the effects of maternal isolation on the ontogeny of
TRANSCRIPT
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· THE EFFECis· OF MATERNAL ISOLATION ON THE ONTOGENY.OF
CIRCADIAN"ACTIVITY RHYTHMS AND THE GROWTH OF RAT PUPS
By
.VEANNE N. ANDERSON, B.Sc.
'A Thesis
SUQrnitted to the School of Graduate Studies
in Partial Fulfi~ment of the Requirements
for the Degree-~. -
Doctor of Philosophy
McMaster University
© April, 1985
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MATERNAL ISOLATION AND THE CIRCADIAN RHY'IJlMS OF RAT PUPS,•
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DOCTOR OF PHILOSOPHY (1985)(PsycholoF)
McMASTER UNIVE~SITY
Ham1lton~ Ontario
L
TITLE: The Effects of Maternal Isolation on the Ontogeny ofCircadian Activity Rhythms and the Growth of Rat Pups
AUTHOR: Veanne N. An4er~on, B.Sc. (Colorado State University)
SUPERVISOR~ Professor G.K. Smith
NUMBER OF PAGES: x, ISS,
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Abstract
The circadian rhythms of young animals can be entrained by
prenatal and postnatal maternal cues. The present research
examined the effects of early postnatal matetnal isolation ~n the-
ontogeny o~ the act~vity rhythm in rat pup~. The studies also
examined the effects of different light cycles, as well as other
stimuli which may serve as synchronizers of the activity rhythm
during the postnatal period. Activ~ty rhythms synchronized toa
light-dark (LD) cycle.appeared as early aa five days after birth in
mother-reared pups. This result contrasts with data from other
reports whic~ indicate a late~ onset. Pups reared without their
mothers (AR pups) between ,3 or 4 to 18 days. postnatally on a LD
cycle had rhythms which were of lower ~plitude and of shorter
duration than those in the mother-reared group. AR pups with a LD
cycle and a feeding cycle which approximated the normal nursing
rhythm sh~~~ more synchronization of their activity than pups with
only a LD or feeding cycle. The mean period of the activity
rhythms of pups-raised under c~nstant light deviated the most from
24 hrs. The introduction of a temperature cycle attenuated the AR
pups' activity. These results indicate that the nursing rhythm, in
conjunction with LD cycles, may serve as synchroni~ers of rat pups'
rhythms. However, nursing and LD cycles represent only a part of
the complex postnatal environment which includes temperature, as
well'as other stimuli not investigated here, such as olfacto~y
cues.
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There was also evidence suggesting that rhythmic factors
during the early postnatal period may influence gr~wth. AR pups
with a cyclic feeding schedule had, ~eavier spleens and lighter
livers than animals with a noncyclic schedule. Heavier forebrains
were associated with a predominantly diurnal fe~ding cycle. These
growth factors may, in turn, influence the rhythmicity of locomotor~
activity.
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Acknowledgements
Research and the preparation of ,a dissertation are rarely
conducted in isolation from the cooperation and collaboration of
other pe?ple. The present experiments and manuscript are not
exceptions. First and foremost, I want to thank my advisor, Dr.
Grant Smith, for his generosity and support throughout all stages
of my graduate career.
Thanks also go to Dr. Harvey Weingarten 'for his comments and
to all of the people in the workshop, particularly E. Mitchell who
was responsible for building and helping with much of the equipment
used in the present experiments. In addition, Peter Northcott
taught me the artificial rearing technique and designed some of the
equipment. I would also like to thank Dr. Greg Brown for his ,suggestiona and the use of his laboratory. Associated with his lab
are Mahendra Joshi and Tim Burns who helped with many stages ~f the
pineal NAS study reported in Appendix F. In addition, Barbara
Graham provided aasistance in the design and execution of the'I
pineal NAS study. I am also grateful to Bev Bardy for help with
some of the revisions.
Most importantly, this dissertation is dedicated to Eric, my,
best friend, scientific colleague, and partner in life. He endured
the hardships and shared th~ pleasures of my doctoral work.
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I rTable of Contents
Abstract .' .
Acknowledgements ...........•.................. ' .
List of Figures .
List of Tables 0" ••••••••••• : •••
Chapter 1 - General IntroductionBackground ................•......................Ontogeny of Biological Rhythms •••• '.:•.•••••••••.Maternal Synchronization and Entrainment ••.••••••Outline of Experiments " .
Chapter 2 - Growth of Artifically Reared RatsI~ troduction .Methods •••••••••••••••••••.••••••••••••••••.•••••Resul ts .
. Discussion••••••••••••••••••••••••••••.••••••••• ,
Chapter 3 - The Development of Circadian Act~vity RhythmsIntroduction•••••••••••••••••••• ;' ••••••••••••••••Methods .Result8 •••••••••••••••••••••••• · ~ ••.•.••••Discussion ~ .
Chapter 4 - General DiscussionRhythm Development ••.•.••.•.•..•••.•••..•....••.••Rhythm Development and Grow~h••••••••••••••••••••
'-;" ' Implications for Human Infants ••••• '.' ••••••••••••. '-" ,~ummary••••••••••••••••••••••••••••••••••••••••••
,-Reference Note's ••••••••••••••••••••••••••••••••••••••••••••••
References ' .
Appendix A - Feeding Schedules r ' ..Appendix B - Autocorrelation analysis ••••••••••••••••••••••••
'.Appendix C - Aurocorrelation data ••••••••••••••••••••••••••••
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viii
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15
1624
273039 •44
57636883
100106108109
111. -'"
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136
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~able of Contenta (cont'd)
Page',
Appendix D - Plota of 3-hr meana ••••••••••••••••••• , ••••••••• 145
,Appendix E - Open-field behavior ••••••••.••• '. • • • • • ..... • • • • • • • • • 147
Appendix F - Pineal NAS study of. 153
. ~
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Figure
..... . ~
List of Figures
Follows Page
1
2
3
A rat pup with the gastric cannula"in'place.I
Mean body weights of the AR and MRLD pupsand the control littermates.
Mean body Weig~S ~t weaning.
32
41
43
4
S
6-l~
Mean relative humidity in the water bathincubators."" 64
or
Drawing of the activity transducer. 64
The 24-hr mean activity for the various groups. 69
11-14
16-20
21-25
26
27-31
32-36
37
38-47
The proportion of dark-period activity forthe various,groups.
The proportion of AR animals food deprivedduring each 3-day block.
The proportion of ~ups in the various groupsshowing significant adtocorrelation peaks.
The mean periods of the activity rhythmsfor the various groups.
Frequency distributions of the,periods ofthe activity rhythma for the AR pupa.
Autocorrelation peak areas for the variousgroups.
Time of occurrence of peak 3-hr meanactivity for the vcriouB groups.
Frequency distribution of the time of,occurrence of 3-hr mean peaks of activity.
Three-hr means of activity for the variousgroups.
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Figure
81
01-010
List of Figures (cont'd)
Ekample of an autocorrelation plot.
•Daily 3-hr mean activity for individualpups ,form the various groups.
Follows Page
140
146
•
El
E2
E3
E5
Average daily body weights for mother-reared,intermittently-fed AR, and continuously-fed"AR pups. I
Average time spent g~ooming for control.IAR'and CAR pups.
Average head raises for control, tAR. andCAR pups.
, .Average ,lines crossed for control, !AR, and.CAR pups.
Average pivots for control, IAR, and CARpups.
"F,'
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, List of Tables
Tablej
1 Artificial diet.
2 Sample sizes, humidity, incubatortemperatures and survival rates.
3 Mean organ weights.
~ Mean organ weights for the independentvariables in the regression analysis.
•,,
,
5 Stepwise regression results for organweight data.
,--- 6 Average age at eye opening.
7 Experimental condLtions and water bathtemperatures_
8
9
10
11
12
,13
14
EI
Fl
Sample sizes for the activity data.~
Mu\tiple R2s and slopes for'the ~inea~regression on 24-hr activity.
Stepwise regression results for the,proportion of dark-period activity. ~
!Deviations of the'proportion of dark-periodactivity from 50%.
Occurrence or autocorrelation peaks.
Mean periods for non-FD and FD autocorrelationpeak!! ..
Partial correlations between the organ weightsand the rhythmicity scores.
Mean age at appearance of developmentalindices
N-acetylserotonin (NAS) levels in pinealglands.
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Chapter 1
General Introduction
Background
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\TerminoloJ\Y\
Bi~l rhythms ,are ubiquit~us in both the animal and plant
kingdoms and affect such diverse prOcesses as pupal eclosion, predatory
hunting, and le~rning and memory. Biological rhythms may be defined as
biological processes which recur or vary in intensity at predictable
time intervals (Rusak & Zucker, 1975). The length of the recurring
time interval, referred to as the period (AscHoff. 1979), is used to
classify rhythms 'into three general types. Infradian rhythms have
periods greater than approximately 28 hrs and' encompass phe~omena sucl>'
as female reproductive cycles and se3sonal breeding in some mammals.
Ultradian rhythms can be represented by sleep-state rhythms and feeding
bouts (Bowden, Kripke, & Wyborney, 1978; Daan & Aschoff, 1981) and have
~peri~s less than about 20 hrs. Rhythms with periods of approximately
24 hrs (Halberg & Lee, 1974), Or circadian rhythms,'will be the major
focus of this dissertation. Rhythms are also described by other
pa~ameters. The peak of a rhythm refers to its maximum value whereas
the trough refers to the rhythm's minimum value. A rhythm's amplitude
is the dlfference between the peak value and the tro~gh value .•
Circadian rhythms can be ~ntrained by rhythmic stimuli, c~lled
zeitgebers Or ".time giving". stimuli (Borbeley, 197B~. When entrained,
a circadian rhythm maintains a stable phase relationship with the
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zeitgeber (Enright, 1981b). For example, when entrained to a zeitgeber
such as the light-dark (LD) cycle, a rat's peak of activity might
consistently occur 1 hr after the onset of darkness. The 1-hr lag
between the onset of darkness and the activity peak would be the phase
relationship. When rhythmic data are fit to a cosine function, the
term, acrophase, is used to describe the phase relationship between the
zeitgeber and the function's peak (Enright, [981b). Several zeitgebers
have been identified; for example, environmental pressure cycles
(Hayden & Lindberg, 1968), social cues (Takahashi & Murakami, 1982),
feeding schedules (Bolles & Stokes, 1965; Krieger, 1979; Spiteri,
1982), and most notably, 1ight-dark cycles One factor determining the
0.
'."-,"
entrairting effectiveness of a zeitgeber is the circadian rhythm itself.
Body temperature rhythms in monkeys are more readily entrained by LD
cycles whereas urinary potassium excretion rhythms are more stable 'with
a feeding cycle (Moore-Ede & Sulzman, 1981).'
Besides entrainment another property of circadian rhythms is•
their ability to freerun, or maintain their rhythmicity, in the absence
of cyclic input from zeitgebers (Aschoff, 1981). Locomotor activity
rhythms in rats (Richter,1971) and cortisol rhythms in humans (Milea,
Raynal, & Wilson, 1977) freerun under conditions of constant darkness
(DD). Rhythmicity is also maintained under conditions of constant
~
light (LL), altho~gh under prd{Onge~ conditions, circadian rhythms
may "disappea,," and ultradian rhytnms may predominate (Albers, Gerall,
& Axelson, 1981; Houma & Hiroshige, 1978). The periods of freerunning
circadian rhythma deviate slightly from 24 hrs (entrained conditions)
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and may depend on the lighting conditions present before placement on
LL or DD (Davis & Menaker, 1981).
Analysis of Rhythmic Data
A variety of methods are available for the a~alyses of rhythmic
data (Enright, 1981a). The two types of analyses used for the rhythm
data presented in Chapter 3 will be described here. Day-night
differences in a set of data are frequently used to establish
rhythmicity. This measure is particularly usefu~ for determining
entrainment of a rhythm to a LD cycle when, the rhythm has defini~e
peaks or troughs during the light or dark period. Nonsign11icant
day-night differences do not necessarily imply a lack of rhythmicity or
even entrainment. In these cases the rhythm may be freerunning or
entrainment may be obscured by the manner in which the data were
sampled and/or combined for' analysis.
Time series analyses 'are more sophisticated ways of determining. .
if rhythmicity is present in a set of data. In general, a prerequisite
for the use of time series analyses is a long series of data consisting
of many "daily obse~ations (Enright, 1981a). One of the more simple
analyses is autocorrelation analysis. This involves the calculation
of a product-moment correlation "between the original data series, and
that seme series when it is 'lagged' on itself by some fixed number of
time units" (Enright, 1981a, p.27). Usually a large number of lags are
'examined and the correlations are then plotted against the lag. If a
stable rhythm is present in the data, the plot of the autocorrelations
against the lags will be, cyclic and the lags of the peaks will
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correspond to the dominant period of the data (Enright, 1981a).
Problems in interpreting the results of autocorrelation analyses will
be discussed in Chapter, 3. Unlike some time series analyses,
autocorrelation analysis does not assume a priori the shape of the'
function which best 'describes the data.
Physiological Aspects
Physiological studies of circadian rhythms have focussed on the
'visual system (Rusak & Zucker, 1979). Transections of the, optic nerves
and ,bilateral enucleatlon do not disrupt free running circadian
rhythmicity in mammals, although entrainment to a LD cycle is lost
(Davis & Menaker, 1980; Deguchi, 1975b; Moore, 1975; Richter, 1971).
Lesions of the primary optic tract and/or the accessory optic tract do
not impede LD entrainment in rats (Moore, 1975) although reentrainment
to a shifted 10 cycle may be retarded in hamsters (Rusak ~ Boulos,•
1981). Similar results are seen when the lateral geniculate nuclei, a
'major terminal site for visual fibers, are 1esioned (Dark & Asdourian,
1975; Rusak & Boulos, i981).
The suprachiasmatic nuclei (SCN) , tWf hypothalamic nuclei
located dorsally to the optic
rhythmicity. ~~ SCN receive
,chiasm, are important to circadian
direct input from the retina via the
"
retinohypothalamic tract (RRT) (Picka~Silverman, 1980; Sawaki,
1977). Lesions of the SCN in rats and hamsters disrupt a variety of
ci~cadian rhythms (Redgate, 1976; Saleh & Winget, 1977; Stephan &
Nunez, 1977) although animals may continue to show ultradian rhythms
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