CHAPTER

Neuroplasticity and
2 the Environment:
Inplications for Sensory Integration
S. Esse JACORs, Pu.D., OTR
MARY L. ScHNEIDER, PH.D., OTR

ore than 25 years ago, Dr. A. Jean Ayres published her seminal papers (1964,
M L1965, 1966, 1969, 1972a), providing a unique contribution to the under
standing of childhood developmental disorders. In her overview of the sensory
integration model, Ayres (1972b) stated that the theoretical franework from
which she developed her treatment procedures included basic science experiments
as well as human and animal behavioral research. Treatment was key in this
model, and Ayres felt strongly that, based on the research existing at that time and
her strong sense of responsibility to provide treatment to the child during a criti-
cal time of development, she should not wait for certainty about treatment proce
dures (Scardina, 1986). Ayres estalblished a treatment approach that sought to
modity the underlying neurological dysfunction rather than simply treat the symp-
toms. She was well aware that with advances in the knowledgc base in the behav-
1oral and neural sciences, sensory integration theory and treatiment procedures
would continue to evolve.
for treatment rests
One of the basic principles upon which Ayres theoretical model
of neural function. She stated that "it is upon this capacity
to
pertains to plasticity
alter the central nervous system of cach child's brain that the success of the sensory
to remediation of learning disabilities
rests" (Ayres, 1972b,
integrative approach
p.16). She based this premise onshowing that the brain could reorganize after
studies
that this reorganizational ability of the
certain portions were lesioned. She recognized
and a likely mechanism by which
developing brain was a normally occurring process
on tasks of learning and perception.
therapy might intluence pertormance
research on plasticity in brain development and
func-
This chapter examines the basic
il. order to bridge the gap from
tion that has implications for sensory integration,
to sensory integration theory and practice.
basic science research on neural plasticity
several of their own studies that suggest biological-
The authors also describe from
in fetal life, reviewing relevant findings
environmental interactions begin early
chronic psycholugical stress and alcohol exposure
two perturbation studies to date,
during pregnancy.

The Organism-Environment Interaction

she gained a deep respect for the

exploration of thhe scientific literature,
From Ayres' i n t e r a c t i o n and its role in
brain development
organism-cnvironment
importance of the as a demonstration
cited Harlow's work on deprivation
and function (1972b). Ayres
environment on the organisin.
of the effects of the

29
 Harlow's work providel foundational
evidencc regarding deprivation. In rhesus
keys separated from their mothers at birth, mon-
vestibular, auditory, and visual stimulation deprivation of tactile, olfactory, thermal,
profound deficits in social behavior (Harlow, usually provided by the mother produced
1971). Subsequent studies demonstrated that 1958; Harlow, Harlow, & Suomi,
exert a carly postnatal rearing cnvironments
significant influence on brain and
belhavior. For example, a series of studiCs
with rodents showed that
environmental influences could actually
change rats
cytoarchitecture. Compared to ats reared in impoverished environments,
the brains
rearecd
in enriched
environments demonstrated an incrcased thickness of the
as a
consequence of increased cell-body sizc, increased numbers of
occipital cortex
greater dendritic branching, and increased dendritic support (glial) cells,
spine density (Diamond,
Rosenzweig, Dennett, Lindner, & Lyon, 1972; Greenough, 1975; for review see
Roscnzveig & Bennett, 1996). Along similar lines, Cooper and Zubek (1958) selec
tively bred rats for their ability to navigate mazes,
dull animals. producing maze-bright and maze
Surprisingly, when animals from either of these groups were reared in
Single cages with little sensory stimulation, all perforned in thc dull range, even the
offspring of maze-bright animals.
More recent studies have focused on the mechanisms
environmental interactions. For example, Meaney and
undcrlying biological-
colleagues examined specific
neural receptor in certain brain areas of handled rodents.
They reported an enduring
increase in the concentration of glucocorticoid receptors in the hippocampus of han-
dled rats compared to their nonhandled
counterparts (for review see Meaney et a.
1994). Recently, others have expanded on Meaney's work to demonstrate that the cat-
alyst for the glucocorticoid receptor up-regulatiOn
is the increase in maternal licking and grooming
Stressor x that handled rat pups receive from their mothers
upon beng returned to the home cage (Liu et al.,
1997). Moreover, an increase in glucocorticoid
Corticotropin receptors is adaptive when the organism experi-
Releasing
Hormone (CRH) ences a stressful situation. Under stressful condi-
tions, glucocorticoid release results in
Glucocoticoid fight-or-flight responses and other stress reactions
Receptors
Hippocampus (see Figure 2.1). The up-regulation of glucocorti-
Adrenocorticotropin coid receptors means that there are more receptors
Hormone available to take up the released glucocorticoids,
(ACTH)
and more rapid uptake of the glucocorticoids
attenuates the organism's stress responses.
Concomitant with the neural changes, tihe handled
Glucocorticoids Stress Reactions
rats showed decreased behavioral reactivity to
Fight or flight environmental stressors. These studies elucidate
Decreased growth
Increased gastric stress the reciprocal nature ot the organism-environment
Immune responses
Metabolic responses interaction and illustrate a recently tormulated
notion that aspects of the environment actually
become incorporated into the biology of the
Figure 2.1. Simplified schematic diagram of organism via altered neural processes. Such neural
the pathway through which a stressor triggers changes then influence the way the organism sub
glucocorticoid release. sequcnly interacts with the environment (Boyce et
A stressor activates release of corticotrophin releasing al., 1998).
hormone (CRH), which causes release of adrenocor
ticotrophic hormone (ACTH). This results in glucocorti-
A review of neurobiological principles of neuro-

oid release and reactions (solid line).

resulting stress plasticity must precede any discussion of environ-
the take up mental influences on development and bchavior.
lucocorticoid receptors in hippocampus
which leads to a damp- Some of the basic sCience reported here served as a
he released glucocorticoids,
of the stress reactions (X; dotted line). bsis upon which Ayres developed her theory of
ning

7 PART 1: THEORETICAL FoUNDATION

 Sensory ntegration. This discussion also draws fronm research that is quite current,
exploring how some of the recently proposed mechanisms of action might influence sen
Sory utegration.

Brain Growth: A Protracted Process

The ability to make an adaptive
response to one's environment is a hallmark ot cen
tral nervous systenm function. To achieve this ability, the brain must go through a com-
plex and dynamic developmental process involving a precise sequence of anatomical,
functional, and organizational changes (Chugani, 1994). Initially, researchers believed
that, except for myelination of subcortical structures, the process ended by 3 years of
age. Researchers now know, however, that major changes in the structure of cortical
connections continue well into childhood (Huttenlocher, 1994) and adulthood (for
review see Buonomano & Merzenich, 1998; Kaas, 1991).
Brain development involves the formation of neurons (neurogenesis) and the estab-
lishment of their connections (synaptogenesis). At birth, the human brain is only
about one-fourth the size of the adult brain. Although the number of neurons orne has
is remarkably constant throughout life, the brain becomes larger because neurons
grow larger, and the number and extent of connections of their processes (axons and
dendrites) increase (Shatz, 1992). For mostspecies, including humnans, brain develop-
ment involves nott only synaptic overgrowth but also synapse elimination or
pruning
which serves to facilitate sensory information processing in the mature brain. The sec
tion on Synaptogenesis and Synapse Elimination, later in this chapter, describes the
key mechanisms of neuroplasticity, which support a basic premise of sensory integra-
tion that input from the environment has the potential to affect brain (and suhsequent
behavioral) functions.

Genes and Environment

Neurobiologists generally agree that genes enable axons to establish the basic wiring
circuits of the brain. However, because of the sheer number of synaptic contacts in the
brain (10" in the adult brain), genetic information by itself cannot specify the total
number of neuronal interconnections that occur (Huttenlocher, 1994; Kandel,
Schwartz, & Jessell, 1991). The circuitry of the nervous system probably arises from
genetically specified instructions that enable detection of the correct pathways and tar-
gets in the brain. However, genes do not specif the patterns of connections among
neurons explicitly. Edelman (1992) stated that connections shift and reassemble as a
result of a dynamic series of events. Influences on the final wiring include the other
cells in the vicinity and whether these cells that share proximity engage in correlated
activity (see the section on Neural Activity later in this chapter).Consequently, the
brain reflects a self-organizing system (Edelman) because the wiring of the brain is not
strictly prespecified and the developmental driving forces, although similar from indi-
vidual to individual, are not identical.

Another important contribution to the final circuitry is the information received from
the environment through the sensory systems during childhood. In this way, the
mature structure and function of the nervous system reflect bidirectional interactions
berween biological and environmental influences (Hann, 1998). nvestigators have yet
to determine the exact way in which these influences vary across development and
what specific biological mechanisms and environmental experiences come into play.
 Synaptogenesis and Synapse Elimination
The overproduction of neuronal
processes and their synaptic contacts in the human
cerebral cortex begins carly in gestation. Most synaptogencsis, however, occurs in tne
postnatal period, with a rapid increase of synaptic development occurring berween
birth and 6 months of age (Huttenlocher, 1979, Huttenlocher & de Courten, 1987).
Axons establish contact with their
target ncurons by branching out and synapsing
with dendrites or other receptive regions on selected target cells. An axon can make
contact with numerous cells, and these cells in turn receive input not only from that
one axon but also from many others (Kalil, 1989). Over time, refincment of these pat-
terns of connections occurs.

all of
Not the numerous contacts formed during early development persist the
ature state. Although growth of connections is the hallmark of infancy, synapse
in

elimination begins at about 1 year of age and, for most brain regions, is complete by
about 10 years (Huttenlocher, 1994). It is inmportant to note that this pruning of con-
nections in childhood might be necessary for efficient cortical processing to emerge.
Pruning might increase synapse efficiency. Furthermore, the fine-tuning of remaining
Synapses that occurs at the molecular level could also increase synaptic efficiency.
Ihese two processes-synapse elimination and fine-tuning-therefore seem related
nor only to brain maturation but also to behavioral competence (Rakic, Bourgeois,
Eckenhoff, Zecevic, & Goldnman-Rakic, 1986).

The Role of Neural Activity in Synapse Connectivity

lo apprc.ate fully the profound influence of childhood sensory experience on
synapse Connectivity, it is necessary to review two neural mechanisms, the Hebb
synapse and long-term potentiation. Elements of these proposed neural processes sup-
port the notion that acrivity or use of a synapse strengthens the connectiviry and also
Suggest that senory input is a primary mode through which this strengthening occurs.

Hebb Synapse
How is it that molecular events contribute to the strengthening or elimination of
synapses? In 1949, Donald O. Hebb proposed that a presynapric cell's repeated or
persistent success in activating a postsynaptic cell strengthens and retains the synapse
contact between the pre- and postsynaptic neurons. That is, neurons that fire togerh-
er, wire together; and the effectiveness of an excitatory synapse Will increase it inpur
activity to this synapse consistently correlates with the activity of the postsynaptic
neuron (Hebb, 1949). Conversely, asynchronous activity berween
pre- and postsy-
naptic neurons selectively el1minates synaptic contacts between those neurons
(Constantine-Paton, Cline, & Debski, 1990). Although some activity-dependent shapp-
ing of connections Occurs prenatally in response to spontaneous neuronal discharges,
activity-dependent modifications result primmarily from sensory expericnce throughout
childhood. This suggests that neuronal activity Is complete brain devel
necesary to
opment and that, within limits, experience itselt can modity and fine-tune the matur-
ing nervous system, giving the brain a certain degree of adaptability (Shatz, 1992).

This experience-dependent adaptability is extremely relevant to the

therapist using a
sensory integrative approach. Ayres referred to the mportance of correlated neural
activity, noting that neurons grow and become nterconnected in relation to the kind
of electrical and chemical impulses that are directed over them (1972b). She further
stated that use of a neural synapse increases the ease by which the fundamental con-
 nehnits mit be belpful
Uderstitndiny; low hehvialrrit ltrr tl fet tnial gilry * t w i1)

oitex d comsetuently i o i f i , te wiy it forte t itp)93.4 gps ihd 1 )

stand challene or seintists. i s i i A WAplbaV 3s5iJttathat
that
ndersteliy sueli ehangs hel latfyfh kit
will y aAiy 11y*A,
cae the icoOtex (eg., perrpfit, lr.rniing, 1mnMTY AUK sai &
hy furnathiny ifu seusy uiput tg
Weinberyer, 1996). Srnsory integrutn nt thrfry, po
n d eliciliug etleil taha/ptu rsfpnnis frt thr yun hild, 11us nafluenee the
Tlebb synalpse (1r nler rllhuhar int'ur tinne tWutt lwad eyiaflir strengthening
turn vibhane the NZanI
u1s/s ynafli itn fivnl y), ttuh h
es

l n
'kening of pr
aton of the bran.

Long-Term Potentiation (1TP)

Evidence tor the poposed lebb synapsr has eineryjpr froni) Muds f kng-tern

potcntiation (LTP') in the part f the bn an that

hippocampus,
a t learning uritnal
196% studits shewed that
n d menory. Investiators first deUribed DTP in th wten

lastiny increases in
controllcd bursts of stimmulation a r G syhaps prKdiu ea) ny,
synaptic ctlicicncy (1liss & Tono, 1970).
inech-
beaUit trvgbit serve as an inportant
Itis relevant at this point to dicu TIV
addressing
ry integrati treat9pnot. Although
t
l s m underlyim,
cllcctie
nodih-
lcarning; and meiory per C, C n t y Mtegatir
sovog}t le inuducing sy1aptic
c a t i o n - o r syuaptIC plasticilyA fi(rted foictiual
cnAguCnce of 1.]P

Properties of LTP
relied
The initial ezperirments to induce 1TP
on

axons a tetanus (a
iving a bundle of presynaptic then
40 bricf burst of high-frequency stimulation),
measuring the resulting excitatory postsynaptic
n e u r o n (Bear,
potential (F:P5P) in the posty naptic
(Remember, one
Connors, & Paradisx, 1996). An
ncuron can receive input irom many axons.)
ndicates that the cel
FPSP in the postsynaptic cell
mcinbraic has depolarized, or become less nega

tive, as a of the presynaptic inputs. The

resuit
demonstrated that, following
carly cxperiments axons
the
the tetanus, stimulation of presyTaptic
than had been mea
65 cvoked an EP'SP much greatcr
burst
0 2 Surcd (igure 2.2). The stinmulus
previously
Time (ms) in fact, caused a modtication ot the activat
had, such that there
cd synapses (synaptic plasticity)
icreased response to the
postsynaptic
was an
Figure 2.2.
solid level of pre.ynaptic
stimulation ( Bear et al.).
A small excitatory postsynaptic
potential (EPSP; sane

an action potential
in the have claritied that it is
line) occurs as a result of More recently, rescarchers
stmulation that induces LTP
stimu-
of high-frequency
presynaptic n e u r o n . A burst not the tctanie
neuron potentiates element 1s activation of the
lation (tetanus) to the presynaptic Rather, the essential
the EPSP (dashed line).

Cudatrn 2 tieriASTICITY AD THE ENVIPOENT 33

 converging presynaptic neurO1s i the Slme time that the postsynaptic neuron depo
arizes strongly. This porentiates, or modifies, the active synapses such that the presy
naptic neurons are more ettective in their effect on the postsynaptic neuron. This point
becomes important in a subscqucnt example of the use of controlled sensory inpur
during sensory integration reatment. The underlying concept is that several presy
naptie cells converge on and simultancously depolarize a postsynaptic cell, not only
enhancing the EPSP bccause of the summated input (Figure 2.2) but also making it
possible tor the presynaptic cells to depolarize the postsynaptic neuron more ettec
ively. Other synaptic inputs onto the same neuron that are not part of this activation
depolarization coupling (i.c., are not simultancously transmitting depolarizing input
will not show LTP A renarkable feature of LTP is the fact that this increased effec
tiveness ot the presynaptic neuron is long-lasting. Bear et al. (1996) showed that LIP
nduced in awake animals lasts many wecks and possibly even a
lifetime
The role of LTP in sensory integration might be as follows. Consider as an example
the child who cannot tolerate much vestibular stimulation but secks proprioceptive
input, A typical therapeutic activity for such a child couples limited vestibular input
(eg, straddling a hammock swing with feet close to the ground) with strong pro
prioceptive input (such as pulling on a rope) to elicit an adaptive response (e.g,
making the hammock move). Imagine that neither the vestibular nor proprioceptive
1nput alone is capable of evoking an action potential in a postsynaptic neuron on
which coupled activation is capable of firing the post-
they converge, but that their
Synaptic neuron (Figure 2.3). Based on the principles of LTP, each of these simulta-
neously activated inputs becomes more etfective
in its ability to activate the postsynaptic neuron.
LI, theretore, could be one mechanism by which
40 the active synapses are potentiated so that either
vestibular or proprioceptive input might activate
the postsynaptic neuron. That is, LTP allows a
weak input to be potentiated, and in the above
activity, the association of weak vestibular input
wIth strong proprioceptive input could have a
potentiating effect on the weak vestibular input.
The
speculation is that the potentiation occurring
during this activity enhances the function of the
vestibular system.
Although investigators have yet to resolve the
underlying mechanisms of synaptic connectiviry
Time (ms) and plasticity, the fundamental feature is that the
neural activity between the pre- and
postsynaptic
Figure 2.3. neurons cannot be random. Indeed, the timing of
action potentials at both sites is essential in deter-
According to the principles of LTP a weak vestibular
input (solid line) coupled with a more robust proprio mining which synaptic connections are
strength-
ened and retained and,
ceptive input (dashed line) elicits an action potential conversely, which are
(dotted line) in the neuron on which the inputs con- weakened and eliminated. Indeed, Ayres
drew on her knowledge of Hebb's work
(1972b)
verge. This results in both the vestibular and proprio-
ceptive inputs becoming more effective in their ability
regarding
convergent afferent impulses when she stated that
to activate the postsynaptic neuron in the future. summation of stimuli, all relevant to the same
A small excitatory postsynaptic potential (EPSP; solid aspect of environment, can produce response
a
line) occurs as a result of an action potential in the not elicited by one source of stimulus aione. It is
presynaptic neuron. A burst of high-frequerncy stimu- in this respect that the
lation (tetanus) to the and the research into LTP
proposed Hebb synapse
presynaptic neuron potentiates provide support for sen-
the EPSP (dashed
line) sory integration theory and treatment.

34 PART 1: THEORETICAL FOUNDATION

The Rolec of Behavior on Synapse Modification
Hebb synapses and LTP address events at the nolecular level of ncuroplasticIty and
brain development. At the behavioral level, there also is cvidence that he brain must
be stimulated in some way during development in order to achieve the precision of the
adult pattern. An cxtensive amount of cvicdence suggests that behavioral Iactors play
a crucial role in ncural plasticity in thal a synaptic connection undergocs signuticant
modification when its activation comneets with outcomes nportant to the animal's
behaviot. ln other words, neural activity assciated with mcaningful hebavioral
responscs is more likely to promote syn:aptic modifications or neuroplasticily.

Ahissar et al. (1992) recently cxamined whether and how general belhavioral factors
such as attention, motivation, and reinforcement affect functional plasticity. From
elcctrophysiological recordings of auditory cortex neurons in adult monkeys, these
investigators observed that the changes in neuronal functional plasticity were always
greater in the presence of relevant behavior than when behavior was either not pre-
sent or not relcvant. Arnd altlhough Ayres (1972h) did not discuss the eural mecha-
nisms of the adaptive response specilically, she gave nunerous examples of how
motivation for and emotional investment in an activity influcnced a child's progress in
therapy The child who becomes involved in purposeful activity and is wiling to put
forth ettort to make a response of a greater complexity of adaptivity is the child who
usually responds well to treatment. Accordingly, this concept of relevant cngagement
supports the adaptive response that Ayres so strongly encouragcd.

Experience-Dependent Cortical Plasticity

Certain types of sensory nput carly in lite actually encourage the tormation of neur-
al connections. One additional support for neuroplasticity comes from research on the
development ot the visual system in cats. There are certain benetits in studying the
cat's visual system in the ettort to underst:and the relarionsh1p between sensory input
and neural connectivity, the most important being the fact that the cat's visual system
is not mature until 2 months after birth. This maturational period makes it possible
for researchers to control visual experience during the final stages of development and
observe the animal's physiological, anatomical, and hehavioral responses.
Several of the most significant carly studies showed that normal visual experience is
critical to the development of primary visual cortex. Conducted in the 1960s and
1970s by David Hubel and Torsten Wiesel, these studies were an outgrowth of their
examination of the cffects of childhood cataracts. Clinicians had noted that failure to
treat a child's condition promptly led to permanent blindness in the obstructed eye.
From Hubel and Wiesel's research, for which they received the Nobel Prize, emerged
the understanding of critical periods of development (see sidebar on page 36).
Hubel and Wicsel reproduced the effect of a cataract in animals by liniting the activ-
ity of one eye for periods ranging from weeks to moinths, an experimental manipula-
tion called monocular deprivation. They produced monocular deprivation by either
animal's eyes or suturing one lid closel. The
placing opaque lens over one of the
an

physiological consequence of this deprivation was asymmetry of synaptic connections.

Electrophysiological recordings showed that the opcn, seeing eye activated cortical
neurons typically driven by inputs from the deprived eye. Funhemore, the cortical
neurons associated with the open eye elaborated new terminal branches into the cor-
tical territory, carrying informatioj from the deprived eye (Wiesel & lulbel, 1963).
Morcover, the degree of domination by the opcn eyc correlated to the duration of

CHAPTER 2: NEUROPLASTICITY AND 1HE EwvirONAME NT 35

 VIsual deprivation. Even short
exposures during a brief, most sensitive period pro
duced pronounced
changes in cye dominance (Constantine-Paton al., 1990; Olson
et
& Freeman,
1975). This was not the case when deprivation later in life. T he
latter Iinding is consistent with the experience of adult humans began
who develop cataracts
that are corrected
surgically and do not cause
lasting
blindness. This lack of alteration
ot the brain's
wiring following a cataract in adulthood is likely due
to the critical
peri
Od
having ended years earlier. These observations
suggest that cortical connectivity
forms as a result of use early in development.

Critical Periods of
Development
There are critical (or
sensitive) periods during sensory cortical development
when adequate stimulation of the infant is necessary for the brain ulti-
mately to achieve its normal adult characteristics (Harwerth, Smith, Duncan,
Crawford, & von Noorden, 1986). Absence of minimal stimulation (touch,
speech, visual images, etc.) during the first year of a baby's life significantly
delays development in motor, sensory, social, and cognitive domains.
Adverse environments can disrupt normal response properties of sensory
system neurons during the early postnatal period. Therefore, the quality of
the sensory environment during this critical period of development has a
significant impact on performance of mature sensory systems.
Anatomical studies later suppiemented the early electrophysiological data. In the
mature VIsual cortex ot cats, monkeys, and humans, input from each eye is arrangea
Into separate, alternating vertical columns of neurons called ocular dominance
columns. n the newborn, ocular dominance columns have not formed yer and input
to the visual cortex is theretore dittuse rather than neatly segregated into eye-specitic
columns. Monocular dleprivation during the critical period prevents the ocular domi-
1.ance columns from fornming properly (Hubel, Wiescl, & LeVay, 1977; Wiesel, 1982).
These studies demonstrated thar the anatomy of the eye-specific cortical regions also
depends on intact visual input. A likely means for the normally occurring columnar
formation is selective retraction (pruning) of asynchronously activated inputs from
one eye, while correlated activity in specific regions of the visual cortex strengthens
and maintains synaptic contacts from the other eye.

Although the focus of this book is the child with developmental disabilities, it is
mportant to appreciate fully that the end of critical periods of development does not
signal the cnd of plasticity in the brain. Adults exhibit experience-dependent plastici-
ty in some higher cortical areas that is as robust as the plastic changes noted in the
sensory cortical regions of developing brains (Bear et al, 1996). Recent research on
monkeys and other animals shows that the brain continually and dynamically reor-
ganizes itself. Understanding the brain's ability for dynamic reorganization in adult-
hood helps explain how patients sometimes recover brain functions damaged by
injury or disease. Although researchers have recognized for years that new neuronal
connections can emerge with surprising speed tollowing injury even in adulthood
(Schmid, Rosa, & Calford, 1995), recent research has demonstrated that specific
regions of the adult mammalian central nervous system generate new neurons con-
rinuously (Johansson et al., 1999). Ofgreat importance is the finding that the prolif-
eration rate of new neurons increases dramatically in response to central inervous
system injury. This provocative new research could prove valuable in understanding
the mechanisms of neuroplasticity throughout the life span.

PART 1: THEORETICAL FOUNDATION

 The Effects of Prenatal Stress on Function
Prenatal strcss and fetal alcohol cxposure are two arcas of research that demonstrate
the ettects of cnvironmeint, specitically the prenat:al environment,
development and function. Reccnt studies
on nervoUS
by Schneider and others
have shownsysten
that
neuroplasticity and environmental programnming of neural systems are important not
only in the postnatal period but in fact begin in the
prenatal
body of literature exists indicating that the fetal brain period. Indeed,
is cspecially
a large
vulnerable to
damage from toxins and malnourishment. The studies reviewed here provide a model
for understanding how the
prenatal environment can mold o r modify the developing
neural system. Furthermore, these studies have
importait implications for sensory
integration because they demonstrate that the nervous system is changealble and can
be altered by environmental intluences. Understanding environmental risk factors
associated with stress, violence,
toxins, and malnutrition and their
development is important for highlighting key prevcntion issues and mpact upon
vention strategies developing pre-
Schneider and colleagues have been studying innportant changes that occur in the
natal behavior and post-
physiology of rhesus
monkeys born to mothers that experienced
mild, chronic, unpredictable psychological stress during
vide evidence that stressful events pregnancy. These studies pro
birth of the infant can
occurring in the nmother's environment betore the
change the behavioral expression of the infant and cause long-
lasting effects on the individual's behavior and physiology as
In the first study, the animals
development unfolds.
experienced 10-minute stressors (removal from home
cage and exposure to three random loud
noises) that modelled recurrent,
stress on
gestational days 90 to 14S of a 165-day gcstation period. The episodic
stressed monkey offspring were lower in birth prenatally
weight, delayed in independent self-
feeding, more distractible, lower on an evaluation of nmuscle tone (Schneider,
and showed decreased 1992b),
postrotary nystagmus (Schncider & Coe, 1993; Schneider,
Roughton, Koehler, & Lubach, 1999). As they matured, they showed evidence of
delayed cognitive development (Schneider, 1992a), inereased stress
& Schneider, 1993; Schneider, reactivity (Clarke
1992c), altered social and adaptive behavior (Clarke,
Soto, Bergholz, & Schneide, 1996), impaired stress hormone
regulation (Clarke,
Wittwer, Abbott, &t Schneider, 1994), and differences in concentrations of dopamine
and norepinephrine neurotransmitters in cerebral
These studies clearly underscore not spinal fluid (Schneider et al., 1999).
only the vulnerability of the prenatal infant's ner-
vous system but also the short- and
long-term etfects of stress on development, learn-
ing, and levels of brain neurotransmitters.
These results led to an
important question: Is there a critical period during fetal devel-
opment when the brain is most vulnerable to prenatal stress effects and, it so, is there
a time when
prenatal stress has its most s1gniticant ctfects? A second study
the offspring of mothers who were stressed during carly gestation (gestationalcompared
days 45
to 90) to those whose mothers were stressed during mid-late
145) and controls. Infants born
gestation (days 90 to
to mothers exposed to stress i early pregnancy
weighed less and had more pronouncd and more pervasive motor
pared to those from the other two groups. Specifically, the earlyimpairments stress
com-

pregnancy
group demonstrated decreased muscle tone, coordination, balance,
es, and postrotary nystagmus response in
righting respons-
comparison to the mid-late gestation stress
and the control
groups. On measures of attention and motor maturity, aninmals from
both experimental groups scored lower than those
undisturbed pregnancies (Schneider et al., 1998).
monkeys whose mothers had

CPAPTER 2: NrROrLASTLCITY AND TUr Fl

 nCse
inings
motor deticits in
suggest th:at maternal stress can induc a
excess

the results fail to

offspring. However,
from a critical or seus these eftects

support the notion that a scnsitive for

perio
SCnsitive period implies that when particular events occur tside C

specific stage of development, they induce altered structureduring Du (SS:llito, 19

or func ad att
ISprg rom mothers
stressed during either early or mid-late gestatio
ton and neuromotor deficits, although nonkevs stressed during early Be a

nad low birth wcights, mo

decreased postrotary nystagmus, and more s
/10001 ght of thc conceptualizations of the sensitive period by boi
989) and Hinde (1962), it is eriod
perhaps more helpful to view the
as
constant but rather as a peak, skewed to thc onset, followed by sensitivc P
1:y tapers oft. In this light, the data from these studies suggest that plateau
a
a o bra
sensitivity
1.1tal stress
peaks in
early gestation and tapcrs off in mid-late
gestation
Alcohol and Stress
During the Prenatal Period
A
Sccondi issue addressed by the research of Schneider and
stress
Cx:acerbates the effects of other others is whether prena
prenatal
developinent of the offspring adverscly, such as perturbations known to aftect neur
question of whether prenatal stress exposure to alcohol. To deal with t
researchCTS r.andomly cxacerbates the effects of known
teratogens, t
receivcd stress alone, aassigned pregnant monkeys to one of four groups: a groupt
lcohol alonc, and a group
that rcceived stress and
control group that received a alcohol, group that rece
a

Roughio1, & Lubach, 1997). sucrose solution

(Schneid
ic
ndimggs ndieled that alcohol
(the teratogen)
t. re'sulted n increased fetal
losses accompanied by stress during
and birth weight
to stress
alone, alcohol alone, or reductions in
controls. Infants from both the males comp
alcohol-plus-stress conditions demonstrated lower scores on alcohol alone a=
and o t o r
nanurity than controls (Schncider et measures of attentic
exposed utero either to alcohol alone al., 1997). Finally, infants that wa
CocoricOd or alcohol plus stress showed increased gl
responsivity to stress
(Schneider && Kochler, 1997).
Neuronnagng studes are
currently underway to establish the
findings and actual alterations in
neural systems, such as linkage between the-
striatum. In addition, the dopamine
authors
mitter funetion and are
behavioral measuresconducting correlative studiesreceptors
of
in t
neurotrar
between brain hunction and in an ettort to
the behavioral elucidate the relationsh
:ndor prenatal alcohol profile associated with
eNOsure. stre prenatal

Implications for Sensory Integration

Research has shown that
number of behavioral and prenatal stress and/or tetal aleohol
studies provile a model for physiological systems in the exposure can affecr
underst.indingg how the developing offspring.
modify the developing neural system and have
prenatal environment can The-
1tegratiOn important mold.
mplications for senso
Anoher interesting
focus of these stulies
Malleabilityof cetain neural Concerns the
noton of
system
dem:nds of tiheir cnvironment. As noted alows individuals to adaptabili
1oratd into the carlie, environmental adapt to the nia
biology of the mdivicltial the torm ot events
inccbecome
Tealieralions then conie into play whein
im

he
altered neural
orgnin encounters peOCesee
C's
new
exDericne
38 PART 1: THEORETICAL FOUNOATION
 (Boyce et al., 1998). For example, the infants from the prenatal stres group showed
high levels of stress hormones under challenging conditions. Because individuals
whose mothers experienced stress during pregnancy are also likely to be born intoa
stresstul environment, increased release of glucocorticoids in response to stress iglit
enable more rapid mobilization of energy resources and might proniote changes in
cognitive processes necessary to deal with a high-stress environment. However, the
bulk of the evidencc supports the hypothesis that aninmals (including humans) from
prenatally stressed pregnancies show alterations in neuronal functioning that arc sim-
ilar to those occurring in depression in humans (Meijer, 1985; Wadhwa, Dunkel
Schetter, Chicz-DeMet, Porto, & Sandman, 1996).
Other researchers have suggested a model for fetal programming of human disease
basedon the concept of a set point determined during intrauterine life (Barker, 1995).
Additional research hopefully will elucidate some of the processes through which pre-
natal stress transforms neural development. Moreover, rescarchers have yet to deter-
mine how the postnatal cnvironment interacts to attenuate or cxacerbate prenatal
stress effects.
Further studies need to examine glucocorticoid reactivity to stress in individuals with
sensory integrative dysfunction. It is interesting to note that Ayres described children
with sensory integrative disorders as fearful and anxious, which suggests cnhanced or
unmodulated stress responsivity. Additionally, she stated that they tend to be "emo-
tionally labile, . . . less well preparcd to cope,. . and emotionally fragile" (1972b,
p. 210). She also described a now well-known syndrome in which children respond to
tactile stinmulation with anxiety and discomfort and subsequently either withdraw or
display overt hostility (Ayres, 1972b).
In a more recent study, Koomar (1996) studied 5- to 13-year-old children whom occu-
pational therapists had identitied as dyspraxic. She reported two relationships in these
children: one between anxiety and gravitational insecurity and another between anx-
iety and dyspraxia. This important study lends support to Ayres' hypothesis that some
children with sensory integrative dystunction are prone to anxiety and provides fur-
ther suggestion of increased responsivity in these children.
If children with sensory integrative dysfunction show this increased responsivity to
stressful or challenging events, might this hyperresponsivity to stress be alerting the
individual to potential danger and helping to mobilize energy? If so, could reduction
in stress reactivity produce more desirable behavioral responsivity? Further studies by
occupational therapy researchers need to examine the hormonal responses to envi-
ronmental stress or challenge in children with sensory integrative dystunction.

Summary
Central to nmany of the theories deseribing mechanisms by which the infant's nervous
system produces an adaptive response to environmental changes and challenges is the
concept of neural plasticity and the way in which the nervous system organizes and
reorganizes relative to experiences with the environment. This provides important and
significant support for sensory integration therapy and practice in that:
1. Sensory input appears capable of enhancing neural connectivity through LTP
and the Hebb cell.
2 Activity that is meaningful to the individual, or what Ayres called the adaptive
response, promotes this neural activity.
3. There is clear evidence of plasticity in the visual system, and it is likely that plas-
ticity also occurs in other sensory systems.

4. Environment and biology interact in a bidirectional manner, and this begins

early in fetal life.