339

Effect of post-weaning normal

females

staggerer

social

experience

on the behaviour

mice interacting C. Feron’,

C. Baudoin’

with

and M.S.

with

of adult normal

Magnusson

male

females 2

’ Laboratoire d’Ethologie

et Sociobiologie, URA 667 CNRS, UniversitP Paris- Nord, France; ’ Department of Physiology, University of Iceland, 101 Reykjavik, Iceland

93430 Villetaneuse,

(Accepted

18 December

1990)

Abstract Adult

male

behaviour. mutant

staggerer

When

males

experience behaviour.

were

be

groups

after

weaning.

One

with

staggerer

mutant

frequency, producing

greater such

Social

Key words:

normal

were

maintained There

were

by

with

experience

synchrony

with

with

female

in

to different

females

behaviour

and

of such

pattern

mice

between modified

of

social male

experience

and

the two

sexual

5% of the

social

female

of interactions normal

the

between

no

however

that the effects

normal

differences

display

mice

changes

subjected

organization

Social

conditions female

hypothesized

clearly

males

and temporal

females.

behaviours

was

standard

with

We

most

of mutant females.

under

a time

revealed

group

duration

and normal

reared for

able to copulate.

would Two

mice

maintained

the

other

groups

in the

mutant

males

male

behaviour,

in

sterqotypic

Social

experience

a reduction

as scratching.

experience;

Staggerer

mice;

Male-female

interaction

Introduction Numerous In particular influences 1986)

factors early

the choice

and the

determine

experience

pattern

of sexual

the orientation alters

the sexual

partners

of socio-sexual

and pattern behaviour

(d’udine behaviour

of sociosexual

of rodents.

and Partridje, (Coulon,

1981;

1971;

Fillion

Gheusi,

behaviour. and Blass, 1984;

Ward

146

and

Reed,

produce

1985).

Juraska

however,

five

provides

social

environment

structures.

of

young

(Rosenzweig

rodents

can

and Bennet,

1972;

1987).

rearing

(Guastavino,

the

in neuro-sensory

Leon,

standard

behaviour

modifying

changes

et al., 1980;

Under

fore

Indeed,

striking

conditions

1982).

male

When

percent

of staggerer

a model

in which

staggerer

reared

males

for

one

copulate.

mutant

mice

show

month

with

normal

The

the environmental

male

effects

staggerer

on male

no

sexual

females,

mutant

there-

behaviour

can be

determined. The

staggerer

were

first

maternal

and

Bulloch the

numerous

neotic

structural

between ral

limited also

various

the

female’s

patterning

male

Using ence

stereotypic body.

normal

experience

should

pattern

Furthermore,

through

identifying

which

Materials Male

staggerer old

1984).

Staggerer recovery

of

studied

(Baudoin

show et

the

1989).

behaviou-

These

falls.

active

et al.,

synapses

1974).

and repeatedly

emphasized

of

by

shows

Crepe1

numerous

al.,

1982;

it also

et al., 1975;

of lateral

behaviours

also

in size

and Changeux,

number

1978;

induced

development

males

involve

are

Staggerer attempt

role

of

not

males to crawl

females

in

encounters. copulation,

specific

1982).

We

in male

should

behaviour

therefore

of socially

behavioural

of behaviour

a small

number

behaviour

analysis

are most

of individual

after

hypothesized

modifications

behaviour

in the

only sexual

that

social

social

Analysis

of the

behaviour.

be particularly conditioned

we

sensitive

experi-

a specific

appropriate

staggerer

foresee

the

to such

social

males.

possibility

of

experience.

and Methods

at 40 days (1978;

aspects

(Sotelo

of functional

detailed

Mallet

These

and

changes

reduced

atypical

staggerer

scratching

of male

being

the

males

(Guastavino,

changes

to cells

of successful

produce

from

and a large

restoration

and sequence

(Guastavino,

morphological

main

et al., 1968;

normal

during

females

demonstrating

behaviour

The

due

Baudoin

index

show

with

for

to

behaviour

males

as sexual

females,

of copulation

the global

staggerer

normal

compared

display

(Sax

pathologies.

et al. (1962)

Apart

1980)

behavioural

by Sidman

and Purkinje

with

to the failure

under

cerebellum.

fibres

interacting

abnormalities

as well

et al., 1986).

Changeux,

numerous

anatomically

abnormalities

and

the parallel

When

provokes

and

behaviour Misslin

are in the

Mariani

in mice

clinically

et al., 1982;

mutation

1980;

mutation

described

two

mice (C57BL/6)

the

These

mice

were

allow

females

(sg/sg) reared

staggerer

mutant

do not provide in

were

under

bred

conditions

mice

to survive

an environment staggerer

in our

the

sexual

behaviour

males

groups,

each of six 40 day old staggerer

laboratory.

Until

described

by Guastavino

until

weaning

adulthood.

stimulating

enough

(Guastavino,

1982).

to induce We

males

maintained

with

a normal

female

(C57BL/6)

the

therefore females

as

follows: Group or

NF:

Each male

was

individually

caged with

(+/+

+/sg).

Group

SF:

(sg/sg). The females When

Each

male

were

the males

the same type also

was

all 40 days were

individually old

caged

and unfamiliar

65 days old the females

unfamiliar

to the males.

Normal

with to the were

a staggerer

female

(C57BL/h)

males. replaced

females

were

with

adult

transferred

females

of

to Group

147 NF and mutant experience

females

within

At 90 days

X 14 cm)

unfamiliar

sexually

behaviour

was

The

<
with

Group

NF and Group

by a preliminary

assumed

that

five

the

minutes

female

introduction

and

DlGging

excavatory

LQComotion SCRatching animal

with

uses

ANS,

SIS,

PAR

BAS

and

HES

We

ends refer

behaviour

are

later

clock.

females

in these

tested

females

normal by the

an

male’s

an electronic

mounting

we

report

interrupted

the force

limbs

established

conditions.

of which

walks

with

was

male. rnale

We

within

by Baudoin

This

catalogue

only

those

by inactivity

et

contains

occurring

in

and episodes

of

limbs

towards

the

is differentiated

in both

to this

and the

Magnusson, are

olfactory

region,

displayed

recording

haviour

plastic

minutes

to the

activity

to the catalogue

not orientated

and becoming

usually

the female. The

with refer

experienced

accepted

experimental

or hind

a video

Sexual

20

to each cage. The

SF females,,

a sexually

transparent

About

the cage.

behaviours

1982).

partner.

from

GROoming

where

the

forthcoming

paper.

(two-tailed),

by the Fisher

to

male.

by the female’s

animals

during

covered becoming

A

the

animal

sniffing

It involves

male

crawling

immobile,

the body

the male

or head.

This

half covered

by

crawling.

the test was noted

data analyzed

statistical

refer

of the staggerer

as partial

here.

and

back or head of the partner.

partially

Quantitative

presented

behaviours

flank,

characteristic

the female

video

fore

using

if she

to short

walking

the anogenital

is a behaviour

behaviour

and

the

of the social

its mouth.

respectively under

into

movements

is rapid

with

in a makrolon

introduced

respectively.

similar

refers

the similarity

shavings.

was

10 minutes

according

interactive

Exploration

its own

and <
in estrus

categorized

39 individual study:

was

data) under

increased

wood

female

SF males

were

al. (unpublished

put on

encounter

of her

Behaviours

our

for

females,,

detected

process

fresh

normal

recorded NF

was

containing

receptive

then

SF. This

of males.

of age each male

cage (26 X I6

terms

to Group

each group

by THEME aspects

syntaxic

analyses

(frequency

pattern

were

exact probability

at one second software

and

analysis

carried

out

intervals

from

(Magnusson,

1983;

duration)

will

by the

be

the

be-

published

in

Whitney

U test

Mann

test and by the Friedman

of

the Lyon

two-way

a

analysis

of variance.

Results Mutant

males

and the tests. were

failed

We

maintained

to copulate

never with

observed females

with

females

mounting nor

during

behaviour

during

the

tests.

both during

No

the cohabitation

period

the 50 days when

vaginal

plugs

were

males

found

in

any of the females. Group

NF

males,

socially

frequency

of anogenital

compared

to Group

more

frequent

females The the tests

(Figure frequency

SF males.

grooming

conditioned

sniffing

(p < 0.05) Moreover,

behaviour

with

normal

and shorter females

(p < 0.05)

tested

for

females,

periods

longer

with

showed

of scratching Group

(p < 0.01)

a greater behaviour

Mr

males

than

did

showed Group

SF

minute

of

1). and duration

to elucidate

of behaviours

chronological

differences

were

then

between

analyzed the two

for

each

experimental

groups.

148

SCR

ANS

Fig. ‘I. Frequency by

males,

and

and duration of

grooming

GRO

(CRO)

by

sniffing

At

the

beginning

than

crawling males

at the also

of

first

spent

less

time

(Figure

4). The

Group

the

minutes

ten

(df = 9,

SF

Anova

exploration,

digging

given

experience

social

and

exploratory

activities

dating

the seventh

During towards

the

first

minute

5) but

showed

males

(Figure

of the

tests

(SCR) behaviour

(*

Group

NF

female

marks

they

tests

frequent

Group olfactory

significant

of their

6) than did Group

males

sixth high

Chi

females The

SF

durations

activity

in Group

more than males

NF tests NF

(including did

males

modified

of exploration

sqr. = 21.82). spent

behaviour

SF females.

scratching

minute

Group

partial

Group of the

observed

explored

5).

reached

minute self

where

anogenital

displayed 3). The

seventh

at the

NF

more

males

SF (Figure

(Figure

(df = 9, Anova

showed

more

at the

modifications

the test:

minute

more

NF

in Group

behaviours)

a mutant

during

males

no modifications

locomotion

their

(Figure

showed

sqr. = 17.62).

only

from

than

themselves

whereas

with

NF

2). In Group

minutes

males

Chi

Group

(Figure

scratching

test

GRO

and of scratching

at p -C0.05, U test).

encounters

SF males

and fourth

during males

the

did Group

SCR

(ANS)

in the IO-minute

females,

differences

sniffing

ANS

of anogenital

(all sniffing

less

time

categories frequency

exploring of sniffing) decreased

Frequency

2.5r

D-U group I- -_I group

NF SF

2.0-

1.5x : ti z

l.O-

I=

05-

0.0 0 Fig. 2. Frequency

of anogenital

1

I

I

I

1

2

3

4

sniffing

significant

,

,,

5 Mill

6

\ 7

by males in each minute differences

8

9

10

of the lo-minute

at p < 0.05, U test).

tests (*

marks

149

x

3. Number

of males (*

, 1 I I I I

\

NF

group

SF

m-

P-4 \

\ \/\

/’ \Ir’

o-----o

Ii \D’ \ 1 \ 1 \’ n

,

D

grow

.--_I

\

\

I

0

Ftg.

I

I I

D-U

2

displaying

I

I

I

1

I

1

1

J

3

4

5

6

7

8

g

10

partial

marks significant

Min

crawling

differences

in each minute

of the IO-minute

at p < 0.05, Fisher

test).

6

10

tests

Duration 16w-0

group

NF

m--m

group

SF

12 -

D

I

2

3

4

5

7

8

g

Mln Fig.

(*

4. Duration

of self scratching

marks significant

differences

behaviour

by males in each minute

at p < 0.05, U test; 0 marks Friedman analysis

in the two

groups

Anova

sqr. = 20.54

Chi

during

the tests SF)).

that

staggerer

differences

tests

at p -C0.05,

of variance).

(df = 9, Anova

(Group

of the IO-minute

significant

Chi

sqr. = 26.44

(Group

NF);

df = 9,

Discussion Our

study

(Cuastavino, female

confirms 1982).

modifies

Nevertheless,

several

staggerer

male

social

mice

show

experience

behaviours.

Males

disrupted

after

sexual

weaning

anogenital

sniffing

behaviour

with

a normal

behaviour

is

0

t

2

3

4

5

6

7

0

9

10

Mln

Fig.

5. Uuratron

females

test;

significant

constant

during

social

behaviour

the

tests.

Males

and were that,

tests,

behaved

they

respond

with

Group

NF

more

often.

social haviour

more

that

have

behaviours

Fig. 6. Frequency tests

activity

whereas lived

females

were

towards

interactive

behaviours

show

females

they

with

less

Friedman

is

increase

normal

the

staggerer the

more

conditioned social

intense

behaviour.

durations

NF

males

D-_-O

9roup

NF

.

9roup

SF

anogenital we

must

before

the They

behaviour

of the

they greater

foster

males.

experience.

social

By their

of

beginning

Furthermore

in particular

U

and digging)

from

showed

different

to the more

Group

other

right

crawling.

of the encounters;

encountering

for

and by 0.05,

of vanance).

Moreover

females

with

at p i

exploration

experimentally

males

exploration

analysis

differs

partial

by males

differences

reduced.

groups

not

and digging)

significant

(locomotion,

to display

differently

also

marks

(scratching)

experimental

numerous

the

sniff

the

males

frequency interactive

of be-

the tests.

13

IO-minute

test

of both

at the beginning

They

during

the

exploration

(*

at p < 0.01,

exploratory

although

males

tests

behaviour

more

emphasize

(locomotion,

IO-minute drfferences

and of their

The sniffing

actrvrties

of the

stereotypic

scratching

remain of

minute

0 marks

and

increased

their

of exploratory

in each

of snuffing (*

marks

r

Frequency T

(includrng significant

ferences

all sniffing differences

at p < 0.02,

Friedman

_ -_I

behaviours) at p ~0.05, analysrs

by females U

test;

0

of variance).

in each minute marks

significant

of the dif-

151 These

behavioural

experienced both

behaviourally

(Larson with

staggerer

In addition

females

males.

must

the

cause

ability

major

to

the

follow

difficulties

the

ovarian

more

activity

rapid

hesitant

movements the

movements

males

compared for

the

and tendency

to

confined

normal with

differ

are irregular

environment

males

of

interacting

females

of normal

social

to equip

environments

of staggerers

stimulating

more

for the staggerer

social

and normal

cycles

motor

a more

are unlikely

different

Staggerer

coordinated

deficiencies,

females

by the

males.

The

constitute

Locomotive

over of the staggerer

with

are induced

by the staggerer

and physiologically.

et al., 1986).

staggerer

fall

modifications

after weaning

with

females.

normal

them

This

females

may during

the tests. This two

interpretation

groups

physical

holds

of staggerer

disabilities

synchronize because

they

social

are

reduces

the

motor

their

social

Animals

reared

with

behaviour

by rearing

staggerer

increased

stereotypic

studies

Ward are

less

model

well

environment The sis

of their

Our

study

of their sexual

social

experience

nisms

restoring

the

during

experience

development

with

of

the

behavioural

behaviour. after

more

at least

to

females,

sensory-motor

gained

shows later

through until

social

day 90 and

the

behaviour

utility

on adult

of

in some

male

environment,

staggerer

and

on the

Blass,

mutant

1986;

however mouse

behaviour

as a

of the

social

weaning. normal

may

staggerer

females

rather

facility

females

experience

social

females

by promoting normal

social Fillion

with

with

and pro-

be the cause

1981;

after

males

interactions

therefore

socio-sexual

development,

stereotypic environment

SF males.

of perinatal

post-weaning

staggerer

with

might

of Group

and Partridje,

of the effect

sensory

females

(scratching)

However,

weaning

sexual

capacity

Normal

can develop

impoverished

staggerer

(d’udine

effects

to examine

experienced

social

with

males

stimulation

the real importance

The

known.

males

the

pronounced

their

females.

stimulation

staggerer

The

behaviour

of adults

1985).

in which

1976).

males

have shown

behaviour

and Read,

NF

between

more

disrupt

normal

This

of the

by the

disabilities

of

Group

environment

(Fentress,

of the

Many

These

females.

observed

are caused

that

provide

deficit

differences

tests

behaviour. little

duced

socio-sexual

the with

staggerer

so facilitates abnormal

active,

would

behavioural

SF males.

behaviour

highly

than

experience

the

during

of the Group

their

stimulation

that

males

than

affects

in interactive act as one

mutant

the

the ontogenebehaviours,

of the

mecha-

mice.

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