Habituation

Habituation is a form of non-associative learning in which an innate (non-reinforced) response to a

stimulus decreases after repeated or prolonged presentations of that stimulus.[1] Responses that habituate
include those that involve the intact organism (e.g., full-body startle response) or those that involve only
components of the organism (e.g., habituation of neurotransmitter release from in vitro Aplysia sensory
neurons). The broad ubiquity of habituation across all biologic phyla has resulted in it being called "the
simplest, most universal form of learning...as fundamental a characteristic of life as DNA."[2] Functionally-
speaking, by diminishing the response to an inconsequential stimulus, habituation is thought to free-up
cognitive resources to other stimuli that are associated with biologically important events (i.e.,
punishment/reward). For example, organisms may habituate to repeated sudden loud noises when they
learn these have no consequences.[3] A progressive decline of a behavior in a habituation procedure may
also reflect nonspecific effects such as fatigue, which must be ruled out when the interest is in
habituation.[4] Habituation is clinically relevant, as a number of neuropsychiatric conditions, including
autism, schizophrenia, migraine, and Tourette's, show reductions in habituation to a variety of stimulus-
types both simple (tone) and complex (faces).[5]

Drug habituation
There is an additional connotation to the term habituation which applies to psychological dependency on
drugs, and is included in several online dictionaries.[6] A team of specialist from the World Health
Organization assembled in 1957 to address the problem of drug addiction and adopted the term "drug
habituation" to distinguish some drug-use behaviors from drug addiction. According to the WHO lexicon
of alcohol and drug terms, habituation is defined as "becoming accustomed to any behavior or condition,
including psychoactive substance use".[7] By 1964 the America Surgeon's General report on smoking and
health[8] included four features that characterize drug habituation according to WHO: 1) "a desire (but not a
compulsion) to continue taking the drug for the sense of improved well-being which it engenders"; 2) "little
or no tendency to increase the dose"; 3) "some degree of psychic dependence on the effect of the drug, but
absence of physical dependence and hence of an abstinence syndrome"; 4) "detrimental effects, if any,
primarily on the individual". However, also in 1964, a committee from the World Health Organization once
again convened and decided the definitions of drug habituation and drug addiction were insufficient,
replacing the two terms with "drug dependence". Substance dependence is the preferred term today when
describing drug-related disorders,[9] whereas the use of the term drug habituation has declined substantially.
This is not to be confused with true habituation to drugs, wherein repeated doses have an increasingly
diminished effect, as is often seen in addicts or persons taking painkillers frequently.[10]

Characteristics
Habituation as a form of non-associative learning can be distinguished from other behavioral changes (e.g.,
sensory/neural adaptation, fatigue) by considering the characteristics of habituation that have been identified
over several decades of research. The characteristics first described by Thompson and Spencer[11] were
updated in 2008 and 2009, to include the following:[12]

Repeated presentation of a stimulus will cause a decrease in reaction to the stimulus. Habituation is also
proclaimed to be a form of implicit learning, which is commonly the case with continually repeated stimuli.
This characteristic is consistent with the definition of habituation as a procedure, but to confirm habituation
as a process, additional characteristics must be demonstrated. Also observed is spontaneous recovery. That
is, a habituated response to a stimulus recovers (increases in magnitude) when a significant amount of time
(hours, days, weeks) passes between stimulus presentations.

"Potentiation of habituation" is observed when tests of spontaneous recovery are given repeatedly. In this
phenomenon, the decrease in responding that follows spontaneous recovery becomes more rapid with each
test of spontaneous recovery. Also noted was that an increase in the frequency of stimulus presentation (i.e.,
shorter interstimulus interval) will increase the rate of habituation. Furthermore, continued exposure to the
stimulus after the habituated response has plateaued (i.e., show no further decrement) may have additional
effects on subsequent tests of behavior such as delaying spontaneous recovery. The concepts of stimulus
generalization and stimulus discrimination will be observed. Habituation to an original stimulus will also
occur to other stimuli that are similar to the original stimulus (stimulus generalization). The more similar the
new stimulus is to the original stimulus, the greater the habituation that will be observed. When a subject
shows habituation to a new stimulus that is similar to the original stimulus but not to a stimulus that is
different from the original stimulus, then the subject is showing stimulus discrimination. (For example, if
one was habituated to the taste of lemon, their responding would increase significantly when presented with
the taste of lime). Stimulus discrimination can be used to rule out sensory adaptation and fatigue as an
alternative explanation of the habituation process.

Another observation mentioned is when a single introduction of a different stimulus late in the habituation
procedure when responding to the eliciting stimulus has declined can cause an increase in the habituated
response. This increase in responding is temporary and is called "dishabituation" and always occurs to the
original eliciting stimulus (not to the added stimulus). Researchers also use evidence of dishabituation to
rule out sensory adaptation and fatigue as alternative explanations of the habituation process. Habituation of
dishabituation can occur. The amount of dishabituation that occurs as a result of the introduction of a
different stimulus can decrease after repeated presentation of the "dishabituating" stimulus.

Some habituation procedures appear to result in a habituation process that last days or weeks. This is
considered long-term habituation. It persists over long durations of time (i.e., shows little or no spontaneous
recovery). Long-term habituation can be distinguished from short-term habituation which is identified by
the nine characteristics listed above.

Biological mechanisms
The changes in synaptic transmission that occur during habituation have been well-characterized in the
Aplysia gill and siphon withdrawal reflex. Habituation has been shown in essentially every species of
animal and at least, in one species of plants (Mimosa pudica),[13] in isolated neuronally-differentiated cell-
lines, as well as in quantum perovskite.[14] The experimental investigation of simple organisms such as the
large protozoan Stentor coeruleus provides an understanding of the cellular mechanisms that are involved
in the habituation process.[15]

Neuroimaging

Within psychology, habituation has been studied through different forms of neuroimaging like PET scan
and fMRI. Within fMRI, the response that habituates is the blood oxygen level-dependent (BOLD) signals
triggered by stimuli. Decreases of the BOLD signal are interpreted as habituation.[16]

The amygdala is one of the most-studied areas of the brain in relation to habituation. A common approach is
to observe the visual processing of facial expressions. A study by Breiter and colleagues used fMRI scans
to identify which areas of the brain habituate and at what rate.[17] Their results showed that the human
amygdala responds and rapidly habituates preferentially to fearful facial expressions over neutral ones.
They also observed significant amygdala signal changes in response to happy faces over neutral faces.

Blackford, Allen, Cowan, and Avery (2012) compared the effect of an extremely inhibited temperament
and an extremely uninhibited temperament on habituation. Their study found that over repeated
presentations individuals with an uninhibited temperament demonstrated habituation in both the amygdala
and hippocampus, whereas participants with an inhibited temperament demonstrated habituation in neither
brain region. The researchers suggest that this failure to habituate reflects a social learning deficit in
individuals with an extremely inhibited temperament, which is a possible mechanism for a higher risk of
social anxiety.[18]

Debate about learning-status

Although habituation has been regarded as a learning process by some as early as 1887,[19] its learning
status remained controversial up until the 1920s - 1930s.[20] While conceding that reflexes may "relax" or
otherwise decrease with repeated stimulation, the "invariance doctrine" stipulated that reflexes should not
remain constant and that variable reflexes were a pathological manifestation. Indeed, air pilots who showed
habituation of post-rotational nystagmus reflex were sometimes ejected from or not recruited for service for
World War I: on the grounds that a variable reflex response indicated either a defective vestibular apparatus
or a lack of vigilance.[21][22][20] Eventually, however, more research from the medical and scientific
communities concluded that stimulus-dependent variability reflexes is clinically normal.[23] The opposition
to the considering habituation a form of learning was also based on the assumption that learning processes
must produce novel behavioral responses and must occur in the cerebral cortex.[21] Non-associative forms
of learning such as habituation (and sensitization) do not produce novel (conditioned) responses but rather
diminish a pre-existing (innate) responses and often are shown to depend on peripheral (non-cerebral)
synaptic changes in the sensory-motor pathway. Most modern learning theorists, however, consider any
behavioral change that occurs as a result of experience to be learning, so long as it cannot be accounted for
by motor fatigue, sensory adaptation, developmental changes or damage.

Criteria for verifying a response-decline as learning

Importantly, systematic response-declines can be produced by non-learning factors such as sensory

adaptation (obstruction of stimulus detection), motor fatigue, or damage. Three diagnostic criteria are used
to distinguish response-declines produced by these non-learning factors and response-declines produced by
habituation (learning) processes. These are:

1. Recovery by Dishabituation
2. Sensitivity of Spontaneous Recovery to Rate-of-Stimulation
3. Stimulus-specificity

Early studies relied on the demonstration of 1) Recovery by Dishabituation (the brief recovery of the
response to the eliciting stimulus when another stimulus is added) to distinguish habituation from sensory
adaptation and fatigue. More recently, 2) Sensitivity of Spontaneous Recovery to Rate-of-Stimulation and 3)
Stimulus-specificity have been used as experimental evidence for the habituation process.[12] Spontaneous
Recovery is sensitive to spontaneous recovery, showing recovery that is inversely correlated with the
amount of response-decline. This is the opposite of what would be expected if sensory adaptation or motor
fatigue were the cause of the response-decline. Sensory adaptation (or neural adaptation) occurs when an
organism can no longer detect the stimulus as efficiently as when first presented and motor fatigue occurs
when an organism is able to detect the stimulus but can no longer respond efficiently. Stimulus-specificity
stipulates that the response-decline is not general (due to motor fatigue) but occurs only to the original
stimulus that was repeated. If a response-decline shows 1) dishabituation, 2) spontaneous recovery that is
inversely correlated with the extent of decline, and/or 3) stimulus-specificity, then habituation learning is
supported.

Despite the ubiquity of habituation and its modern acceptance as a genuine form of learning it has not
enjoyed the same focus within research as other forms of learning. On this topic, the animal psychologist
James McConnell said “...nobody cares…much about habituation”).[24] It has been suggested that the
apathy held towards habituation is due to 1) resistance from traditional learning theorists maintain memory
requires reproduction of propositional/linguistic content; 2) resistance from behaviorists who maintain that
"true" learning requires the development of a novel response (whereas habituation is a decrease in a pre-
existing response); 3) the behavioral measure of habituation (i.e., a response-decline) is very susceptible to
confound by non-learning factors (e.g., fatigue) which, therefore, make it more difficult to study).

Theories
Various models have been proposed to account for habituation including the Stimulus-Model Comparator
theory formulated by Evgeny Sokolov,[25] the Groves and Thompson dual-process theory,[26] and the SOP
(Standard Operating Procedures/Sometimes Opponent Process) model formulated by Allan Wagner [27]

Stimulus-model comparator theory

The stimulus-model comparator theory emerged from the research of Sokolov who used the orienting
response as the cornerstone of his studies, and operationally defining the orienting response as EEG
activity. Orienting responses are heightened sensitivity experienced by an organism when exposed to a new
or changing stimulus. Orienting responses can result in overt, observable behaviors as well as
psychophysiological responses such as EEG activity and undergo habituation with repeated presentation of
the eliciting stimulus. The Sokolov model[25] assumes that when a stimulus is experienced several times,
the nervous system creates a model of the expected stimulus (a stimulus model). With additional
presentations of the stimulus, the experienced stimulus is compared with the stimulus model. If the
experienced stimulus matches the stimulus model, responding is inhibited. At first the stimulus model is not
a very good representation of the presented stimulus, and thus responding continues because of this
mismatch. With additional presentations the stimulus model is improved, there is no longer a mismatch, and
responding is inhibited causing habituation. However, if the stimulus is changed so that it no longer
matches the stimulus model, the orienting response is no longer inhibited. Sokolov locates the stimulus
model in the cerebral cortex.

Dual-process theory

The Groves and Thompson dual-process theory of habituation posits that two separate processes exist in
the central nervous system that interacts to produce habituation. The two distinct processes are a habituation
process and a sensitization process. The dual-process theory argues that all noticeable stimuli will elicit both
of these processes and that the behavioral output will reflect a summation of both processes. The
habituation process is decremental, whereas the sensitization process is incremental enhancing the tendency
to respond. Thus when the habituation process exceeds the sensitization process behavior shows
habituation, but if the sensitization process exceeds the habituation process, behavior shows sensitization.
Groves and Thompson hypothesize the existence of two neural pathways: an "S-R pathway" involved with
the habituation process, and a "state pathway" involved with sensitization. The state system is seen as
equivalent to a general state of arousal.[26]

Examples of the habituation process in animals and humans

Habituation has been observed in an enormously wide range of species from motile single-celled organisms
such as the amoeba[28] and Stentor coeruleus[15] to sea slugs[29] to humans.[30] Habituation processes are
adaptive, allowing animals to adjust their innate behaviors to changes in their natural world. A natural
animal instinct, for example, is to protect themselves and their territory from any danger and potential
predators. An animal needs to respond quickly to the sudden appearance of a predator. What may be less
obvious is the importance of defensive responses to the sudden appearance of any new, unfamiliar stimulus,
whether it is dangerous or not. An initial defensive response to a new stimulus is important because if an
animal fails to respond to a potentially dangerous unknown stimulus, the results could be deadly. Despite
this initial, innate defensive response to an unfamiliar stimulus, the response becomes habituated if the
stimulus repeatedly occurs but causes no harm. An example of this is the prairie dog habituating to humans.
Prairie dogs give alarm calls when they detect a potentially dangerous stimulus. This defensive call occurs
when any mammal, snake, or large bird approaches them. However, they habituate to noises, such as
human footsteps, that occur repeatedly but result in no harm to them. If prairie dogs never habituate to
nonthreatening stimuli, they would be constantly sending out alarm calls and wasting their time and
energy.[31] However, the habituation process in prairie dogs may depend on several factors including the
particular defensive response. In one study that measured several different responses to the repeated
presence of humans, the alarm calls of prairie dogs showed habituation whereas the behavior of escaping
into their burrows showed sensitization.[32]

Another example of the importance of habituation in the animal world is provided by a study with harbor
seals. In one study researchers measured the responses of harbor seals to underwater calls of different types
of killer whales.[33] The seals showed a strong response when they heard the calls of mammal-eating killer
whales. However, they did not respond strongly when hearing familiar calls of the local fish-eating
population. The seals, therefore, are capable of habituating to the calls of harmless predators, in this case,
harmless killer whales. While some researchers prefer to simply describe the adaptive value of observable
habituated behavior, others find it useful to infer psychological processes from the observed behavior
change. For example, habituation of aggressive responses in male bullfrogs has been explained as "an
attentional or learning process that allows animals to form enduring mental representations of the physical
properties of a repeated stimulus and to shift their focus of attention away from sources of irrelevant or
unimportant stimulation".[34]

Habituation of innate defensive behaviors is also adaptive in humans, such as habituation of a startle
response to a sudden loud noise. But habituation is much more ubiquitous even in humans. An example of
habituation that is an essential element of everyone's life is the changing response to food as it is repeatedly
experienced during a meal. When people eat the same food during a meal, they begin to respond less to the
food as they become habituated to the motivating properties of the food and decrease their consumption.
Eating less during a meal is usually interpreted as reaching satiety or "getting full", but experiments suggest
that habituation also plays an important role. Many experiments with animals and humans have shown that
providing variety in a meal increases the amount that is consumed in a meal, most likely because
habituation is stimulus-specific and because variety may introduce dishabituation effects.[35] Food variety
also slows the rate of habituation in children and may be an important contributing factor to the recent
increases in obesity.[36]
We also find that habituation is found in our emotional responses, called the opponent-process theory,
proposed by researchers Richard Solomon and John Corbit (1974). It is known that responses by the
subject tend to change by repetitively presenting certain stimuli. But concerning the opponent-process
theory, some emotional reactions to the stimuli weaken (decrease) while others' reactions are strengthened
(increase). Take, for example, that it is the end of the semester at your university. You have been worried
about your grade for the entire semester and you need a grade of "A" on the final to pass the course. You
study efficiently for the test and after taking it, you feel that you will receive a very high grade. But once
you check the gradebook, you see that you did not get an "A" on your exam. Instead, you received a "C+".
Now you are distraught and know that there is no other way to pass the course for the semester. After a few
minutes you begin to calm down and by the next hour, you are back to your normal emotional state. This is
an example of an emotional response explained by the opponent-process theory. It begins with an outside
stimulus provoking an emotional reaction that increases rapidly until it is at its most intense (presumably
after you learned that you did not receive a high letter grade). Gradually, your emotional state declines to a
level lower than normal and eventually returns to neutral. This pattern coincides with two internal processes
referred to as the a-process and b-process. The a-process, or "affective" response to a stimulus, is the initial
emotional response one has and can be pleasant or unpleasant. The b-process is the after reaction and has a
lower intensity than the a-process. The a-process is very fast-acting and ends as soon as the stimulus ends
or is removed. Unlike the a-process, the b-process is much slower in returning to baseline. Concerning the
definition of the opponent process theory—repeated presentations present habituation—the a-process does
not necessarily change. It is the b-process that is strengthened instead and rises more quickly to reach the
highest intensity, and much slower in attempting to return to baseline after the stimulus is removed. To sum
it all up, with the opponent-process theory, repeated presentations of the same stimulus will result in
habituation, where subjects show little to no reaction. It is the after-reaction that is much larger and
prolonged, than if an initial reaction to a stimulus occurred.[37]

Relevance to neuropsychiatry
Habituation abnormalities have been repeatedly observed in a variety of neuropsychiatric conditions
including autism spectrum disorder (ASD), fragile X syndrome, schizophrenia, Parkinson's disease (PD),
Huntington's disease (HD), attention deficit hyperactivity disorder (ADHD), Tourette's syndrome (TS), and
migraine.[5] In human clinical studies, habituation is most often studied using the acoustic startle reflex;
acoustic tones are delivered to participants through headphones and the subsequent eye-blink response is
recorded directly by observation or by electromyography (EMG). Depending on the disorder, habituation
phenomena have been implicated as a cause, symptom, or therapy.[5] Reduced habituation is the most
common habituation phenotype reported across neuropsychiatric disorders although enhanced habituation
has been observed in HD and ADHD.[5] It also appears that abnormal habituation is often predictive of
symptom severity in several neuropsychiatric disorders, including ASD,[38] PD,[39] and HD.[40][41]
Moreover, there are instances where treatments that normalise the habituation-deficit also improve other
associated symptoms.[42] As a therapy, habituation processes have been hypothesized to underlie the
efficacy of behavioural therapies (i.e. habit reversal training, exposure therapy) for TS and PTSD,[43]
although extinction processes may be operating instead.

Uses and challenges of the habituation procedure

Habituation procedures are used by researchers for many reasons. For example, in a study on aggression in
female chimpanzees from a group known as the "Kasakela Chimpanzee Community", researchers
habituated the chimpanzees by repeatedly exposing them to the presence of human beings.[44] Their efforts
to habituate the chimpanzees before the field researchers studied the animal's behavior was necessary in
order for them to eventually be able to note the natural behavior of the chimpanzees, instead of simply
noting chimpanzee behavior as a response to the presence of the researchers. In another study, Mitumba
chimpanzees in the Gombe National Park were habituated for at least four years before the introduction of
systematic data collection.[45]

Researchers also use habituation and dishabituation procedures in the laboratory to study the perceptual and
cognitive capabilities of human infants. The presentation of a visual stimulus to an infant elicits looking
behavior that habituates with repeated presentations of the stimulus. When changes to the habituated
stimulus are made (or a new stimulus is introduced), the looking behavior returns (dishabituates). A recent
fMRI study revealed that the presentation of a dishabituating stimulus has an observable, physical effect
upon the brain.[46] In one study the mental spatial representations of infants were assessed using the
phenomenon of dishabituation.[47] Infants were presented repeatedly with an object in the same position on
a table. Once the infants habituated to the object (i.e., spent less time looking at it) either the object was
spatially moved while the infant remained at the same place near the table or the object was left in the same
place but the infant was moved to the opposite side of the table. In both cases, the spatial relationship
between the object and the infant had changed, but only in the former case did the object itself move.
Would the infants know the difference? Or would they treat both cases as if the object itself moved? The
results revealed a return of looking behavior (dishabituation) when the object's position was changed, but
not when the infant's position was changed. Dishabituation indicates that infants perceived a significant
change in the stimulus. Therefore, the infants understood when the object itself moved and when it did not.
Only when the object itself moved were they interested in it again (dishabituation). When the object
remained in the same position as before it was perceived as the same old boring thing (habituation). In
general, habituation/dishabituation procedures help researchers determine the way infants perceive their
environments.

Habitation is a useful primary tool for then assessing mental processes in the stages of infancy. The purpose
for these tests, or paradigms records looking time, which is the baseline measurement. Habituation of
looking time helps to assess certain child capabilities such as: memory, sensitivity, and helps the baby
recognize certain abstract properties. Habituation is also found to be influenced by unchangeable factors
such as infant age, gender, and complexity of the stimulus. (Caron & Caron, 1969; Cohen, DeLoache, &
Rissman, 1975; Friedman, Nagy, & Carpenter, 1970; Miller, 1972; Wetherford & Cohen, 1973).

Though there are various challenges that come with habituation. Some infants have preferences for some
stimuli based on their static or dynamic properties. Infant dishabituation also is not perceived as a direct
measure for mental processes as well. In previous theories of habituation, an infant's dishabituation was
thought to represent their own realization of the remembered stimulus of stimuli. For example: if infants
would be dishabituated to a certain color item to a new item, we would know that they remembered the
color and compared the two colors for differences. Also, another challenge that comes with habituation is
the dichotomy of novelty vs familiar stimuli. If an infant preferred a novel still, this meant the infant
observed the new spatial relation of the object, but not the object itself. If an infant preferred familiarity, the
infant would notice the pattern of the stimuli, instead of the actual new stimuli.
[48]

The habituation/dishabituation procedure is also used to discover the resolution of perceptual systems. For
instance, by habituating someone to one stimulus, and then observing responses to similar ones, one can
detect the smallest degree of difference that is detectable.

See also
Psychology portal
 Adaptive system
Aplysia
Consumer demand tests (animals)
Desensitization (psychology)
Hedonic adaptation
Konrad Lorenz, Behind the Mirror: A Search for a Natural History of Human Knowledge: on
habituation (https://books.google.com/books?id=7al9AAAAMAAJ&q=habituation)
Preference tests (animals)
Tachyphylaxis, the effect of continued exogenous entries (habituation of) into the metabolism
of an organism within the scope/field of biological chemistry

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Further reading
Kececi, H.; Degirmenci, Y.; Atakay, S. (2006). "Habituation and Dishabituation of P300".
Cognitive and Behavioral Neurology. 19 (3): 130–134.
doi:10.1097/01.wnn.0000213911.80019.c1 (https://doi.org/10.1097%2F01.wnn.000021391
1.80019.c1). PMID 16957490 (https://pubmed.ncbi.nlm.nih.gov/16957490).
S2CID 41790159 (https://api.semanticscholar.org/CorpusID:41790159).

External links
Dana Sugu & Amita Chaterjee 'Flashback: Reshuffling Emotions', International Journal on
Humanistic Ideology, Vol. 3 No. 1, Spring-Summer 2010 [1] (https://sites.google.com/site/sug
udana/articles-1)
Usabilityfirst.com.=913 "Definition of Habituation" (https://web.archive.org/web/2004121109
0446/http://www.usabilityfirst.com/glossary/main.cgi?function=display_term). Retrieved
August 29, 2008.
BBC "Definition in context" (https://www.bbc.co.uk/dna/h2g2/A914339). Retrieved August
24, 2009.

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