DEVELOPMENT OF SPATIAL MEMORY STRATEGIESIN SQUIRREL MONKEYS (COGNITIVE MAP).

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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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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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