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DEVELOPMENT OF SPATIAL MEMORY STRATEGIESIN SQUIRREL MONKEYS (COGNITIVE MAP).
Item Type text; Dissertation-Reproduction (electronic)
Authors BAILEY, CATHERINE SUZANNE.
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8712859
Bailey, Catherine Suzanne
DEVELOPMENT OF SPATIAL MEMORY STRATEGIES IN SQUIRREL MONKEYS
The University of Arizona PH.D.
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Copyright 1987
by
Bailey, Catherine Suzanne
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1987
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University Microfilms
International
DEVELOPMENT OF SPATIAL MEMORY STRATEGIES IN
SQUIRREL MONKEYS
by
Catherine Suzanne Bailey
A Dissertation Submitted to the Faculty of the
DEPARTMENT OF PSYCHOLOGY
In Partial Fulfillment of the Requirements For the Degree of
DOCTOR OF PHILOSOPHY
In the Graduate College
THE UNIVERSITY OF ARIZONA
1 987
Copyright 1987 Catherine Suzanne Bailey
THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Final Examination Committee, we certify that we have read
the dissertation prepared by Catherine Suzanne Bailey
entitled Development of Spatial Memory Strategies in Squirrel Monkeys
and reccmmend that it be accepted as fulfilling the dissertation requirement
for the Degree of Doctor of Philosophy
if /)-o(~:;. Date I
Date ~~7/O7
~~~ 4L'kJ/f?7 Date J 7
<t (za(p-Z Date
Date
Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College.
have read this dissertation prepared under my that it be accepted as fulfilling the dissertation
Dissert
STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the library.
Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgment of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the" copyright holder.
SIGNED: ~ ~ ~; 01~ --~-----------f~~O-
ACKNOWLEDGMENTS
No work is complete without the thanks that are
due to many people directly and indirectly involved. I
am especially grateful to the members of my committee,
Sigmund Hsiao, Lynn Nadel, Rosemary Rosser and Joseph
Stevens, for their generous advice and willingness to
share their knowledge of things scientific and otherwise.
Any family that puts up with neglect such as I
have forced upon them for the sake of an enigmatic goal
deserves more appreciation than I can possibly give. To
Chuck, Audrey, Dorothy, Charles, Craig and Curtis go my
everlasting gratitude.
To Virginia and Grant go my warmest thanks for
their encouragement and advice concerning some of the
difficult, yet essential, tasks involved in completing a
dissertation.
And I am indebted to John, who put up with many
nights of obsessive behavior and other inconveniences in
the midst of his own busy career. His contribution to
this work was multifaceted.
iii
TABLE OF CONTENTS
Page
LIST OF ILLUSTRATIONS vi
LIST OF TABLES vii
ABSTRACT • • • • • vii i
1. REVIEW OF LITERATURE: THE DEVELOPMENT OF
2.
3.
SPATIAL MEMORY STRATEGIES • • •• • •••
Neural Basis of Spatial Function • Development of the Hippocampus • Aging Hippocampus • • • . ••
Development of Spatial Behaviors .••• Egocentric Behavior ••••••• Allocentric Behavior •••
Spatial Strategies • • • • . • •• Summary........ . ..... . Conclusion and Statement of the Problem
METHOD
Subjects. Apparatus Procedure
Pretraining •••••• Training • Testing ••.••••••
RESULTS.
Tester Reliability •••• Scoring System ••••• Strategy as a Function
of Age and Experience • Strategy as a Function
of Age and Training Site ••. Description of Individual Patterns ••
iv
1
7 10 13 17 17 19 23 27 28
30
30 31 32 34 35 35
37
37 37
37
44 46
TABLE OF CONTENTS -- Continued
4. DISCUSSION
Patterns of Responding ••• Developmental Trends . • • . Primate-Rodent Differences • Future Research
APPENDIX A: TESTER RELIABILITY
APPENDIX B: RAW DATA .
REFERENCES . • . . .
v
56
56 59 62 63
65
67
104
LIST OF ILLUSTRATIONS
Figure Page
1. Schematic of the Hippocampal-Dentate Complex.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
The Quadruple T-maze
Theoretical Route Strategy Response Pattern •
Theoretical Direction Strategy Response Pattern • • •
Theoretical Place Strategy Response Pattern
Age x Test Site Function.
Subjects with Not-Place Patterns of Responding ••••
Subjects with Context Patterns of Responding •••
Route-Like Pattern in Mature Animals.
Route-like Pattern in Adult Animals
Route-like Pattern in 'Young Animals.
Proposed Variation of the Cross Maze
vi
9
33
38
39
40
43
51
52
53
54
55
60
Table
1.
2.
3.
4.
5.
LIST OF TABLES
Perspectives on Space ••
Source Table for Age x Test Site x Experience ANOVA •
Source Table for Age x Train Site x Test Site ANOVA
Frequency of Response Patterns by Type and Age •••
Reliability of Reported Goal Choice.
vii
Page:
4
42
45
47
66
ABSTRACT
When different developmental rates for
psychological processes such as those in spatial memory
exist, they can be linked to relevant brain areas via
thei r d i ff-er"ent deve I opmenta I rates. The hippocampus and
caudate nucleus have been implicated in allocentric and
egocentric spatial behavior changes found in youth and
old age.
Variation in allocentric and egocentric behavior
in squirrel monkeys due to age was examined using a
quadruple T-maze and animals in three age groups: 0.3 - 4
year olds, (n = 12), 5 - 10 year olds (n=12) and
year olds (n=12).
11 - 17
Subjects were trained to go to one of three goals
in the maze from one of two training release locations.
When they reached criterion for consistent responding,
they were given probe trials pseudorandomly interspersed
with the training trials in which they were released from
one of the three other locations.
viii
i X
The 12 test sessions were divided into three
phases consisting of four each. A 3 <age groups> X 3
(probe sites) X 3 <phases) mixed design ANOVA with
~- epea ted
revealed
measures
only a
on the second and
significant effect
third factors
for probe site
<E_ <1,33) 14 . 55' Q_ < . 01 ) using the Geisser-Greenhouse
correction for heterogeneity of variance. The pattern of
r esponding most clearly resembled route and was stable
over testing. Age was not significant although there was
a trend towa r d random behavior in young and
like behavior in older animals.
m o r e ~- o u t e-
Intrinsic maze cues effects on responding were
examined. These data were analyzed using a 3 <age
X 2 <training groups) x 3 <probe sites) mixed
design ANOVA with repeated measures on the last factor,
and again revealed only a significant probe site effect
( E_ ( 1 '33 ) 14 . 55' Q_ < • 0 1 ) . Thus cues intrinsic to the
maze did not affect response pattern.
Only 13 subjects clearly used one of the
three spatial strategies: 6 route, 3 direction, and 4
place. Of the remaining 23 animals 11 were young, 5 were
adult and 7 were mature. Two used a variation of place,
x
three used a combination of strategies, four were
idiosyncratic, 10 used proto-route (route-like, but not
systematic enough to be route) and three were random.
The use of place strategy by animals as young as 4 and as
old as approximately 17 implicates hippocampal changes
occurring outside this age range.
CHAPTER 1
REVIEW OF LITERATURE: THE DEVELOPMENT OF
SPATIAL MEMORY STRATEGIES
One of the most stimulating areas of current
research in psychology concerns how the brain manipulates
and transforms the information that it receives. The
brain could process information in at least two
fundamentally different ways: all inputs could receive
the same processing regardless of their nature, or
processing could be dependent upon the nature of the
input.
This latter notion, that the brain may be
modular, is not new (Gall's phrenology was just such an
attempt) but neuroscience has now provided much knowledge
of how different modules might work.
sizable portion of the steps involved
For instance a
in the initial
processing of sensory information have been specified in
a fair degree of detail and certain commonalities have
emerged, such as the topological properties of neuronal
arrangement that reorganize yet preserve the fidelity of
the signal, or the facilitation that attention provides
1
2
in associating signals from various modalities. Yet
visual perception is defined by procedures quite specific
to that modality; and other modalities may be just as
unique. Understanding how these categories have been
grouped, either according to type of information or task
specificity (Fodor, 1985; Marshall, 1984; Tulving, 1985)
could greatly foster the understanding of brain-behavior
relationships, particularly in less clear areas such as
different kinds of memory.
The perception and use of space is comp I ex .and
rich, providing a domain within which one can examine
issues of modularity. Notions of space have been
addressed at a remarkably wide variety of levels.
Philosophers since ancient times have wondered: is space
itself absolute or relative, a real entity or the product
of the mind's attempt to impose relationships?
Physicists and cosmologists have made striking
discoveries of the nature of our non-Euclidean universe,
but it took the mathematicians to first propose that non-
Euclidean geometries were not only possible, but
logically sound. others have focussed not on space
itself, but on how organisms interact with it.
Biologists have contributed mathematical models of how
organisms optimally use their immediate space,
3
developmental psychologists have proposed theories of how
the geometry of our psychological space may change
ontogenetically, and cognitive psychologists have
proposed ways in which we may mentally represent space.
Of thEse levels the study of psychological space most
directly addresses the issue of modularity.
It appears that we have more than one
psychological space. It is then natural to ask: what
kinds of psychological space are there? Are they
generated with the same, or separate, brain systems? Do
they appear at different times in the lifespan?
The different levels of analysis used to provide
answers to these questions demonstrate an interesting set
of relationships to each other (Table 1).
The distinction between egocentri and allocentric
psychological space rests in the nature of how space is
psychologically determined. The referent in egocentric
space is the self. The locations of objects are
determined by their relationship to the observer. An
object's location may be defined as, "to the right," or,
"on my left," or, "in front of me," or,
other object."
"toward that
However, in allocentric space, locations are no
longer defined by their position relative to the
observer. Rather,
4
they are defined by their metrical
relationships to other objects. This relational
information includes not only direction, but distance as
well. Thus the allocentric representation of an
environment includes the self as one of the objects
represented, and not as the point of reference.
Table 1
Perspectives on Space
referent
strategy
information
neural
There
egocentric egocentric allocentric
route direction place
vestibular visual multimodal
caudate parietal hippocampus
are three categories of behaviors
associated with allocentric and egocentric referents.
These three behaviors may be thought of as strategies for
way-finding. An organism using route strategy will guide
its behavior with the aid of internal information (e.g.
"turn right"). Direction strategy employs landmark
information (e.g. "go toward the sun"). Both of these
are egocentric behaviors. Place strategy, an allocentric
behavior, employs the metrical relationships between
objects to find a location (e.g. "the place in the center
5
between the psychology building and the administration
building").
The kind of information necessary for successful
way-finding also varies with each strategy. At a
minimum, vestibular, proprioceptive and kinesthetic
information is necessary for successful route behavior
and the caudate nucleus appears to play a central
integrative role in processing that information. Several
studies have demonstrated its involvement in egocentric
tasks such as alternation (Gross, Chorover & Cohen, 1965)
or position discrimination (Potegal, 1969) and it appears
to integrate vestibular information from the cerebellum.
A double dissociation ablation study of hippocampus and
caudate nucleus indicated their separate involvement in
allocentric and egocentric space respectively (Abraham,
Potegal & Miller, 1983).
To employ direction strategy, inputs conveying
in addition to landmark information are necessary
vestibular information. In the case of primates this
information is predominantly conveyed by the visual
system, although other modalities, particularly in other
species, may contribute as well. Species differences may
be considerable here. Parietal cortex seems to playa
critical role in the integration of visual spatial
6
information in primates. Egocentric spatial tasks are
impaired by lesions of the parietal cortex. In lesioned
monkeys, route following is impaired (Petrides & Iversen,
1979), and misguided reaching is seen in either dark or
light conditions (Ettlinger & Wegener, 1958). Patients
with parietal cortex damage cannot state which of two
objects is closer, and have difficulty avoiding objects
in their path of travel. That parietal injury generates
misreach in dark conditions, where presumably vestibular
cues are still available, implies that the distinction
between parietal and caudate involvement is not complete.
Place strategy requires much more complex
knowledge of an environment and hence, is typically uses
multimodal information sources. The hippocampus seems to
playa central role in integrating a wide variety of
sensory and affective information into spatial memories.
This structure in particular appears to have a different
developmental time course from most of the other brain
structures.
The remainder of this introduction will discuss
the development of allocentric psychological behaviors as
they relate to the neurobiological development of the
hippocampus.
7
Neural Basis of Spatial Function
Some of the first reports of hippocampal
involvement in spatial function came from Mahut (1971)
who found a specific impairment in spatial reversal
learning in subjects with hippocampal lesions. O'Keefe &
Dostrovsky (1971) and Ranck (1973) then reported the
discovery of cells in the hippocampus that fired in
response to the organism's location in a specific part of
its environment, so called "place" cells. From that time
on a large body of data has been massed in an effort to
clarify the relationship between allocentric spatial
function and the hippocampus (see O'Keefe & Nadel, 1978;
Seifert, 1983 for reviews).
The adult hippocampus, located in the temporal
lobes, is composed of two horseshoe shaped cellular
regions that are intertwined: the dentate gyrus (area
is curved around the dentata, or fascia dentata)
hippocampus proper, which is composed of CAl fibers
(regio superior) and CA3 fibers (regio inferior). CAl
and CA3 pyramidal cell bodies are ordered into layers,
and all their dendritic projections extend in the same
direction. Inputs, mainly from the entorhinal cortex via
the perforant path, synapse onto dendritic processes of
the granule cells in the fascia dentata, pyramidal cells
8
in area CA3 and possibly those in CAl as well (Fig. 1).
Granule cells send their output (mossy fibers) to CA3
pyramidal cells, which in turn sends their outputs
(Schaffer col laterals) to CAl. There may also be
feedback from the Schaffer collaterals into CA3. From
there outputs exit to entorhinal cortex and other parts
of the brain, although there is some feedback from the
limbic area via cingulate and subiculum to CA3 (John &
Schwartz, 1978). Teyler & Discenna (1984) have proposed
that this three-synapse system (granule cells - CA3
pyramidal cells CAl pramidal cells), along with theta
rhythm, can act as a four-dimensional system fOI-
associating information that is stored elsewhere in the
cortex.
The proposed mechanism of this system for
associating and retrieving information is long-term
potentiation (LTP, or long-term enhancement, L TE) • A
brief tetanic stimulus, when applied to cells will cause
9
? .
PI) -------'-----<] --
MI=
CA'3- Pc.
CA1.- 'pe.-
Fig. 1. Schematic of the Hippocampal-Dentate Complex.
CAl-PC = CAl pyramidal cell, CA3-PC = CA3 pyramidal cell,
GC = fascia dentata granule cell, MF = mossy fiber, PP =
perforant path, SC = Schaffer collateral, ? = connection
not completely specified.
10
them to later fire in response to a stimulus that
normally would have been subthreshold. This alteration
in response can last quite some time, weeks or more and
may be the mechanism by which memories are formed
(Barrionuevo & Brown, 1984; Berger, 1984).
A current popular model of hippocampal function
is that the pattern of inputs received from sensory areas
alters, via LTP, a set of synaptic connections. As a
result, a later partial input will be able to retrieve
The spatio-temporal the entire pattern of associations.
"content" of this neural activity is provided by the
cellular and synaptic architecture of the hippocampus and
dentate gyrus (O'Keefe & Nadel, 1978).
Development of the Hippocampus
The development of the
been most thoroughly studied in
differences in brain structure,
between rodents and primates,
hippocampal system has
the rat. Given the
function and behavior
any comparisons with
respect to spatial function will depend on specifying the
primate brain more completely. The fascia dentata
develops more slowly than the rest of the hippocampus.
Approximately 80-90X of the dentate granule cells are
formed postnatally (Altman & Das, 1965; Schlessinger,
Cowan & Gottlieb, 1975). The mossy fiber system appears
1 1
to develop in an organized, topographic, and stepwise
fashion (Bentivoglio, Kuypers, Catsman-Berrevoets & Dann,
1979; Gaarskjaer, 1985). The origin an~ termination of
this fiber system is orderly throughout development and
is reflective of adult organization: it proceeds from
lateral to medial in the hilus and from proximal to
distal in CA3 (Gaarskjaer, 1985).
The primary proliferative zone for granule cells
is near the ventricles in both the rat and in the rhesus
monkey (Nowakowski & Rakic, 1981). In the rat this zone
actively produces granule cells between day 14 and birth.
(Gestation in the rat is approximately 21 days long.)
Somewhere between day 14 and 17 some of these granule
cells stop dividing (Hine & Das 1974) and migrate to the
future site of the hippocampus where they establish a
secondary proliferative zone. The cells collect together
by about the 19th day of gestation and begin to form the
fascia dentata (Bayer & Altman, 1974). It assumes its
mature form by about 28 days after birth.
The granule layer enlarges by adding new cells to
the medial and deep surfaces, but the two zones develop
differently. The superficial layer appears initially
more mature and growth is first medial and then deep.
Six days after birth, all the superficial cells look
12
mature and new cells are added only to the deep part.
The deep layer looks initially immature and grows first
in the medial and deep parts and then only in the deep
parts. By the time these cells have migrated to the
granule layer they have stopped mitosis; but they rest
for a period before beginning to produce mossy fibers
(Gaarskjaer, 1985).
In adult rats the mossy fibers of granule cells
that mature earlier are longer and more divergent than
fibers from later-maturing cells. Gaarskjaer (1978)
suggests that this implies that the time of their origin
is important to their organization when mature. Cells in
the rhesus monkey granule layer are stacked according to
age: the oldest cells are at the outer surface and the
youngest cells at the inner surface of the granule layer
(Duffy & Rakic, 1983; Rakic & Nowakowski, 1981). The
growth ofaxons from the first (oldest) layer of cells in
the superficial layer is orderly and proceeds from
lateral to medial. These probably are from cells
originating in the primary
from the second layer of cells
proliferative zone. Axons
sprout together and push
between the older cells. This is repeated for subsequent
rows until the deep surface is reached. These cells,
which sprout fibers concurrently, are probably derived
13
from the secondary proliferative zone (Eckenhoff & Rakic,
1984). Mossy fibers are found in CA3 after the third
post natal day (Zimmer & Haug, 1978), and from the outset
have an adult appearance (Amaral & Dent, 1981; Zimmer &
Haug, 1978). The formation of synapses between the
perforant path axons entering from the entorhinal cortex
and the granule cell dendrites takes place as cells are
forming, most prominently between days 4 and 11, but the
adult level of complexity is not achieved until about 25
days old (Cotman, Taylor, & Lynch, 1973). The onset of
theta rhythm in CAl cells correlates with the onset of
exploratory behavior which in the rat occurs around day
28 (Douglas, Peterson & Douglas, 1973). The exact age of
hippocampal maturity in primates is unknown, but though
to be between 1 and 2 years of age in human (L. Nadel,
personal communication, 1987).
Aging Hippocampus
Several changes have been noted in aging
hippocampus, but which if any of these represent critical
ones for spatial memory is unclear. The hippocampal CAl
region as well as the dentate gyrus, has a diminished
capacity to regenerate synaptic connections in aged rats
(Anderson, Scheff & DeKotsky, 1986). Aged animals can
restore synaptic connections to preoperative densities
14
but required more time to do so, particularly initially.
Also, hippocampal synapses are capable of attaining the
same amount of long term potentiation in both young and
old animals, but old animals take longer to reach this
maximum and retain it less well (Barnes, 1979; Barnes &
McNaughton, 1980), suggesting that there might be a
decrease in the ability to retain information.
Barnes & McNaughton (1985) examined this latter
notion by comparing rates of acquisition and forgetting
of a spatial memory task with rates of increase and decay
of LTP of hippocampal synapses for both adult and aged
rats. They found a correlation between both measures and
differences between age groups: the aged rats had slower
rates of learning and faster ratc~ of forgetting on the
problem than did the young rats, and their rates of LTP
were also slower to reach asymptote and quicker to decay
than in the young rats. The correlation was particularly
strong for rates of forgetting and rates of LTP decay.
The quality of information entering the
hippocampus may have been degraded. Hippocampal place
cells increase their rates of firing when the subject is
in a well-defined region of its environment. In old
animals, these place fields are less definite, suggesting
that the quality of spatial information received by the
hippocampus has been
0' Keef e , 1983).
impaired (Barnes,
15
McNaughton &
It is also possible that age related changes in
spatial memory are due to specific neurochemical changes,
but investigations in this area have not found robust
effects (for review see Panksepp, 1986). Young and aged
rats that demonstrated differences in spatial behavior on
a radial arm maze also showed age-related differences in
adrenergic, but not cholinergic or GABAergic functioning
in hippocampus (Ingram, London & Goodrick, 1981). But
others have found decreased cholinergic and GABAergic
activity in aged animals (Bartus, Dean & Beer, 1980;
Stl-ong, Hicks,
robust effects
Hsu, Bartus & Enna, 1980).
been found for ACTH,
Neither have
somatostatin,
vasopressin or oxytocin on performance of a short-term
memory spatial task (remembering which of 9 panels was
lit) in cebus monkeys (Bartus, Dean & Beer, 1982).
Thus, although there is evidence that cholinergic
functioning is impaired in both senescence monkeys and
humans (e.g. Bartus, Fleming, & Johnson, 1978; Bartus &
Johnson, 1976; D~achman & Leavitt, 1974), and is involved
in overall cognitive impairment of memory (e.g. Bartus,
1978; Bartus, 1979a; Drachman, 1977), and in particular
may be implicated in Alzheimer's disease (Perry, Perry,
Gibson,
Blessed,
Blessed & Tomlinson,
Bergmann, Gibson &
1977;
Perry,
16
Perry, Tomlinson,
1978; Reisine,
Yamamura, Bird, Spokes & Enna, 1978), there is no clear
evidelice linking this neurotransmitter to spatial memory
impairments associated with old age
Beer & Lippa, 1982 for review).
(see Bartus, Dean,
Barnes & McNaughton's (1985) finding of a
correlation between LTP and aging effects on spatial
performance implicates neurophysiological changes
involved in this process. But investigations of yaung
and old hippocampal CAl cell membrane properties have not
demonstrated any differences in resting membrane
potential, input resistance, spike size and overshoot,
after-potentials or EPSP's (Segal, 1982) . Nevel- the less,
future investigations need to be directed toward
clarifying changes in aging hippocampus that are related
to LTP.
Ultrastructural changes in aging hippocampus have
also been examined. In aged marmosets there is evidence
for increased macrophage activity (Honavar & Lantos,
1985) • There is also an increase in the number of
astrocytes, and thickening of capillaries, but no
neurofibrillary tangles, or senile plaques. In semithin
sections of CA3 hippocampal fields in aged rats, there
17
was approximately a 25% decrease in neuronal density and
increase in glia, but no increase in astrocytes
(Landfield, Braun, Pitler, Lindsey & Lynch, 1981). In
conclusion, although many putative age changes have been
identified, those clearly involved in spatial memory have
not been isolated.
Development of Spatial Behaviors
Correlation of hippocampal development with
spatial behavior changes can help elucidate how
allocentric and egocentric spaces are processed. But
which are the relevant behaviors to use as correlates?
Egocentric Behavior
No ,- ma 11 y ,
egocentrically,
proximal cues are more easily used
whi Ie distal cues, which require
incol-poration of information about distance and
direction, are more easily used allocentrically. Rudy,
Stadler-Morris & Albert (1987) have demonstrated that 17-
day old rat pups are capable of using proximal cues to
solve the Morris water maze task. The pups were not
capable of using distal cues to solve the task until they
were 20 days old and by 23 days displayed adult levels of
performance. If this task makes a true allocentric
demand then it is interesting that the age at which they
successfully solved the task
18
coincided with the
maturation of rat hippocampus.
While motor difficulties cannot explain the
failure of younger pups, it is possible that the visual
system of the pups had not developed sufficiently to
allow use of distal cues at 17 days; yet the remarkably
dramatic improvement in performance of the distal task
over the next week
explanation. This time
of life would argue against this
course coincides with the final
stages of development of the fascia dentata, which is
mature by day 28, the formation of mossy fibers, and
synapse formation which is mature by day 25.
The onset of mature egocentric space (left-right
position discrimination) appears somewhere between 15 and
45 days in rhesus monkeys (Harlow, 1959; Mahut & Zola,
1977) and the capacity to perform position discrimination
reversal appears prior to 3 months (Mahut & Zola, 1977).
Interestingly, the onset of adult levels of object
discrimination occurs at 4 to 5 months (Harlow, Harlow
Rueping & Mason, 1960; Mahut & Zola, 1977).
An important aspect of space perception is the
determination of how far away an object is from the
observer. Depth perception has classically been studied
by observing whether or not a subject will jump from a
high place. Typically,
19
the probability of jumping
decreases as the height of the stand increases (Spalding,
1873; 1875). Many animal species tested in the apparatus
show depth perception (Walk, 1965; Walk, 1979; Walk &
Gibson, 1961). Apparently the perception of depth is
either innate or develops quite early which would be a
biological advantage, particularly for precocial animals
(Spalding, 1873; 1875).
Allocentric Behavior
Observations of wild chimpanzees in the Ivory
Coast indicate selective transportation of appro~riate
clubs and stones used for cracking nuts of different
hardness. The researchers concluded that chimpanzees can
represent Euclidean space, measure and remember dist-
ances, and compare several distances in order to choose
the closest appropriate stone or club (Boesch & Boesch,
1984).
Other investigations have attempted to test
predictions derived from optimal foraging theory, the
idea that the foraging behavior of species has evolved to
optimize the ratio of energy intake to energy expenditure
(Cody, 1974; Schoener, 1971). In one case juvenile
chimpanzees were carried around an outdoor field and
shown up to 18 randomly placed hidden foods (the
20
"travelling salesman problem"). When they were released
their search pattern approximated an optimal route, and
they rarely revisited places they had already been
(Menzel, 1973).
Chimpanzees observed via closed-circuit
television a familiar caretaker walk through an outdoor
field and disappear from sight. When released into the
field the chimpanzees who were exposed to the television
were more successful in finding the person than those who
were not (Menzel, Premack & Woodruff, 1978).
A study using humans that was patterned after the
optimal foraging tasks, required 6- and 8-year old child
ren to retrieve marbles from hiding places along the
periphery of a large room (Cornell & Heth, 1986). Some
were allowed to watch as the 100 marbles were hidden,
while others did not. When allowed to search the room,
both groups of children tended to concentrate their
search activities in certain areas of the room and were
sensitive to clusters of proximal sites: success at
finding a marble led to increased searching nearby. As
expected, those with prior knowledge of marble location
retrieved a high percentage of marbles.
The question of when onset of allocentric
behavior occurs in humans has received much
21
investigation. The answers to that question appear to be
largely influenced by task difficulty (Rosser, 1983), the
type of st imu Ii
response requil-ed
Fishbein, 1974).
used (Eiser, 1976) or the type of
Nigl & (Borke, 1975; Liben, 1978;
Piaget & Inhelder (1967) claimed that
children did not attain adult proficiency of allocentric
space until approximately 7 years. Yet his operational
definition of adult performance required correct
performance of a rather complex task, that of predicting
the perspective of someone else viewing the same scene.
Although these findings were replicated (Laurendeau &
Pinard, ·1970), others have found evidence of allocentric
behaviors at as early as 2 1/2 years of age (Lempers,
Flavell & Flavell, 1977; Masangkay, McClusky, McIntyre,
Sims-Knight, Vaughn & Flavell, 1974).
Kosslyn, Pick & Fariello (1974) taught 4- and 5-
year old children and adults to go from one location to
10 other goal locations. They had no experience going
directly from one goal location to another. They were
then asked to list in order according to distance each of
the goal locations relative to the other goal locations.
The children were only slightly less accurate than the
adults in their representations of the environment, and
the responses of both age groups more closely resembled
22
Euclidean distances than the route distances they had
travelled.
Another illustration of the relevance of task
parameters is the comparison of results from two similar
to each other. In the first, 4 year old children were
led through a series of rooms in which toy animals had
been placed. When asked to recall the animals by their
spatial location, they performed poorly (Hazen, Lockman &
Pick, 1978). However, a second study demonstrated that,
when given the same task in their home environment, ·the
same aged children were successful (Pick & Lockman,
1979), emphasizing the importance of non-developmental
parameters such as the relevance of the task
subject.
Acredolo ~1985) placed infants 6, 1 1
to the
and 16
months in a room facing two windows. After the child
learned to anticipate a pleasant event behind one of the
windows, it was then moved to a new location in the room,
relative to the windows. The 6 month olds responded
egocentrically by repeating the same behavior (e.g.
turning to the right) which had allowed them to see the
event and which now occurred to the child's left. Fifty
percent of the 11 month olds were able to incorporate and
use a cue placed on the correct window. By 16 months,
23
attention to features of space was quite superior to that
of 6 month olds, again indicating competence at &ges far
younger than Piaget predicted.
Spatial Strategies
Given that even very young organisms can perceive
"spatial" cues in the environment, one must ask how these
cues are being used. If organisms are not random in
their ability to find sites, then a logical question is
how are they using that information?
Observations of spatial behavior have led
researchers to postulate three kinds of strategies for
using spatial information. Egocentric space can be
mediated by one of two strategies: route (orienting with
respect to proprioceptive, vestibular and kinesthetic
cues) or direction (orienting with respect to an external
cue) • Both of these employ simple associative processes.
However, place strategies, which use mediate allocentric
space, require a different kind of internal
representation, one consisting of the geometrical
arrangements of objects in the environment. Information
about the environment is encoded such that it can be used
like a map to locate any place in that environment; hence
the term "cognitive map" (Tolman, 1948). Self is treated
as another ob jec t in allocentric space, while in
24
egocentric space it is the central reference point
(Blodgett, McCutchan & Mathews, 1949; O'Keefe & Nadel,
1978). Because allocentric space is associated with
hippocampal functioning, use of place strategies should
depend on this brain system as well.
Evidence for the use of place strategies comes
mostly from investigations employing mazes. The radial
maze consists of a circular platform from which extend a
number of narrow arms, each baited with food at the end.
The food is in a well, visible to the animal only after
it has approached the end of the arm. The number of arms
can vary from 4 to 17, with 8 the most common number
(Olton, 1979). Optimal foraging theory predicts that
organisms should follow the most efficient strategy, that
of visiting each arm only once (Charnov. 1976; Gaffan,
Hansel and Smith, 1983; Kamil & Roitblat, 1985). In
fact, animals are able to forage efficiently in the maze,
and rapidly reach asymptotic performance of visiting each
arm only once (Maki, Brokofsky & Berg, 1979).
Traditional learning theory predicts that organisms
should return to an arm in which they were previously
rewarded (Young, Greenberg, Paton & Jane, 1967); hence it
has been unable to satisfactorily account for radial maze
behavior.
Information
capacities predict
processing models of
25
spatial
that an animal will, as a function of
familiarity with the maze, be able to locate particular
places on the basis of cues external to the maze itself
(e.g. Bowe, 1984; Honig, 1981 ) • Beatty and Shavalia
(1980) placed salient cues around the room and allowed
rats to enter four of the arms of an 8-arm radial maze.
The rat was then removed and the maze rotated 90°. When
the rat was replaced in the maze it responsed as if the
maze had not been rotated. When the cues in the ~oom
were rotated instead of the maze itself, the rat
similarly reoriented its responses in relation to the
moved cues. However, when the environment was homogenous
<curtains and false ceiling) rats resorted to local cues
such as odor. Thus, these .animals responded on the basis
of place strategies when appropriate cues were available.
Other studies support the notion of contextual
use of cues. Organisms such as bees and birds rely on
sensitivity to magnetic fields, celestial cues, and solar
cues to navigate, but when these cues are not available,
they will use landmark cues to navigate. Pigeons are
only unable to return home when released in an unfamiliar
area on cloudy days when solar cues were obscured and
wearing helmets that contained magnetic coils (Roitblat,
26
1982).
Investigations of strategy preference in primates
have typically employed a variation of the T-maze.
Andrews (1984) used an elevated runway maze, consisting
of a long runway containing three goals, which was
intersected by two shorter runways, to examine the use of
three strategies (route, direction and place) in squirrel
and titi monkeys of both sexes. The animals were trained
to go to the center goal from one of the four release
sites at the ends of the shorter runways. Then on
randomly ordered probe trials they were released from one
of the other three sites. Andrews did not find
consistent strategy use within a species, nor did he find
consistent differences in strategy use between species.
But he did find fairly consistent strategy use within
individuals with the exception of one animal who behaved
randomly and two individuals who appeared to switch
strategies part way through the test phase (one switched
from one direction to the opposite direction, the other
from route to direction).
Summary
1 • The notion of separate brain systems for the
processing and use of information appears to hold for the
case of spatial information. The parietal cortex and
27
caudate nucleus are involved in egocentric space and the
hippocampus is involved in allocentric space.
2. The hippocampus matures later than other brain areas
and its maturation corresponds to the onset of
allocentric behaviors in the rat.
3. The hippocampus' unique cytoarchitecture suggests
that it is processing 4-dimensional information.
4. LTP, a possible mechanism for learning, is found in
hippocampus and has properties which vary with age and
correlate with behavioral changes
to age.
in spatial memory due
S. Neurochemical agents probably do not play a critical
role in spatial perception.
6. Other aging changes such as neuronal loss, macrophage
activity or astrocytes may represent events that have not
been ruled out
hippocampus.
as explanations of aging effects in
7. Egocentric behaviors emerge early in life in most
species and appear to do so before allocentric behaviors
emerge.
8. The precise timing and sequence of expression of
these behaviors has not been precisely described.
28
9. Some of the reasons for this
knowledge include non-developmental task
lack of precise
parameters such
as difficulty, stimuli employed and responses required.
Conclusion and Statement of the Problem
Examination of the literature for examples of
egocentric and allocentric classes of spatial behavior
draw developmental distinctions between
Egocentric behavior such as depth perception
the two.
is evident
quite early on, while allocentric behaviors emerge later
in childhood.
What is known about the developmental sequence of
hippocampal neurobiology, namely its slowness to mature
relative to other brain areas, imp lies that behaviol-s
depending on it, such as allocentric place behaviors,
should be likewise slow to mature and indeed this has
been shown to be the case in at least the rat. But
detailed information for primates is not available.
Changes in senescent primate hippocampus relevant
to spatial behavior have yet to be completely identified
and understood as well; nevertheless, the behavioral data
are highly suggestive. As this brain system deteriorates
29
it is likely that the complex processing of information
will become increasingly more difficult and the organism
may be forced to substitute more simple strategies such
as egocentric responding for allocentric cognitive
mapping.
The present research focusses on the behavioral
component of the developmental timecourse of allocentric
spatial perception in a primate species. Specifically,
it addresses two questions: (1) are the changes seen in
spatial strategy use during development and aging in
rodents also seen in primates, and (2) are these changes
the same as have been seen in rats; specifically, is
there a paucity of allocentric strategy use in the very
young and very old relative to egocentric strategy use?
These questions will be answered by examining responses
in a spatial task similar to the one used by Andrews
(1984).
CHAPTER 2
METHOD
Subjects
Subjects were 36 squirrel monkeys, Saimiri
sciureus sciureus, housed in the Psychology Department
Animal Laboratory. Most of the animals' ages were known
to the nearest year; for infants, juveniles, and some of
the young adults the exact dates of birth were known.
For those animals whose ages were unknown (limited to the
oldest individuals) their ages were estimations made from
by dental examination and general appearance.
The subjects were divided into three groups:
infants aged 4 months to 4 years (4 females, 8 males; n =
12), young adults aged 5 - 10 years <2 females, 10 males;
n = 12) and mature adults aged 11 - 17 years (2 females,
10 males; n = 12). Squirrel monkeys are thought to live
to approximately 22 years in captivity, thus, the eldest
animals are mature, but not necessarily senescent.
30
31
Apparatus
Subjects were trained and tested in a quadruple
T-maze with dimensions of 1.8 x 3.7 m which was elevated
1 m from the floor. The entire maze was housed in a 3 x
6 m room with fluorescent lights, partitions,
miscellaneous objects and three doors that together
provided ample peripheral cues.
The maze runway was constructed of 5 x 10 cm wood
painted grey, and enclosed with 1 cm2 hardware cloth to
form a 36 cm diameter tube. The goals were baby food
jars that had been painted grey and glued to the runway.
The release platforms were constructed of grey painted
wood and designed to hold a transport cage against the
open arm of the maze. Wood guillotine doors blocked the
arms not in use on a given trial (Fig. 2).
To make the appearance of the center goal as much
as possible like the other goals (which dead end), a
moveable hardware-cloth guillotine door was placed behind
the center goal; thus on a given trial the animal was
allowed access to either Goals X and Y or Goals Y and Z,
but never all three together.
32
Procedure
Seven persons collected the data. Each subject
was assigned to one tester who trained and tested that
individual. Testers were given a written protocol on
training and data collection procedures and were
constantly supervised until they had mastered the entire
procedure. Following that, weekly supervision ensured "
uniform data collection.
Subjects were tested five days a week. Each
subject was brought to the test room in a transport cage
which was placed on the appropriate release platform.
The subject could not see the maze from within the cage.
Each day's session consisted of 12 trials that were
reinforced with one eighth of a miniature marshmallow
placed in the goal cup.
The subject's choice of goal and goal latency
were recorded. Goal latency was the time it took from
exiting the box to either taking the reinforcer from the
cup or looking into the cup if there was no reinforcer in
that cup. The subject was allowed up to 30 sec to make a
response; if it did not make a response within the
allotted period a score ")30 sec" was assigned and the
33
Across Test Site Beside Test Site
Training Site 1 Beside Test Site*
Fig. 2. The Quadruple T-Maze
* Training Site for Group 2 animals. The distances from
release site to intersection and from intersection to
goal were all 1 m (figure is not drawn to scale>.
34
trial was ended. On test trials subjects were allowed up
to 2 min to make a response. Testers measured latencies
to the nearest sec with a handheld stop watch.
To control for any effects of cues unique to the
release sites, subjects were assigned to one of two
groups with age as a blocking variable. Group 1 was
trained from Release Site 1 and Group 2 was trained from
Release Site 2.
Pretraining
The subjects were given pretraining to
familiarize them with the test environment and eliminate
response biases. On the first day, subjects were
released into the maze and allowed 30 min to explore the
entire maze.
On following days, the reinforcer was attached to
the rim of the cup and subjects made "forced" choice
I-esponses wi th arms blocked off in a pseudo-random
Gellermann (1931) series. Subjects were trained to
return to the release cage at the end of the trial when
the door was opened where they were rewarded with
marshmallow.
Over the trials, the reinforcer was gl-adually
placed lower within the cup until it was at the bottom
and the animal responding from memory. Criterion for
35
advancing to the next phase (training) was responding in
less than 15 sec on 20 out of 24 trials in two
consecutive sessions.
Training
Subjects were trained to go to goal Y by
reinforcing only that goal in free-choice trials in a
pseudo-random Gellerman series. When the animal made 20
correct responses out of 24 responses in 2 consecutive
sessions, testing was begun.
Testing
Once the animals consistently responded to Y,
test trials were inserted periodically to assess the
strategies they were using to find Y. A relatively large
number of training trials is necessary to minimize
effects of learning that occurs on test trials.
Therefore each session consisted of 9 training trials and
3 test trials. The first three trials of each day's
session were always training trials. These were followed
by three triplets of trials, each consisting of one test
and two training trials. The position of the test trial
within the triplet was pseudorandom with at least one
training trial between test trials. Probe trial order
was counterbalanced.
36
The entire testing period consisted of 12 test
sessions. A subject had to choose correctly on at least
7 of the 9 training trials within a session to advance to
the next test session.
CHAPTER 3
RESULTS
Tester Reliability
The testers' reliability was examined to ensure
no differences between them in reporting either the
subjects' choice of goal. There was perfect agreement
among testers for report of goal choice (Appendix A).
Scoring System
The total number of responses to the center (V)
goal for each animal were calculated for each of the test
sites. Thus, an animal using route strategy had a low
score for the across and between sites with a high score
on the diagonal site (Fig. 3). A subject using direction
strategy had a high score for the across site, and low
scores for the beside and diagonal
using a place strategy the scores
sites (Fig. 4). If
for all three sites
were high (Fig. 5). Thus the patterns for responding for
each strategy are distinctly different. Animals
responding randomly have scores of 6.
Strategy as a Function of Age and Experience
The subjects' responses were divided into three
parts: phase 1 (sessions 1 - 4), phase 2 (sessions 5 - 8)
37
No. of y
Responses
Fig. 3.
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Theoretical Route Strategy Response Pattern
38
39
12
1 1
10
9
8
7
6
No. of y 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 4. Theoretical Direction Strategy Response Pattern
40
12 , • • 1 1
10
9
8
7
6
1\10. of Y 5
Responses 4
3
2
1
(I
Across Beside Diagonal
Test Trial Release Site
Fig. 5. Theoretical Place Strategy Response Pattern
and phase 3 (sessions 9 - 12).
41
To examine whether the
three strategies varied as a function of age or learning,
a 3 (age groups) x 3 (test sites)
design ANOVA with repeated measures
x 3 (phases) mixed
on the second and
third factors was performed (Table 2). Results showed a
significant probe site effect (F(1,33) = 14.55, e < .01)
using a Geisser-Greenhouse correction for heterogeneity
of variance, but no other significant main effect or
interaction. Post hoc Newman-Keuls tests revealed all
three comparisons (across-beside, beside-diagonal and
across-diagonal) were significantly different
.01 ) .
The response patterns were stable over the entire
test phase and the overall pattern of responding most
resembled the pattern for route, although route strategy
responses should not differ significantly in the across-
between post hoc comparison (Fig. 6).
scores were near chance in all
The young group's
three test site
conditions. The adult group had a small beside score,
while the mature group had a large diagonal score. Thus,
the patterns of responding show a trend for more route
like patterns as age increased.
Scores indicating the degree of similarity to
perfect place or route response patterns were calculated.
42
Table 2
Source Table for Age x Test Site x Experience ANOVA
SOUl-ce df SS MS F
Between
Age 2 25.12 12.56 3.23 .75**
Error 33 128.51 3.89
Within
Test Site 2 100.12 50.06 14.55* .78***
Age x Site 4 21.64 5.41 1.57 .60**
Err 01- 66 227.13 3.44
Experience 2 1. 01 0.50 0.42 0**
Age x
Expel- i ence 4 7.98 1.99 1.67 .60**
Error 66 78.90 1.20
Site x
Experience 4 0.59 0.15 0.92 0**
Age x Site
x Exp'ce 8 2.99 0.37 0.49 0**
Error 132 100.87 0.76
Total 323 694.85
Note. * Significant at g < .01. ** Power. *** Effect
size.
43
12 Young 6- A
1 1 Adult 0 0
10 Mature t:I--O T 9
8
7
6
1-.10. of Y 5
Responses 4
3
2 1 1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 6. Age x Test Site Function
Only test site is significant (2 < .01).
44
"Routeness" scores were calculated as:
B(O - B) - (A - B)J / A + B + 0,
and "placeness" scores as:
(12-A) + (12-B) + (12-C),
where A = number of B choices from the across site, B =
number of B choices from the beside site and 0 = number
of B choices from the diagonal site.
These scores were then correlated with the
animal's age in years (estimated for those animals in the
mature group). The pearson's correlation coefficients
were +.12 for age and " rou teness" and -.19 for age and
"placeness."
Strategy as a Function of Age and Training Site
To control for nuisance variables associated with
intramaze cues, the subjects had been divided into two
groups and trained from different release sites. A 3
(ages) x 2 (groups) x 3 (test sites) mixed design ANOVA
with repeated measures on the last factor was used to
test for these effects. Again, test site was the only
significant effect found (F(2,60) = 14.55, ~ < .01) using
the Geisser-Greenhouse correction for heterogeneity of
variance (Table 3).
45
Table 3
Source Table for Age x Train Site x Test Site ANOVA
--------------------------------------------------------
Source df SS MS F
Between
Age 2 75.35 37.68 3.22 .75**
Train Si te 1 4.90 4.90 0.42 0**
Age x
Train Site 2 42.54 21.27 1.82 .50**
Error 30 350.50 11.86
Within
Test Site 2 300.35 150.18 14.55* .91***
Age x
Test Site 4 64.93 16.23
Train x
Test Site 2 4.14 2.07
Age x
Train x
Test Site 4 45.39 11.35
Error 60 619.45 10.32
Total 107 1507.55
Note. * Significant at Q. < .01. ** Powel-.
size.
1.57 .60**
0.20 0**
1.10 .30**
*** Effect
46
Description of Individual Patterns
Due to the small number of subjects and the high
amount of between subjects variability response patterns
for each animal were graphed (Appendix B). A description
of those patterns is useful for distinguishing strategy
use from other patterns of responding (Table 4).
Subjects with patterns clearly resembling those
for the three strategies were grouped together. There
were six route users, three adults and three mature. The
youngest route user was 7 years old, while the oldest was
13. Three adults clearly used direction. Only four used
place: one young, one adult and two mature. The young
place user was four years old, which is at the extreme
end of that age group, while the others were 5, 13 and 16
years old. Thus the total number of animals clearly
using a strategy was 13 and all of these animals were 4
years old or older.
This accounted for only 36X of the subjects
tested. So the remaining 23 subjects were examined for
heretofore unidentified patterns of responding. The
subjects were grouped according to whether their scores
were random or systematic. Random was defined as all
three scores between four and eight. Three animals
showed this type of responding: a 3 year old female and
47
Table 4
Frequency of Response Patterns by Type and Age
Pattern Young Adult Mature n
Route 0 3 3 6
Direction 0 3 0 3
Place 1 1 2 4
----------------------------------
Total 1 7 5 13
Rando m 1 1 1 3
Not Place 1 1 0 2
Context 2 0 1 3
Route-like 4 3 4 1 1
Othe r- 3 0 1 4
----------------------------------
Total 1 1 5 7 23
two males, 10 and 12 years old. The number of systematic
responders was significantly different from the number of
random responders <Chi square <1, . ~ = 23)
• 01 ) •
= 14.90,
The 20 systematic pattern users were
Q. <
the n
examined and described. Two, a 1 year old female and a 7
48
year old female, had low scores for all three test sites,
essentially the opposite of place pattern <Fig. 7>. This
pattern could be described as a "win-shift with respect
to place" <or "not place"), just as place strategy could
be described as "win-stay with respect to place."
Thl-ee subjects, 2 - 4 year old males and a 15
year old female, had high scores on across and diagonal
and low scores on beside test sites. This pattern could
be described as contextual use of two of the three
strategies based upon location in the room <Fig. 8>. The
subject could be using route or direction when on one
side <at the training and beside sites), then switching
to place when on the other side of the maze (the across
diagonal sites>. version (and equally
possible) is the subject could be using place or
direction on one side <the across and training sites) and
switching to route on
diagonal sites>.
the other side <the beside and
Of the remaining subjects, patterns for four of
them could not be interpreted. These subjects were a 3
month old male, a 1 year
and an 11 year old male.
old female, a 3 year old male
They all were dissimilar in
p a t t e r n and no common y- e 1 a t i on s h i p of s e x , group o ,- p ,- i o ~-
history could be identified. Thus these subjects
49
probably represent idiosyncratic responding (i.e.,
preference for one or more goals unique to that
individual, although the pretraining procedure was
designed to prevent this).
The remaining 11 subjects all had in common a
pattern that resembled route to a greater or lesser
When these animals were divided into their age
groups an interesting pattern emerged. The four mature
animals showed patterns most clearly resembling route,
with high scores on diagonal and low scores on beside
test sites. Across scores tended to be near random (Fig.
9). The three adult animals showed a more V-like version
of route: beside scores were small, and diagonal scores
were higher than across, but not as much as in the older
group (Fig. 10). The youngest animals had patterns which
least resembled route pattern, although the V-shaped
function was still discernable. The lowest score of the
three sites was still from the beside test site. The
differences between subjects in this group were more
pronounced as well (Fig. 11>'
Originally it had been proposed to study the
hypothesis strengths of each of the three strategies on
67 animals. Due to technical difficulties the number of
animals available for study was considerably reduced;
50
thus, it became impossible to meaningfully analyze
hypothesis strength scores as a function of age using
MANOVA.
Latency data had been recorded for time to reach
choice and time to reach goal. These were to be used in
an analysis to determine whether latency measures were
affected by the animal's choice of strategy. But the
accuracy of these data (measured to the nearest sec) was
not sufficient to permit evaluation. Also, very few
animals used allocentl-ic strategy which preculded
comparing latencies for egocentric and allocentric
strategies. either between or within subjects.
51
12
11
10
9
8
7
6
No. of Y 5
Responses '+
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 7. Subjects with Not-Place Patterns of Responding
52
12
11
10
9
8
7
6
No. of Y 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 8. Subjects with Context Patterns of Responding
53
12
11
10
9
8
7
6
No. of Y 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 9. Route-Like Pattern in Mature Animals
54
12
1 1
10
9
8
7
6
No. of Y 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 10. Route-Like Patterns in Adult Animals
55
12
11
10
9
8
7
6
No. of Y 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Fig. 11. Route-Like Patterns in Young Animals
CHAPTER 4
DISCUSSION
Patterns of Responding
The results of this study show that most subjects
used route or route-like patterns of responding.
However, this contrasts with the results Andrews obtained
in his study of spatial strategy use in squirrel and titi
monkeys, although he did find fairly consistent
responding within sUbjects. There are several possible
explanations for the paucity of allocentric behaviors in
the present study.
One possible explanation is that the task took
place in a room novel to all of the subjects. Their only
experience with the room was received from the viewpoint
of within the maze itself and its four entry points. If
Andrews' animals were familiar with the maze setting,
then they may have had a richer representation of the
setting and this may have led to more place strategy use.
Forming an allocentric representation of an
environment may require more than merely experiencing
that environment: it may be that the experiences must
involve multiple perspectives rather than mere
repetition. If the subjects had received a training
56
57
experience involving multiple perspectives or tested in a
room with which they were already familiar, the number of
animals using allocentric strategies might have been
greater. This is consistent with the fact that the
animals did not change patterns of responding as a
function of
received.
how much testing experience they had
The ability of Gibson's infants to perceive depth
changed as a function of experience, but the experience
was of particular kind: they received their experience by
actively moving around in their environment, and this
exploration may extract information conceptually
different from that received during repetition of routes.
Another possible explanation for the predominance
of route-like behavior is that the maze was enclosed in
wire mesh to confine the animals to the maze runways. It
is possible that the visual barrier created by the mesh
was sufficient to discourage use of distal cues in the
room. However, this is unlikely in view of the fact
subjects typically did a large amount of visual scanning
of the room, particularly during the first experiences in
the maze.
That route, place and direction account for only
some of the systematic responses is interesting. With
58
the exception of ideosynchratic and random responders,
none of the other behaviors seen were fundamentally
different from route, direction or place, and indeed, it
was possible to conceptualize them as variations of the
original three strategies. Win-shift with respect to
place is consistent with optimal foraging theory and
conceptually similar to place. But if it truly
represents use of an allocentric representation, then
hippocampus must be functional by at least age 1 in the
squirrel monkey,
place user.
which was the age of the youngest not-
If context represents the combined use of two or
more strategies, then distinguishing contextual from non-
contextual use of strategies will be difficult in the
present maze. Half of the possible responses represent
confounded strategies and this presents a serious problem
in trying to estimate hypothesis strengths, the usual
measure of strategy.
redesign a maze such
Instead, a better approach is to
that one and only one strategy is
associated with a given behavior. The parking lot maze
represents one such possible design. When this variation
of the cross maze is physically rotated 180 0 or 90 0 and
displaced half of the width of the maze, then each arm
then is associated with only une of the three strategies
59
(Fig. 12) • Consistent use of contextually based
strategies would then be easy to identify. An animal
using route and place contextually would have route
responses when the maze is in one orientation relative to
the setting
orientation.
and place responses when it was in another
Developmental Trends
Although age effects were not significant
overall, the trends are conceptually quite interesting.
First, those animals clearly using
all five years or
route,
older.
direction or
A current
controversy concerns whether allocentric perspectives
supplement egocentric perspectives. Piaget
claimed that allocentric perspective replaced egocentric
perspective as age increases, but route was well-
represented in the oldest groups. The present data argue
that allocentric perspective becomes available in
addition to egocentric perspective rather than replacing
it.
Second, it is unexpected that clear use of route
was not found in animals under 5 years of age,
particularly when position discrimination tasks elicit
egocentric behaviors in rhesus of 15-45 days, and rhesus
are slower to mature than squirrel monkeys. The age of
60
B
Route Directio n
" JI
I X Iplace
A
Fig. 12. Proposed Variation of the Cross Maze
Rotation and displacement allows for detection of
unconfounded strategy use. A = original training release
location, B = test release location, X = training reward
site, --- = position of maze in training,
of maze in testing.
= = position
61
the youngest clearly route user was 7 and there were four
young route-like users.
The maze used
conceptually difficult
in this study may represent a
spatial task. The analogous task
in humans was too difficult for 3-6 year olds to solve,
even though egocentric behaviors have been found in much
younger children when different tasks were used. The
tasks three probe sites can be viewed as spatial
involving
displacement
displacement
two
of
some
original training
kinds
some
numbel-
site.
of problems: a horizontal
distance and a rotational
of degrees relative to the
In this situation the beside
site represents a task with horizontal displacement but
no rotational displacement and the other two sites
represent horizontal
rotations.
displacements accompanied by 180 0
The horizontal displacement involved in the
beside task is a 2 m distance. It is possible that the
.stimulus array is not sufficiently changed to affect the
animals' responding. However, the 180 0 rotation involved
in the across and diagonal sites presents the animal with
a new visual array as it leaves the release box. If 0 0
displacement is an easi el- task to solve than is 180 0
displacement and the differences between the horizontal
62
displacements involved in the three task sites are
trivial, then the beside test site should be the easiest
of the three tasks to solve. This could explain the
lowered scores in the beside condition for animals
showing route-like trends.
Primate-Rodent Differences
Primates appear to be using the same three
strategies that have been presented in the rodent
literature. There have not been any reports of t~ese
strategies used in different combinations or variations.
Thus it is interesting that
demonstrated patterns of this type.
a few individuals
Primates may be more
adept at altering strategies to suit new situations.
There is an increase in route use in rats as they
become older and this trend is also seen in the present
study in primates. Although route strategy predominated
over place strategy in all age goups, it is possible that
with a different training protocol, more place use by
adults might have been seen. It is also possible that
the T-maze and the quadruple version of it are
functionally different tasks. The T-maze is typically
moved with respect to the environment for probe trials,
while in the quadruple version, the animal is moved with
respect to the environment. Or primates may simply be
more sensitive to the parameters of the task
are rats.
Future Research
63
itself than
The results of this study give hints about when
allocentric behavior develops or declines. Place users
ranged in age from 4 to approximately 16, nearly the
entire span of ages tested. (If the win-shift version of
place is interpreted as allocentric then the span becomes
even wider.) Questions addressing the development of
hippocampus and allocentric behaviors should focus on
animals younger than about 4. If human hippocampus
matures between 1 and 2 years of age, then hippcampal
development in squirrel monkeys may occur sometime less
than that.
It seems likely that the eldest animals in the
study do not represent truly senescent animals. What we
know of the variability in onset of senescence in humans
leads us to predict a likewise variability in non-human
primates. It will also be important to have accurate
ages on old subjects.
The choice of task in discernment of egocentric
from allocentric behaviors will also demand attention.
Piaget's tasks have been criticized for their conceptual
difficulty, and the same criticism may be relevant to
some of the animal tasks. Care will also have
64
to be
taken with such variables as novelty, type of
familiarization procedure used and context.
The use of combinations or
strategies bears further investigation.
variations of
This represents
a phenomenon which may have some theoretical importance,
particularly with regard to context. How much of a role
context may play in primate-rodent differences in solving
spatial tasks is unknown.
And a last question is: just how much and how
many different perspectives of an environment must a
subject experience before a mental representation of that
environment is formed? Is a mental map something more
than merely the sum of the multiple parts (associations)
that went into it?
APPENDIX A
TESTER RELIABILITY
Interrater reliability was examined for reports
of goal. The testers could not be tested all at the same
time so they were divided into two groups (1 and 2).
Group 1 observed and recorded data on one animal for one
entire test session consisting of 12 trials, and group 2
did the same on a second animal.
The animal's goal choice as reported by the
testers in both groups are listed in Table 6.
perfect agreement among testers.
65
There was
66
Table 5
Reliability Of Reported Goal Choice
--------------------------------------------------------
Group 1 2
------------------- -------------
Testel- 1 2 3 4 5 6 7
Goal B B B B C C C
B B B B B B B
B B B B C C C
B B B B B B B
B B B B C C C
B B B B C C C
C C C C C C C
B B B B C C C
B B B B B B B
B B B B B B B
A A A A B B B
B B B B C C C
Note. Testers' reports were in perfect agreement.
APPENDIX B
RAW DATA
Individual patterns of responding are given for
each animal.
center goal
Each score represents the total number of
(B) responses the animal made in 12 test
sessions from each of the three release sites.
response level is 6.
67
Chance
68
Subject: Silver
Sex: Male
Age: 17 Years
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
69
Subject: Seneca
Sex: Male
Age: 0.3 Year
12
1 1
10
9
8
7
6
~ No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Mario
Sex:
Age:
No. of B
Responses
Male
0.5
12
11
10
9
8
7
6
5
4
3
2
1
0
70
Year
Across Beside Diagonal
Test Trial Release Si te
Subject: Lee
Sex: Male
Age:
No. of B
Responses
1
12
1 1
10
9
8
7
6
5
4
3
2
1
0
71
Year
Across Beside Diagonal
Test Trial Release Site
Subject: Melanie
Sex:
Age:
No. of B
Responses
Female
1 Year
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across
Test
72
Beside Diagonal
Trial Release Site
Subject: Velvet
Sex:
Age:
No. of B
Responses
Female
1 Year
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across
Test
73
Beside Diagonal
Trial Release Site
Subject: August
Sex:
Age:
No. of 8
Responses
Male
3
12
11
10
9
8
7
6
5
4
3
2
1
0
Years
Across
Test
74
Beside Diagonal
Trial Release Site
Subject: Duncan
Sex:
Age:
No. of B
Responses
Female
3 Years
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across
Test
75
Beside Diagonal
Trial Release Site
76
Subject: Bobbie
Sex: Female
Age: 3 Years
12
11
10
9
8
/ 7 / /
/ /
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Max
Sex: Male
Age:
No. of B
Responses
4
12
11
10
9
8
7
6
5
4
3
2
1
0
77
Years
Across Beside Diagonal
Test Trial Release Site
Subject: Puff
Sex:
Age:
No. of 8
Responses
Male
4
12
1 1
10
9
8
7
6
5
4
3
2
1
0
78
Years
Across Beside Diagonal
Test Trial Release Site
79
Subject: Sparkey
Sex: Male
Age: 4 Years
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
80
Subject: Spack
Sex: Male
Age: 4 Years
12
1 1
10
9
8
7
6
No. of 8 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
81
Subject: Ben
Sex: Male
Age: 5 Years
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Si te
Subject: Darwin
Sex: Male
Age: 5 Years
No. of B
Responses
12
11
10
9
8
7
6
5
4
3
2
1
o
\ \ \
\
Across Beside Diagonal
Test Trial Release Site
82
Subject: Sherman
Sex:
Age:
Male
5
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
o
Years
Across Beside Diagonal
Test Trial Release Site
83
84
Sub j ec t: D. J.
Sex: Male
Age: 6 Years
12
1 1
10
9
8
7
6
No. of B 5 ,
Responses 4 '\. •
3
2
1
0
Across Beside Diagonal
Test Trial Release Si te
Subject: Jonathan
Sex:
Age:
No. of B
Male
6
12
1 1
10
9
8
7
6
5
Responses 4
3
2
1
o
Years
,
Across Beside Diagonal
Test Trial Release Site
85
Subject: Jamie
Sex:
Age:
No. of B
Responses
Female
7 Years
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across
Test
86
Beside Diagonal
Trial Release Site
Subject: Olivia
Sex:
Age:
No. of B
Responses
Female
7 Years
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Across
Test
87
Beside Diagonal
Trial Release Site
Subject: Busby
Sex:
Age:
No. of B
Responses
Male
8
12
11
10
9
8
7
6
5
4
3
2
1
0
88
Years
Across Beside Diagonal
Test Trial Release Site
89
Subject: Basil
Sex: Male
Age: 9 Years
12
1 1
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Chester
Sex:
Age:
No. of B
Responses
Male
10
12
1 1
10
9
8
7
6
5
'+
3
2
1
0
Years
Across
Test
90
Beside Diagonal
Trial Release Site
Subject: Phillip
Sex:
Age:
No. of B
Responses
Male
10
12
11
10
9
8
7
6
5
4
3
2
1
0
Years
Across
Test
91
Beside Diagonal
Trial Release Site
92
Subject: Theodore
Sex: Male
Age: 10 Years
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
93
Subject: Alex
Sex: Male
Age: 1 1 Years
12
1 1
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Nicholas
Sex:
Age:
No. of B
Responses
Male
1 1
12
11
10
9
8
7
6
5
4
3
2
1
0
Years
Across
Test
94
Beside Diagonal
Trial Release Site
Subject: Whiskers
Sex:
Age:
No. of B
Male
11
12
11
10
9
8
7
6
5
Responses 4
3
2
1
o
Years
/
/
Across Beside Diagonal
Test Trial Release Site
95
Subject: Wheezer
Sex:
Age:
No. of B
Responses
Male
12
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Years
Across
Test
96
Beside Diagonal
Trial Release Site
97
Subject: Chip
Sex: Male
Age: 13 Years
12
1 1 , ,
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Rodney
Sex:
Age:
No. of B
Responses
Male
13
12
1 1
10
9
8
7
6
5
4
3
2
1
0
98
Years
Across Beside Diagonal
Test Trial Release Site
99
Subject: Sean
Sex: Male
Age: 14 Years
12
1 1
10
9
8
7
6
\ No. of B 5 '" '\ Responses 4 "" ~ 3
2
1
0
Across Beside Diagonal
Test Trial Release Site
100
Subject: Patches
Sex: Female
Age: 15 Years
12
11
10
9
8 I 7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Si te
101
Subject: Cinnabar
Sex: Female
Age: 16 Years
12
11
'" 10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Site
Subject: Admiral Harry
Sex:
Age:
No. of B
Responses
Male
17
12
1 1
10
9
8
7
6
5
4
3
2
1
0
Years
Across
Test
102
Beside Diagonal
Trial Release Site
103
Subject: Lloyd
Sex: Male
Age: 17 Years
12
11
10
9
8
7
6
No. of B 5
Responses 4
3
2
1
0
Across Beside Diagonal
Test Trial Release Si te
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