Origins of habituation research - The University of Texas at Dallas

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Habituation
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Running Head: HABITUATION IN INFANCY RESEARCH








Habituation in Infancy Research: Beyond Novelty Preference

Literature Review

Ana
-
Maria Mata
-
Otero

The University of Texas at Dallas
Habituation
2

The Origins of

Habituation Research

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4

Sensory Adaptation and Effector Fatigue

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6

Characteristics of Habituation

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8

Orienting Reflex

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14

Neuronal Model Theory

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15

Dual
-
Process Theory

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17

Developmental Aspects

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19

Types of procedure

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19

Familiarity Preference

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21

Novelty Preference

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23

Hunter and Ames’ Multifactorial Model

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25

A More Complex Ca
se: Categorization

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28

Conclusions and Future Directions

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31

References

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Habituation
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Hab
ituation in Infancy Research: Beyond Novelty Preference




The core issue in developmental psychology has been some version of the ancient
nativism/empiricism controversy. This certainly goes back as far as Plato. In Plato’s
celebrated dialogue the
Meno
, S
ocrates presented an experiment done on a child

(82b
-
85b)
. It is almost certain that that experiment was imaginary. Nowadays we can tackle the
problems that vexed Plato, categorization and identification,
by

perform
ing

real
experiments. The vast bulk of th
ese experiments rely on the use of one or another
habituation technique. Habituation is normally thought of as the simplest form of
learning. That may be true, but habituation is far from simple, and possibly too complex
to be used as an indicator of perce
ptual/cognitive processes.

Learning is traditionally defined as the process by which adaptive changes in an
organism’s behavior arise as a result of experience. Habituation is an aspect of learning
that is characterized by a decrease in response to a repea
tedly presented stimulus.
Because this type of learning occurs in the absence of any apparent associated stimulus, a
reinforcer or other consequent, it is considered to be nonassociative in nature. In this
respect, it is widely considered to be the simples
t form of learning exhibited throughout
an expansive range of organisms. A classic example of habituation is the responsive
behavior of the snail
Helix albolabris
to noxious stimulation
.

When a shock is given
through the surface on which the snail is walki
ng, the animal withdraws its tentacles for a
short time. If the shock is repeated regularly at constant intensity, the magnitude and
duration of the tentacle withdrawal gradually decreases until the animal becomes
accustomed to the stimulus. The present pa
per aims to present a body of research that
may elucidate the time
-
course and underlying mechanisms in infant habituation.

Habituation
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The Origins of Habituation Research

Humphrey (1933) is commonly credited with the discovery of habituation,
providing the first compr
ehensive review of the topic and establishing its fundamental
importance. He noted that habituation is a ubiquitous process that can be observed
through a wide variety of organisms, from the single celled amoeba to humans. Examples
of responses include the

withdrawal response in the earthworm (Roberts, 1966), the body
withdrawal in the snail (Cook, 1975), the escape response in the crab (Rakitin, Tomsic, &
Maldonado, 1991), the tail
-
flip response in the goldfish (Rodgers, Melzack, & Segal,
1963), the mobbin
g reflex of the chaffinch (Hinde, 1960), the rotation nystagmus in the
dog (Collins & Updegraff, 1966), and the startle reflex in the human infant (Engen,
Lipsitt, & Kaye, 1963).

It is most probable that habituation is a term denoting many processes. Hump
hrey
cautioned that different mechanisms are likely to be involved in all of the aforementioned
cases. In animals without a central nervous system such as Aplysia or “spinal” subjects
whose spinal cord has been severed from the brain, habituation is a rela
tively simple
phenomenon involving processes local to sensory systems (Squire & Kandel, 1999). One
should not expect the habituation observed in more complex behaviors to involve exactly
the same mechanisms as those responsible for comparable behavioral ef
fects in more
simply reflexive responses.

Lorenz (1965) suggested that habituation is likely to be the phylogenetically
oldest process for modifying an organism’s behavior. The universality of habituation
implies that this process, however it may be exp
lained, is fundamental to the adjustment
Habituation
5

of all organisms in their respective environments and that it has not altered radically
through evolution. As Humphrey (1933) emphasized, the pervasiveness of habituation as
an “elementary conservative phenomenon co
mmon to living systems of many different
grades of complexity, belonging to them
qua
self
-
conserving systems however they may
be organized” (p. 135) justifies an inquiry into the nature of the phenomenon without
giving a precise description of all the proc
esses concerned. Clearly, the capacity to ignore
only those stimuli that are irrelevant and to channel behavior into organized and directed
actions in response to meaningful stimuli is necessary to conserve energy and focus
behavior.

There is as adaptive
an advantage in eliminating existing patterns of
responsiveness that fail to perform a useful function as there is to acquiring new patterns
of responsiveness which result in escaping danger or releasing consumatory acts. For
instance, many young animals
show escape responses to a wide range of stimuli that
could indicate potential dangers, in particular stimuli that are novel, sudden, moving, or
of high intensity (Thorpe, 1963). This overgeneralization ensures that these young
organisms are attentive to m
ost of the threats they encounter. However, sensitivity to
such a wide range of stimuli could easily overwhelm the organism’s senses and interfere
with other critical tasks. Hence, the necessity for a process by which responsiveness to
innocuous stimuli be
comes temporarily or permanently eliminated. Habituation performs
that function.

Habituation
6

Sensory Adaptation and Effector Fatigue

A few decades after Humphrey’s initial exposition of habituation, Thorpe (1963)
defined habituation as “the relatively permanent waning

of a response as a result of
repeated stimulation which is not followed by any kind of reinforcement” (p. 61), further
specifying that it is specific to a particular stimulus and relatively enduring so as to
differentiate it from other response
-
fading pro
cesses such as fatigue, sensory adaptation,
or trauma.

Until the 20
th

century, the scientific consensus held that reflexes were invariable,
a view generally known as the “invariance doctrine,” and habituation was thus perceived
as a manifestation of patho
logy (Christoffersen, 1997). At the wake of World War I,
aviators exhibiting habituation of the post
-
rotational nystagmus reflex were deemed
defective and were hence denied entry into the Air Force. It is likely that this notion
emanated from the behaviora
l similarities between habituation, sensory adaptation, and
motor fatigue. Although the distinction is at the present time clear, the response
decrement that is evidenced in all three generated fuzzy conceptual boundaries between
them.


Distinguishing hab
ituation from adaptation and fatigue forces one to admit that
behavioral changes due to an inability to detect a stimulus at the sensory level or to
respond to it at the motoric level cannot describe all instances of response decrement.
Behavioral and phys
iological evidence has confirmed that habituation is a learning
process that cannot be explained by these simpler potential causes of cessation in
response. Adaptation is unlikely to be a factor of waning if a same stimulus elicits a
Habituation
7

different response aft
er having initially faded. For example, Prechtl (1958) found that
stimulation to the reflexogenous area around the mouth of a

hungry human newborn

produced a rooting reflex towards the stimulated point. The response fades after repeated
stimulation but is
sometimes replaced by another response mediated by the same sensory
region and presumably by the same receptors. Another source of evidence that decreased
response cannot be due to adaptation comes from studies whereby a stimulus to which the
organism no l
onger responds again elicits a response when presented in a different
context. Engen and Lipsitt (1965) elicited responses from newborns to one odor when
their response to a mixture of that odor coupled with another one no longer elicited a
response. The i
nitial waning thus cannot be ascribed to sensory adaptation.

Correspondingly, motor fatigue is ruled out if the same muscles can be used for a
different response or if a different stimulus triggers the initial response. For instance,
Franzisket (1963) obt
ained a decrement in frogs’ leg wiping movements to stimulation of
the skin on their backs by giving a series of 100 trials. However, the same reduction was
not found if the stimulation used was pinching of the hindlimb, although both responses
relied on t
he activation of the same group of muscles. The paradigm of choice in studies
of perception and cognition in human infants relies on the second exclusionary criterion
for effector fatigue, whereby presentation of a novel stimulus after habituation to a
fam
iliar one usually yields greater attention. Fatigue is also excluded when a more
intense stimulation restores the response to the original stimulus, as is the case in the eye
blink reflex in humans since a fatigue that is diminished by a stronger stimulati
on would
be oxymoronic.

Habituation
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Characteristics of Habituation

Several characteristics of habituation have been found in a variety of species,
vertebrate and invertebrate alike. Highlighting such properties is needed to direct and
guide the search for underlying m
echanisms. Thompson and Spencer (1966) delineated a
detailed operational definition of habituation that includes the nine following parameters.

1.

The time course of habituation.
Given repeated applications of a stimulus that
initially elicits a particular re
sponse, further presentations of the stimulus result in a
response decrement depicted by a negative exponential function of the number of
stimulus presentation (Figure 1A). This is the primary operational definition of
habituation. In this sense, it has be
en widely documented in research with various
organisms. For example, Wolda (1961) demonstrated habituation of the water boatman
to pin pricks of the water. These insects lie inverted beneath the surface of the water
waiting for prey. Number of responses
decreased in eight successive sets of 25 trials.

2.

Spontaneous Recovery.

If the stimulus is withdrawn, the response reappears
over time (Figure 1B). Hinde’s (1960) study on the response of wild
-
caught chaffinches
to live owls and owl models demonstrated tha
t the time of response recovery after
habituation is relatively rapid. In a comparison of the first trial response of the initial
habituation series with the first trial response of the recovery series, Hinde reported that
the rate of recovery reached near
ly 50% after 30 min, and grew subsequently for 24
hours; no subsequent measures were taken.

3.

Relearning Effects.
If repeated series of habituation and spontaneous recovery
are offered, habituation occurs more rapidly each time (Figure 1C). This was exempli
fied
in the decline in responsiveness to foot shock found over days in thigh electromyogram
Habituation
9

of spinal frogs (Farel, 1971). When sessions of presentation were repeated daily, response
amplitudes decreased progressively more rapidly from one day to the next.

4.

The Effects of Stimulus Frequency.
The greater the presentation of the stimulus,
the faster or the more pronounced becomes habituation (Figure 1D). In a study of
habituation in the nematode
Caernorhabditis elegans,

Rankin and Broster (1992) found
that its

tap withdrawal responses were sensitive to the frequency of stimulation. If taps
were presented at a short interstimulus interval (ISI) of 10 seconds or less, the tap
response waned at a faster rate and more completely than if the taps were given at a
lon
ger ISI of 60 seconds. Additionally, they demonstrated that spontaneous recovery
occurred faster for worms trained at short ISIs, while those trained at longer ISIs showed
a relatively protracted recovery.

5.

The Effects of Stimulus Intensity.
The weaker th
e stimulation, the faster or the
more pronounced is habituation (Figure 1E). With a very strong stimulus there may be no
response decrement but rather an initial response increment. In a study of contraction to
mechanical shock in the flatworm
Stenostomum,

Applewhite and Morowitz (1966)
reported that more intense stimuli took longer to habituate to and were slower to recover
from. In particular, recovery was concluded in 4
-
8 minutes with a weak stimulus and
remained incomplete after 8 minutes with the more
intense ones. However, Sokolov
(1963) posited that the relationship between stimulus intensity and the orienting response
(also called the orienting reflex, or OR) is not linear. Interestingly, he found that near
-
threshold stimuli elicit relatively large r
esponses.

6.

Asymptotic Response Levels.
The effects of habituation training may persist
beyond the zero or asymptotic response level. Even after a response has disappeared or
Habituation
10

remained at a stable level, the organism will recover more slowly if it is exposed
to
additional habituation series beyond that point (Figure 1F). Consequently, there should be
less spontaneous recovery with increased number of habituation trials. In an attempt to
dissect the dynamics of the neural systems involved in habituation,
Teyler
, Chiaia,
DiScenna, and Roemer

(1984) studied the distribution of central nervous system
habituation
-
sensitization at the cellular level. Tests using the rat allocortex (hippocampal
slices) indeed showed that the magnitude of recovery taken 30 seconds afte
r 10 1
-
per
-
second stimuli was at 97% of the control levels whereas equivalent measures taken after
40 1
-
per
-
second stimuli dropped to 67%.

7
.

Stimulus Generalization.
Habituation of a response to a particular stimulus is
accompanied by stimulus generaliza
tion to other stimuli (Figure 1G). Hence, habituation
is often used to determine which stimuli organisms find similar. For instance, Johnson
and Aslin (1995) found that after habituating 2
-
month
-
old infants to a black rod moving
behind a white stationary b
ox, the infants generalized habituation to a solid rod but not to
a discontinuous rod. This finding suggests that these young infants treated the familiar
stimulus as a continuous rod moving behind the box although the middle section of the
rod remained in
visible.

8.

Dishabituation.

Presentation of a novel stimulus results in recovery of the
initial response (Figure 1H). In the previous example, the increased looking time obtained
by presenting the discontinuous rod is an instance of dishabituation. More trad
itional
studies using dishabituation aim to elicit a response again after its initial waning has
occurred by presenting the habituatory stimulus in the presence of an irrelevant stimulus.
In an experiment conducted by Groves and Thompson (1970), rats were
exposed to a
Habituation
11

series of 14 tones to which the rats’ startle response habituated. Then a flashing light was
presented to the experimental group before the 15
th

tone whereas the control group
received no light. The first group exhibited a sudden return of sta
rtle response, although
short lived, above the initial response level while the latter group continued on a
habituating trajectory. Initially, this type of finding was used to infer that it is a process of
inhibition that causes the response decrement whic
h is then disinhibited by the novel
stimulus. Yet, it became clear that dishabituation is not a disruption of habituation but
rather a superimposed process of response sensitization which overrides the processes
underlying the waning (Groves & Thompson, 19
70; Thompson & Spencer, 1966). This
notion formed the basis for the dual
-
process theory which will be discussed later.

9.

Habituation of Dishabituation.
Repetition of the dishabituatory stimulus results
in a waning of dishabituation, that is habituation of di
shabituation. For example, Lehner
(1941) reported that various responses, including the tail reflex in spinal rats to repeated
tapping, the respiratory startle in response to auditory stimulation in intact rats, and the
umbilical abdominal reflex in humans
, were revived with presentation of an extraneous
stimulus once habituated through repetition. These dishabituatory effects themselves
waned progressively showing less and less recovery with each habituation series.

Habituation
12

Figure 1



















A.
The time course of habituation

Number of Stimulations


Response amplitude

Time

Resp
onse amplitude


B.
Spontaneous recovery


100


50


0



Habituation

Spontaneous Recovery


0


50


100

Time

Response amplitude


C.
Relearning effects

1
st

series

2
nd

series

1

per 3.2 sec

1

per sec

Time


0


50



100

Response amplitude


D.
The effects of stimulus frequency

Habituation
13


















E.
The effects of stimulus intensity


7 V

25 V

45 V

Response amplitude


0


50


100

Time


100


50


0

Response amplitude

Habituation
to zero

Habituation
below zero

F.
Asymptotic response levels

Time


G.
Stimulus

generalization


Time

Response amplitude


0


50


100

Time


Response amplitude


0


100


50

Novel
stimulus

Familiar
stimulus

H.
Dishabituation

Test stimulus

(1/min)

Ha
bituating stimulus

(1/sec)

Habituation
14






Note.

Adapted from “A Model Phenomenon for the study of Neuronal Substrates of
Behavior,” by R. F. Thompson and W. A. Spencer, 1966,
Psychological Review, 12,
p. 24
-
26. Copyright 1966 by the American Ps
ychological Association.



Orienting Reflex

Although Humphrey (1933) has been credited with the discovery of the
habituation phenomenon, we should equally credit Pavlov. In the course of his analysis of
conditioned reflexes, Pavlov (1927/2003) discovered
the “investigatory” or the “what
-
is
-
it?” reflex. He noted that this OR occurs whenever something novel is detected by an
organism, upon which the individual interrupts its activity and makes a “full
investigation” of the event. This sequence is best descri
bed in the following quotation:

In a normal animal the slightest alteration in the environment

even the very
slightest sound or the faintest odour, or the smallest change in the intensity of
illumination

immediately evokes the reflex which I referred to …

as the
investigatory reflex

‘What is it?’

manifested by a very definite motor reaction.

Duration of dishabituation


0


50


100


10


20


0


I.
Habituation of dishabituation


1st

2nd


3rd


1st


2nd


3rd


% od increase in response

Successive dishabituations

Habituation
15

However, if these neutral stimuli keep recurring, they spontaneously and rapidly
weaken in their effect upon the hemispheres, thus bringing about bit by bit the
remova
l of this obstacle to the establishment of a conditioned reflex. (p. 29)

An illustrative anecdote is mentioned by Ohman (1983) whereby Pavlov’s
students encountered considerable frustration after going to great lengths to train a dog to
exhibit a consisten
t conditioned response (CR), instead finding that the animal would
inevitably display an OR to their mentor rather than the previously established CR.
Furthermore, the OR is not only an obstacle to be removed by controlling the
experimental environment as

accurately as possible in order to avoid unintentional ORs,
it is also a needed behavior in that the novel stimulus cannot become a conditioned
stimulus (CS) until an OR is elicited. Hence, habituation of the OR is a necessary
prerequisite of classical co
nditioning.

Neuronal Model Theory

Some years later, Sokolov (1963), another prominent Russian researcher,
developed a stimulus comparison theory of habituation based primarily on data from the
human orienting response. In his investigation of the effects
of recurring presentations of
a novel meaningless event, Sokolov noted that the OR is manifested in both physiological
and behavioral changes through somatic (movements of the body, head, eyes, ears, etc.),
autonomic (cardiovascular and respiratory changes
, cutaneogalvanic reaction), and
electroencephalographic (depression or exaltation of
α
-
rhythm, changes in cortical
reactivity) outputs.
This influential theory depicts habituation as a perceptual process in
which the repeated presentation of an event results in the development of a neuronal
Habituation
16

model. With repetition, the sensory input is comp
ared with the “engram” of the expected
stimulation. This neuronal model retains all aspects of the stimulus, including duration,
interstimulus interval, and the relationship between several stimuli across time. A
mismatch between the model and the stimulus

activates the OR and produces longer
looking while the system processes discrepancies between the two. If there is a match, the
model inhibits the OR and habituation occurs. Consequently, looking is regarded as
encoding and habituation is considered to b
e the result of a more complete neuronal
model from repeated presentations. The strength of the OR is directly proportional to the
degree of discrepancy between the input and the neural model.

The neuronal model is said to reflect the interaction of two
systems. Stimulation is
transmitted via specific pathways (1) to a comparator system in the cortex and via non
-
specific pathways (2) to an amplifying system in the reticular formation. A novel
stimulus creates a mismatch with the neuronal model and discrep
ancy signals are sent
from the comparator to the amplifying system (5). This then elicits the autonomic and
somatic components of the OR via efferent pathways (7). Responses resulting from a
match leave the modeling system via the specific pathways (6). Fu
rthermore, output from
the comparator system stimulates the amplifying system (5). Simultaneously, this system
activates the comparator system via an activating pathway to prompt it to develop or fine
-
tune the current neuronal model (4). Stimulus repetitio
ns lead to the formation of a more
complete neuronal model in the cortex, producing a negative feedback via the
inhibitatory pathway that blocks impulses to the amplifying system and inhibits the OR
(3). This relationship is represented schematically in Fi
gure 2.

Habituation
17

Figure 2
.
Sokolov’s (1960) scheme for the OR elicitation and habituation








Note.

Adapted from “Neuronal Models and the Orienting Reflex” by E. N. Sokolov,
1960, in M. A. Brazier (Ed.),
The central nervous system and behav
ior,
p. 187
-
276.
Copyright 1966 by the Macy Foundation.


The most compelling evidence for this model comes from studies in which a
sound of a particular duration is presented until the organism habituates. Then, when a
sound of a shorter duration is prese
nted the OR reappears at its termination. If, on the
other hand, a sound of a longer duration is presented, the OR reappears at the end of the
duration of the previous stimulus (Sokolov, 1960).


Dual
-
Process Theory

Another theoretical approach was proposed

by Thompson and Spencer (1966)
predominantly on the basis of neurophysiological research on the hindlimb flexion reflex
of acute spinal cats. They presented evidence that behavioral responses elicited by
repeated stimulation reflect the net outcome of two

independent, superimposed processes:
habituation and sensitization. Sensitization refers to an increase in response magnitude as

Comparator

System


Amplifying

System

1

2

3

4

5

6

7

Habituation
18

a result of a stimulus that increases arousal. These two processes are assumed to occur in
two different parts of the nervous

system with the habituation process occurring in the
“S
-
R system” and the sensitization process in a “state system.” The first evokes a
response by activation of a stimulus response reflex arc from the organism’s perceptual
encoding of the stimulus to the

muscle systems. The second is the arousing system that
determines the organism’s general level of responsiveness, or readiness to respond. The
change in behavior is determined by whichever process is stronger. As will be discussed
later, a common finding
in habituation research is an initial response increase before
declining, implying an initial greater effect of sensitization over habituation, with further
presentations producing more habituation than sensitization. This theory can account for
many of th
e behavioral phenomena of habituation and sensitization.

A study of the rat startle reflex done by Davis (1974) has offered momentous
support for the Dual
-
Process theory. He presented evidence that repeated presentation of
a tone leads to either a decreas
e or an increase in response depending on the level of
background noise: startle responses to a 110
-
db tone habituate when background noise
level is at 60
-
db, whereas responses rise with a background noise level of 80
-
db. These
results lend themselves to b
e interpreted in light of the competing processes that are
habituation and sensitization. Low sensitization levels arise from the exposure to the low
background noise resulting in the net gain of habituation, whereas sensitization prevails
over habituation

and is maximized by the low background noise.

Habituation
19

Developmental Aspects


Before Sokolov introduced his model of habituation of the orienting reflex,
research on habituation with infants was sparse. His postulation of the location of the
comparator system in
the cortex created a major interest in habituation by developmental
psychologists and others. The main focus of this developmental interest was not
habituation per se: habituation became a subject of study as a means to assess infants’
perceptual capaciti
es, their ability to discriminate between stimuli.

Types of procedure

Just as in animal studies, the habituation paradigms in studies of infancy
traditionally involve the repeated presentation of a visual, an auditory, an olfactory, or a
tactile stimulus
over an extended period. In visual studies, this habituation phase ends
when the participant has either accumulated a predetermined amount of time looking at
the display (fixed
-
trials), or decreased looking time below a certain criterion usually
defined as

three consecutive trials totaling 50% or less of the time spent looking at the
first three trials (infant

controlled trials). The habituation phase is then followed by one
or two test trials during which the familiar stimulus and a novel one are displayed

simultaneously (visual preference comparison task) or by a new stimulus in isolation
(habituation
-
dishabituation task). With any combination of these subtypes of habituation
and test trials, the novel stimulus is expected to elicit differential interest (
more
or

less
attention) than the familiar one.

Habituation
20

Horowitz, Paden, Bhana and Self (1972) aimed to replicate a previous study done
with 3
-

to 14
-
week
-
old infants by changing the procedure from fixed
-
trials to infant
-
control. The compelling criticisms of the f
ixed
-
trials procedure they set forth established
the infant
-
controlled procedure as the favored paradigm by most researchers. The use of a
standard 30
-
second presentation in fixed
-
trials procedures is problematic in that the
inspection time the infant devo
tes to a stimulus can be artificially truncated if the infant
diverts her gaze from the stimulus between its onset and offset or if she hasn’t finished
inspecting it upon offset. Horowitz et al. reported remarkable advantages in infant
cooperation as seen
in reduction of infant fussiness and increase in session completion.
Allowing infants to control stimulus presentation also resulted in longer looking duration
than most researchers had foreseen, with the longest single look lasting 1,073 seconds
and looki
ng times over 2 minutes being very common. The operating assumption is that
this procedure accommodates individual differences in processing time, allowing infants
to pace themselves. In a more recent study conducted by Millar and Weir (1995),
comparison o
f fixed
-
trials and infant
-
controlled procedures with 6
-

to 13
-
month
-
old at
-
risk infants,yielded responses to novelty for the latter paradigm

solely
.

Yet, in studying
the response of 10
-
week
-
old infants to facelike patterns, Haaf, Smith, and Smitley (1983)
found no evidence of a met
hodological advantage for

infant
-
controlled procedures over
fixed
-
t
rial ones.
In fact
,

a surprising result emerged: babies were more likely to cry and
fuss when trial duration was contingent on their behavior than when it was
pred
etermined. Of the 22 infants who did not complete the test session, one
had been
assigned to the

fixed
-
trial
s

condition

(trials and intervals duration were predetermined)
,
five
to

the offset
-
control condition

(trial termination controlled by the infant)
, a
nd an
Habituation
21

outstanding 16
to
the onset
-
offset
-
control condition

(trial initiation and termination both
controlled by the infant’s behavior)
.

Familiarity Preference

Novelty preference as a result of recovery from habituation is the most popular
paradigm for stud
ying perception in infants, especially newborns. This is so despite the
difficulty of demonstrating that newborns will habituate to a stimulus. This is likely
attributable to the parsimonious explanation the Neural Model theory provides of the
reason infan
ts prefer novelty
. Most researchers construe habituation in information
processing terms involving processes that reflect a mental representation of the stimulus
and an ongoing comparison of new presentations to that representation. O
nce the infant
forms a
n internal representation that closely resembles that of the external stimulus,
inhibitory processes prevent further orientation to it and the novel stimulus becomes more
interesting.

Fantz (1964) was one of the first to use the phenomenon of habituation
as a
tool to investigate the perceptual world of
the young infant
. He serially presented 10 pairs
of visual stimuli to infants from 1 to 6 months of age. One member of each pair remained
constant and the other member varied across all trials. Each trial co
nsisted of the
presentation of magazine advertisements and photographs for a duration of 1 min. Fantz
found that only infants
over 2 months of age

showed decreased looking to the familiar
stimulus, whereas infants in the 1
-

to 2
-

month age range showed no
preference for either
the familiarity or
novelty.

Although, Fantz did not obtain preferences
in

1
-

to 2
-

month
-
old babies,
his

data supported the
view

that novel stimuli attract

more and more attention

with increased age
.


Habituation
22

The pattern of responding in infa
nt studies is not theoretically simple. In
newborns, it is not usual to see simple declines in attention.
Indeed
, the first consequence
of repeated presentation of the same stimulus in
newborns

is an increase in looking over
trials. Various studies of rela
tively short duration have borne out that newborns prefer a
familiar stimulus over a novel one. Using a non
-
nutritive sucking paradigm, DeCasper
and Fifer (1980) found that newborns preferred their mother’s voice over that of another
woman when they read a

passage of a child story.
DeCasper and Spence

(1986)
confirmed a preference for the familiar in assessing the effects of prenatal maternal
speech on newborn preference. In this instance, newborns preferred the prose passage
they had been exposed to in
-
ute
ro over a novel one. In another study of neonatal
preference for maternal features, Walton, Bower and Bower (1992) obtained evidence of
preference for mother’s face over that of a stranger, using images presented on a
computer screen. In crossmodal matchin
g studies, newborns have also been found to
prefer to look at a visual display of a pacifier they have already explored orally rather
than a display of one they have not explored (Kaye & Bower, 1994; Meltzoff & Borton,
1979)

and
to increase their explorato
ry activity for a familiar object held in the right hand
when simultaneously presented with a novel object in the left hand (Molina & Jouen,
2003).
Barrile, Armstrong, and Bower (1999) examined preference for familiar over
novel stimuli over repeated prese
ntations in both visual and auditory modalities using an
operant sucking paradigm. They found a strong primacy effect for faces and consonant
-
vowel syllables but no

evidence of a shift from familiarity preference to novelty
preference across time in this 5

min. experiment. Barrile et al. make the noteworthy point
that novelty preference may certainly be induced under particular conditions but that it
Habituation
23

need not be expected in studies that do not follow a strict habituation protocol.
Drawing
on Piaget’s observ
ations of children, Hunt (1963) proposed a two
-
stage developmental
sequence marked by an initial preference for familiarity and a subsequent preference for
no
velty. Hunt theorized that the u
nderlying cause of the shift from the former preference
to the lat
ter is the development of cognitive representations of familiar patterns at around
6 months. The act of recognition is in itself rewarding to the young infant and familiarity
is sought. As the infant gets older and recognition becomes more repetitive, fami
liar
patterns loose their attractiveness and

an inclination for

novelty ensues. Support for this
model was lent by Weizmann, Cohen, and Pratt (1971) and Wetherford and Cohen
(1973) who observed age related changes in habituation in infants younger than 3 m
onths
of age. In the first study,
after having been familiarized to a stabile between 2
-

to 4
-

weeks of age,
infants tested at 6 weeks looked more at the familiar than at the novel
display, wher
eas infants tested at 8 weeks
show
ed

n
o preference one way or
another
. In
the second study, 10
-

to 12 week
-
olds, habituate
d

to colored geometric shapes

and to
prefer novel patterns

that were interspersed at 3 intervals during the familiarization series.
Younger infants, 6
-

to 8
-

weeks, did not habituate, maintaining
a preference for familiar
patterns.

Novelty Preference

Other lines of evidence suggest that novelty preferences following familiarization

can be observed soon after birth.
Several researchers have reported neonatal preferences
for simple and complex shape
s contingent upon successful habituation to the familiar
stimulus (Friedman, Carpenter, & Nagy, 1970; Slater, Morison, & Rose, 1983
b,

1
984).

In
an attempt to
specify the locus

of habituation in the newborn
, Slater, Morison, and Rose
Habituation
24

(1983a)

investigated re
sponses to monocular presentations of color and shape


They
observed

that
,

after looking at familiarization trials through one eye only, infants
recovered looking at a novel stimulus
through the other eye
during test trials, discrediting
Bronson’s (1974)
v
iew that newborn habituation was a result of retinal adaptation.
In the
tactual domain,
in contrast to the familiarity preference
Molina and Jouen (2003)
found
following habituation
,
evidence for novelty preference is also available.

In a series of
studies


with neonates

and 5
-
month
-
olds
, Streri et al. (
1986
, 2000,
2005
)
offered

that
infants can habituate to shape by exploring objects manually and detect differences in the
contour of two small object
s

as evidenced by increased holding times for novel over
f
amiliar
stimuli
. I
nvestigators have also examined the ability of newborns to abstract
numerosity. Over counter
-
balanced presentations of 2
vs.

3 dots and 4
vs.

6 dots,
newborns showed novelty preferences in the small number set
(Antell & Keating,
1983)
.

In

a series of studies of newborns’ level of visual processing and categorization,
researchers have obtained novelty preferences using both fixed
-
trials and infant
-
controlled procedures (Macchi Cassia, Simion, Milani, & Ulmita, 2002; Quinn,
Slater,
Brown, Ha
yes, 2001
; Slater & Morison, 1987; Slater, Morison, & Rose, 1983; Turati,
Simion, & Zanon, 2003).

This is an apparent contradictory pattern of results. Many studies look for a
marker of habituation that is idiosyncratic (e.g., three successive looking tim
es from the
fourth trial totaling less than 50% of the first three, two consecutive trials with looking
duration of 3 seconds or less, etc.). Dannemiller’s (1984) analysis of the statistical
soundness of the 50% decrement habituation criterion casts doubt
on the validity of these
arbitrary cut
-
off points. The evidence from his study seems “to preclude the use of trials
Habituation
25

to criterion as an index rate of habituation” (p. 147). This procedure possibly ignores
some important information: it has been proposed, a
nd seems at times ignored, that
habituation is a process of perceptual learning that initially requires increased looking in
younger organisms (e.g. Cashon & Cohen, 2001; Cohen, 2004; Hunter & Ames, 1988;
Roder, Bushnell & Sasseville, 2000; Slater, Morison
, & Rose, 1984).

Hunter and Ames’ Multifactorial Model

Hunter and Ames (1988) have proposed an appealing multifactor model of infant
preferences for novel and familiar stimuli. The inverted
-
U function that results from this
model has three stages, with eac
h phase corresponding to different levels of encoding.
The infant will thus follow an invariable sequence of no preference, followed by a
preference for familiarity, and finally a preference for novelty (see Figure 3).
Additionally, the model posits three
sources of influence: 1) the duration of
familiarization, 2) the age of the infant, and 3) the difficulty of the task. Slater (1995)
found evidence for the first of these factors. In a pilot familiarization study with neonates,
he noticed that “all of the
babies whose accumulated looking time over six trials
exceeded 180 s gave a familiarity preference, and all of the babies whose accumulated
looking time was less than 180 s gave a novelty preference” (p.122). Slater further noted
that newborns will habitua
te over longer periods of time to “any visual stimulus, however
much it is preferred” (p.156). The infant will show a familiarity

preference while
information about the stimulus is gathered. Once the stimulus has been fully encoded, she
will become bored w
ith it, showing a preference for the new stimulus. For newborns
then, stimulus encoding will obviously be longer than for older infants, resulting in an
increase in time taken to habituate. Similarly, the complexity of the stimulus will also
Habituation
26

influence patt
erns of preference. More difficult tasks will require more information
processing and thus engender a slower rate of progression through the sequence of stages.
A study by Cohen, Deloache, and Rissman (1975) supported the relationship between
task difficul
ty and subsequent preferences for familiar and novel stimuli, finding that
infants habituated faster to simple than to complex stimuli.

Figure 3:
Hunter and Ames’ (1988) inverted
-
U function

Familiarization Time
Preference
Familiar
None
Novel

Many investigators have argued that novelty preference indicates

complete
encoding of the familiar stimulus, familiarity preference incomplete encoding, and a null
preference a period during which the attention grasping quality of the two stimuli are
equal (
Colombo, 1993;
Houston
-
Price & Nakai, 2004; Hunter & Ames, 198
8; Sophian,
1980
). It should be noted that theoretically there will be two or three periods of null
preference in a sequence. The sequence of preference includes five distinct phases in all:
a) no familiarity, therefore no preference, b) stimulus 1 becomes

familiar and is preferred,
c) stimulus 2 (the novel one) becomes familiar and a null preference is reestablished, d)
Habituation
27

stimulus 1 is too familiar, a preference for stimulus 2 appears, and e) stimulus 2 becomes
over
-
familiar, a null preference reappears.

In

an effort to integrate the different lines of investigation present in the literature,
Cohen (1972) assessed the relative importance of turning towards a stimulus versus
fixating it. The traditional checkerboard pattern was used to examine the importance
of
stimulus complexity in attracting and maintaining infant attention during habituation by
repeatedly presenting either a 2 X 2, 8 X 8, or 24 X 24
pattern to 4
-
month
-
old infants. His
model offered two separated processes of attention: an attention
-
getting

aspect measured
by latency to turn toward the visual stimulus and an attention
-
holding aspect measured by
the duration of infants’ fixation on the stimulus. Cohen’s results confirm that infants’
preference for complex patterns can be determined by two ind
ependent looking
measures: longer duration and shorter latency of visual fixations.

Richard, Normandeau,
Brun, and Maillet (2004) mirrored these results in the auditory modality.

However, t
he
se

studies, and most of Cohe
n’s corpus of research, are
based on

observations of 3
-

to 5
-
month
-
olds.

This restriction makes this model less tenable than others that have included
a wider
variety
of
age ranges
.

Cohen

has admittedly
avoided the neonatal population

for
logistical reasons
:

I admit I’ve never had the courag
e to run a full
-
blown experiment with human
newborns. For those who may not be aware of the difficulties involved, running
such an experiment can be a formidable task: convincing hospital administrators
and personnel in the neonatal nursery the research is

worth while; setting up
elaborate equipment often in cramped, temporary quarters; obtaining permission
from mothers who are still recovering from their deliveries; waiting, sometimes
Habituation
28

for hours, until the infant to be tested is in a quiet, alert state; cop
ing with the
infant’s inevitable changes in state after testing has begun; and interpreting the
infant’s responses that at one moment may seem to be nothing more than a blank
stare and at another moment active involvement with the stimulus” (Cohen, 1991,
p
. 1)
.

Alternative interpretations of the dynamics of infants’ r
esponses to checkerboard
patterns

favor the Dual
-
Process theory

(Bashinski, Werner, & Rudy, 1985;
Kaplan,
Goldstein, Huckeby, & Cooper, 1995;
Kaplan & Werner, 1986, 1987; Kaplan, Werner, &
Rudy
, 1990)
.
These experiments involved sensitization

by way of stimulus complexity or
infant directed speech,
produced increments in responsiveness to early trials
, which
decay
ed

spontaneously thereafter.

A More Complex Case: Categorization


In two studies in
vestigating infant categorization, Slater and Morison (1987) and
Quinn, Slater, Brown and Hayes (2001) presented newborns sequentially with several
exemplars of a given shape in a fixed
-
trial familiarization procedure. When this was
followed by visual pref
erence test trials, newborns did not show a significant difference
in looking time for either the novel or the familiar stimulus. Thus habituation does not
reveal any evidence of form categorization in newborns.

Mata
-
Otero and Bower (2004) replicated Slat
er et al.’s study of categorization
using an operant sucking paradigm. The operant sucking paradigm facilitates the study of
newborn perceptual abilities by permitting a precise and simple way of obtaining
habituation
-
like data (e.g. Aldridge, Stillman, &
Bower, 2001). As in the habituation
paradigm, the infant becomes familiar with the repeated presentation of a stimulus.
Habituation
29

Differential attention to the novel stimulus demonstrates discrimination and visual
recognition memory. However, whereas habituation ref
ers to the passive decrease in
responsiveness that occurs when a stimulus becomes familiar, the operant sucking
procedure relies on the active self
-
presentation of the stimuli contingent on sucking
behavior.
This procedure is a great improvement over older

ones, since the newborn has
complete control over what stimulus is presented and for how long.

The emergence of evidence for specific categorization abilities in infants seems to
depend on the demands of the tasks that are presented to them (Mareschal & Q
uinn,
2001; Oakes, Plumert, Lansink, & Merryman, 1996). It could thus be argued that
newborns’ failure to show categorization reflects inadequacies of the habituation
procedures used in Quinn et al. (2001) and Slater and Morison (1987) rather than the
abse
nce of such abilities per se. For instance, research has revealed that young infants
may have difficulties looking away from highly salient stimuli once their attention has
been focused (
Frick, Colombo, & Saxon, 1999;
Friedman, 1972; Hood, 1995;
Johnson,
P
osner, & Rothbart, 1991;
Stechler & Latz, 1966). Similarly, Haith (1980) has noted that
“very young infants tend to look at only one stimulus in a paired
-
stimulus array, whereas
older infants look at both” (p. 123). These behavioral tendencies could have c
ontributed
to the lack of findings in the aforementioned studies. This distinction may be the reason
we
did find evidence of form categorization by newborns in the operant study
.


Additionally, Mata
-
Otero and Bower’s

claim depends on a between
-
subject
anal
ysis, focusing on novelty preference rather than on a decrement in response as is
found in habituation. There was no within
-
subject evidence of habituation but the
between
-
subject novelty effect was significant. Other well
-
known studies have relied on a
Habituation
30

si
milar statistical analysis (e.g., Eimas et al., 1971). Moreover, categorization does not
necessarily imply habituation. Whereas, the “sameness” between stimuli is perfect in
traditional discrimination studies that use literally the same familiar stimulus,
in
categorization studies stimuli elements change with each presentation although the
stimulus is conceptually the “same.” In the latter, the differences between the familiar
stimuli could be large enough to sustain the interest of the infant, resulting in

a failure to
show a decline in attending although the invariant properties across stimuli are detected.
Then, once a distinctly novel stimulus is presented (i.e., one that does not share the
previously perceived invariant), attention increases significant
ly, indicating an
intensification of processing effort.

To untangle the discrepancy in results found in the aforementioned research,
Mata
-
Otero and Bower (2006) conducted a study of pure habituation. Newborns were
repeatedly presented with a simple geomet
ric shape (a cross, a circle, a square, or a
triangle) for a 25
-
second period with a 3
-
second interstimulus interval. Newborn
-
looking
during the stimulus presentation periods was measured over the duration of the study.
There was no evidence at all of habi
tuation over the 14.53 minutes of the study. Yet,
Slater, Morison, and Rose (1983) found that infants with an average age of 3 days readily
habituated to each of the four stimuli. Do infants develop so rapidly? Or is there some
sinister factor, such a cri
terion that is responsible? Or is the state of the baby a factor?
Prechtl (1967) argued that most seeming newborn habituation is an artifact of trials to
criterion procedures interacting with spontaneous fluctuation in the state of the baby.


Numerous stud
ies have
upheld

the proposition that infant response is affected by level of
Habituation
31

arousal

(
e.g.
Campos & Brackbill, 1973;

Lester, Als, & Brazelton
, 1982; van den Boom
& Gravenhorst, 1995).

Thus far we have not addressed the knotty question of the nature of the
stimulus
presented. Despite Cohen’s claim above there must be some doubt over whether one can
observe or measure habituation to mother’s face in infants, whether newborn or older.
Walton, Armstrong, and Bower (1998) and Pascalis, de Schonen, Morton, Deruel
le, and
Fabre
-
Grenet (1998) have commented on this. In a very real sense one would not expect
habituation to occur to mother’s face. The baby obviously does have to learn to identify
her face. Habituation is a phenomenon that occurs with reflexive, unlearn
ed behaviors.
Learned behaviors would not habituate. In fact, as
noted earlier
, habituation must occur
before one simple form of learning, classical conditioning, can occur.

Why would we expect the currently voguish stimuli, geometric forms, to elicit
any
kind of unlearned behavior? These are completely artificial stimuli. Hebb (1949)
spent many pages speculating how an organism might learn to identify a triangle. Is there
any reason now to dissent from this view? Is there any reason to believe that triangl
es are
at all like faces?
Through evolution, selection forces have promoted organisms who
attend to elements of the environment that have adaptive value.
There is every reason to
believe that evolution would have selected for sensitivity to human faces

(Sl
ater &
Quinn, 2001)
. Has evolution even had time to select for sensitivity to geometric forms
?

Conclusions and Future Directions

The major question that we must address is

how to reconcile the incompatible
conclusions that the different indicators suggest.

In the most recent studies, newborns
Habituation
32

were only hours old and it may be that they are unlikely to be bored by anything they are
shown. Habituation is, after all, a manifestation of boredom. The literature on habituation
to geometric forms in young infants
is, sadly, a contradictory mess. Consider the pair of
habituation studies described above, the Slater et al
.

study and the Mata
-
Otero study. It is
possible that the main difference, causing the different results, is the age of the babies, <
1day VS > 3d
ays. It is possible that something has happened in three days. One thing
might be a sudden neural maturation that allows habituation to occur. That is certainly
possible but
hardly
testable. It is also possible that learning of a Hebbian sort, learning to
encode straight lines, has occurred
.
In any case, is seems
unequivocal

that a
new theory
of perceptual learning to use in studies of habituation to geometric forms

is needed
. It
would appear that the existing theories assume an almost photographic process
.
M
ore

complex and more adequate
, neurally constrained computational models

probably do an
adequate job of accounting for visual behavior in

habituation (e.g. Sirois & Mareschal,
2002, 2004)
.
It would be possible to test these as models for perceptual lear
ning of

various

geometric forms.


It should be clear from this short review that there is anything but consensus in
studies of habituation in early infancy.

I am forced to ask why should we study
development of perception of geometric forms in this way. Ca
tegorization is interesting
but does not require habituation for a demonstration. There are gestalt aspects of
perception that are interesting. Do they require habituation studies?
Several researchers

despair of traditional habituation paradigms
, opting fo
r

regression models

to fit
habituation curves to individual infants’ re
s
ponses

instead of arbitrary window approach
criteria (Ashmead & Davis, 1996;
;
Lavoie & Desrochers, 2002;

Thomas & Gilmore,
Habituation
33

2004).

Others have called attention to the biasing nature of

subject attrition in habituation
experiments

(Bell & Slater, 2002; Lewis & Johnson, 1971; Richardson & McCluskey,
1983). Rates commonly run

above 50%

of the initially recruited cohort

raising the
question of the generalizability of the results.


Another i
ssue is that habituation does not
elucidate the nativism
-
empiricism debate. It is very hard to draw any conclusions on data
from
3
-

to 5
-

month
-
old infants. Any infant
older
than

a few h
ours
,

for that matter
,

has
already
encountered

in
nume
rable
patterns an
d objects, and
engaged in

extensive learning.
Haith (1998) cautioned that:

Habituation sequences create complications because one doesn’t know whether
infants compare the test experience with what happened during familiarization, or
with their life experie
nce, or a mix of the two, or whether experience is irrelevant.
An infant comes to the lab
with
a lot of history, and it is unclear how th
a
t history
interacts with the familiarization experience (p.171).

Lastly,

w
e can look at form preference without habitu
ation.
We could use
different methodologies to get a
t

shape perception that would circumvent the problems
posed by habituation. A

classical conditioning paradigm
is a likely candidate
. I myself
am now reluctant to inflict another habituation study on a wor
ld that is, I am sure, as
weary of the topic as I am.

Habituation
34

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