Animal habituation and sensitization

Habituation is a simple form of nonassociative learning that has been demonstrated in organisms as diverse as protozoans, insects, Nereis (clam or ragworms), birds, and humans. The habituated organism learns to ignore irrelevant, repetitive stimuli, which, prior to habituation, would have produced a response. With each presentation of the habituating stimulus, the responsiveness of the organism decreases toward the zero, non-response level. If habituation training continues after the zero-response level, the habituation period is prolonged. Habituation to a particular stimulus naturally and gradually disappears unless the training continues. If training is resumed after habituation has disappeared, habituation occurs more rapidly in the second training series than in the first. Habituation is important for the survival of the individual. Many stimuli are continuously impinging upon it. Some are important, others are not. Important stimuli require an immediate response, but those that result in neither punishment nor reward may be safely ignored.

Stimulus and Response

When a new stimulus is presented (when a sudden change in the environment occurs), the organism—be it a bird, beast, or human—exhibits the “startle” or “orientation” response. In essence, it stops, looks, and listens. If the stimulus is repeated and is followed by neither reward nor punishment, the organism will pay less and less attention to it. When this happens, habituation has occurred, and the organism can now respond to and deal with other stimuli. On the other hand, if, during habituation learning, a painful consequence follows a previously nonconsequential stimulus, the organism has been sensitized to that stimulus and will respond to it even more strongly than it did before the learning sessions, whether they are occurring in the laboratory or in the field.

Young birds must learn to tell the difference between and respond differently to a falling leaf and a descending predator. A young predatory bird must learn to ignore the reactions of its prey, which pose no danger, and the reactions that the predator initially feared.

A theory known as the dual-process habituation-sensitization theory was formulated in 1966 and revised in 1973. It establishes criteria for both habituation and sensitization. Criteria for habituation (similar to those proposed by E. N. Sokolov in 1960) are that habituation will develop rapidly; the frequency of stimulation determines the degree of habituation; if stimulation stops for a period of time, habituation will disappear; the stronger the stimulus, the slower the rate of habituation; the frequency of stimulation is more important than the strength of the stimulus; rest periods between habituation series increase the degree of habituation; and the organism will generalize and therefore exhibit habituation to an entire class of similar stimuli. Stimulus generalization can be measured: If a different stimulus is used in the second habituation series, habituation occurs more rapidly; it indicates generalization.

Sensitization

Sensitization, a very strong response to a very painful, injurious, or harmful stimulus, is not limited to stimulus-response circuits but involves the entire organism. After sensitization, the individual may respond more strongly to the habituating stimulus than they did prior to the start of habituation training.

There are eight assumptions about sensitization in the dual-process theory. Sensitization does not occur in stimulus-response circuits but involves the entire organism. Sensitization increases during the early stages of habituation training but later decreases. The stronger the sensitizing stimulus and the longer the exposure to it, the greater the sensitization. Weaker stimuli may fail to produce any sensitization. Even without any external intervention, sensitization will decrease and disappear. Increasing the frequency of sensitization stimulation causes a decrease in sensitization. Sensitization will extend to similar stimuli. Dishabituation, the loss of habituation, is an example of sensitization. Sensitization may be time-related, occurring only at certain times of the day or year.

According to the dual-process theory, the response of an organism to a stimulus will be determined by the relative strengths of habituation and sensitization. Charles Darwin, the father of evolution, observed and described habituation, although he did not use the term. He noted that the birds of the Galápagos Islands were not disturbed by the presence of the giant tortoises, Amblyrhynchus; they disregarded them just as the magpies in England, which Darwin called “shy” birds, disregarded cows and horses grazing nearby. Both the giant tortoises of the Galápagos Islands and the grazing horses and cows of England were stimuli which, though present, would not produce profit or loss for the birds; therefore, they could be ignored.

The Neurology of Stimulus Response

Within the bodies of vertebrates is a part of the nervous system called the reticular network or reticular activating system; it has been suggested that the reticular network is largely responsible for habituation. It extends from the medulla through the midbrain to the thalamus of the forebrain. (The thalamus functions as the relay and integration center for impulses to and from the cerebrum of the forebrain.) Because it is composed of a huge number of interconnecting neurons and links all parts of the body, the reticular network functions as an evaluating, coordinating, and alarm center. It monitors incoming message impulses. Important ones are permitted to continue to the cerebral cortex, the higher brain. Messages from the cerebral cortex are coordinated and dispatched to the appropriate areas.

During sleep, many neurons of the reticular network stop functioning. Those that remain operational may inhibit response to unimportant stimuli (habituation) or cause hyperresponsiveness (sensitization). The cat who is accustomed to the sound of kitchen cabinets opening will sleep through a human’s dinner being prepared (habituation) but will charge into the kitchen when she hears the cat food container opening (sensitization).

Researcher E. N. Sokolov concluded that the “orientation response” (which can be equated with sensitization) and habituation are the result of the functioning of the reticular network. According to Sokolov, habituation results in the formation of models within the reticular activating system. Incoming messages that match the model are disregarded by the organism, but those that differ trigger alerting reactions throughout the body, thus justifying the term “alerting system” as a synonym for the reticular network. Habituation to a very strong stimulus would take a long time. Repetition of this strong stimulus would cause an even stronger defensive reflex and would require an even longer habituation period.

The Role of Neurotransmitters

Neurotransmitters are chemical messengers that enable nerve impulses to be carried across the synapse, the narrow gap between neurons. They transmit impulses from the presynaptic axon to the postsynaptic dendrite(s). Eric R. Kandel, in experiments with Aplysia californica (the sea hare, a large mollusk), demonstrated that as a habituation training series continues, smaller amounts of the neurotransmitter acetylcholine are released from the axon of the presynaptic sensory neuron. On the other hand, after sensitization, this neuron released larger amounts of acetylcholine because of the presence of serotonin, a neurotransmitter secreted by a facilitatory interneuron. When a sensitizing stimulus is very strong, it usually generates an impulse within the control center—a ganglion, a neuron, or the brain. The control center then transmits an impulse to a facilitatory interneuron, causing the facilitatory interneuron to secrete serotonin.

Increased levels of acetylcholine secretion by the sensory neuron result from two different stimuli: direct stimulation of the sensory neurons of the siphon or serotonin from the facilitatory interneuron. Facilitatory interneurons synapse with sensory neurons in the siphon. Serotonin discharged from facilitatory interneurons causes the sensory neurons to produce and secrete more acetylcholine.

On the molecular level, the difference between habituation and adaptation—the failure of the sensory neuron to respond—is very evident. The habituated sensory neuron has a neurotransmitter in its axon but is unable to secrete it, thereby enabling the impulse to be transmitted across the synapse. The adapted sensory neuron, by contrast, has exhausted its current supply of neurotransmitters. Until new molecules of neurotransmitter are synthesized within the sensory neuron, none is available for release.

In 1988, Emilie A. Marcus, Thomas G. Nolen, Catherine H. Rankin, and Thomas J. Carew published the multiprocess theory to explain dishabituation and sensitization in the sea hare, Aplysia. Based on their experiments using habituated sea hares that were subjected to different stimuli, they concluded that dishabituation and sensitization do not always occur together; further, they decided there are three factors to be considered: dishabituation, sensitization, and inhibition.

Habituation Studies

Habituation studies have utilized a wide variety of approaches, ranging from the observation of intact organisms carrying out their normal activities in their natural surroundings to the laboratory observation of individual nerve cells. With different types of studies, very different aspects of habituation and sensitization can be investigated. Surveying the animal kingdom in 1930, G. Humphrey concluded that habituation-like behavior exists at all levels of life, from the simple one-celled protozoans to the multicelled, complex mammals.

E. N. Sokolov, a compatriot of Ivan P. Pavlov, used human subjects in the laboratory. In 1960, he reported on the results of his studies, which involved sensory integration, the makeup of the orientation reflex (which he credited Pavlov with introducing in 1910), a neuronal model and its role in the orientation reflex, and the way that this neuronal model could be used to explain the conditioned reflex. Sokolov measured changes in the diameter of blood vessels in the head and finger, changes in electrical waves within the brain, and changes in the electrical conductivity of the skin. By lowering the intensity of a tone to which human subjects had been habituated, Sokolov demonstrated that habituation was not the result of fatigue because subjects responded to the lower-intensity tone with the startle or orientation reflex just as they would when a new stimulus was introduced. Sokolov concluded that the orientation response (which is related to sensitization) and habituation are the result of the functioning of the reticular network of the brain and central nervous system. Sokolov emphasized that the orientation response was produced after only the first few exposures to a particular stimulus, and it increased the discrimination ability of internal organizers. The orientation response was an alerting command. Heat, cold, electric shock, and sound were the major stimuli that he used in these studies.

E. R. Kandel used the sea hare, Aplysia, in his habituation-sensitization studies. Aplysia is a large sluglike mollusk with a sheetlike shell-producing body covering the mantle. Aplysia has a relatively simple nervous system and an easily visible gill-withdrawal reflex. (The gill is withdrawn into the mantle shelf.) Early habituation-sensitization experiments dealt with withdrawal or absence of gill withdrawal. Later experiments measured electrical changes that occurred within the nerve cells that controlled gill movement. These were followed by studies that demonstrated that the gap (synapse) between the receptor nerve cell (sensory neuron) and the muscle-moving nerve cell (motor neuron) was the site where habituation and dishabituation occurred and that neurohormones such as acetylcholine and serotonin played essential roles in these processes. Kandel called the synapse the “seat of learning.”

Charles Sherrington used spinal animals in which the connection between the brain and the spinal nerve cord had been severed. Sherrington demonstrated that habituation-sensitization could occur within the spinal nerve cord even without the participation of the brain. Pharmaceuticals have also been used in habituation-sensitization studies. Michael Davis and Sandra File used neurotransmitters such as serotonin and norepinephrine to study modification of the startle (orientation) response.

Habituation studies conducted in the laboratory enable researchers to control variables such as genetic makeup, previous experiences, diet, and the positioning of subject and stimulus; however, they lack many of the background stimuli present in the field. In her field studies of the chimpanzees of the Gombe, Jane Goodall used the principles of habituation to decrease the distance between herself and the wild chimpanzees until she was able to come close enough to touch and be accepted by them. The field-experimental approach capitalizes on the best of both laboratory and field techniques. In this approach, a representative group of organisms that are in their natural state and habitat are subjected to specific, known stimuli.

Learning to Survive

Habituation is necessary for survival. Many stimuli are constantly impinging upon all living things; since it is biologically impossible to respond simultaneously to all of them, those that are important must be dealt with immediately. It may be a matter of life or death. Those that are unimportant or irrelevant must be ignored.

Cell physiologists and neurobiologists have studied the chemical and electrical changes that occur between one nerve cell and another and between nerve and muscle cells. The results of those studies have been useful in understanding and controlling these interactions as well as in providing insights for therapies. Psychologists utilize the fruits of habituation studies to understand, predict, modify, and control the behavior of intact organisms. For example, knowing that bulls serving as sperm donors habituate to one cow or model and stop discharging sperm into it, the animal psychologist can advise the semen collector to use a different cow or model or simply to move it to another place—even as close as a few yards away.

Conservationists and wildlife protectionists can apply the principles of habituation to wild animals, which must live in increasingly closer contact with one another and with humans so that both animal and human populations can survive and thrive. For example, black-backed gulls, when establishing their nesting sites, are very territorial. Males that enter the territory of another male gull are rapidly and viciously attacked. After territorial boundaries are established, however, the males in contiguous territories soon exhibit “friendly enemy” behavior: They are tolerant of the proximity of other males that remain within their territorial boundaries. This has been observed in other birds as well as in fighting fish.

In a study of yellow-bellied marmots (Marmota flaviventer) in high and low human disturbance colonies, those living in high-disturbance areas tended to practice higher vigilance on average than those in low-disturbance areas. Even after fifteen years of study and several generations of marmots living in areas with humans, they remained vigilant. However, the distance at which they would flee from humans decreased over time, meaning they let humans get closer to them over time. Though these factors indicated that marmots' proximity to human development caused little harm, their average body mass was lower than that of those living in less disturbed colonies, indicating poor fitness outcomes.

Principal Terms

Acetylcholine: A neurotransmitter produced by a nerve cell that enables a nerve impulse to cross a synapse and reach another nerve or muscle cell

Aplysia: A large sluglike mollusk that lives in saltwater and has been used in habituation experiments; its outer covering is called the mantle

Impulse: A “message” traveling within a nerve cell to another nerve cell or to a muscle cell

Motor Neuron: Nerve cell that causes a muscle cell to respond

Neurotransmitter: A chemical substance that enables nerve impulses to cross a synapse and reach another nerve cell or muscle cell

Orienting Reflex: An unspecific reflex reaction caused by a change in the quantity or quality of a stimulus; it will disappear or decrease after repeated presentations of the stimulus

Sensitization: An arousal or an alerting reaction that increases the likelihood that an organism will react; also, a synonym for loss of habituation with increased intensity of response

Synapse: The minute space or gap between the axon of one nerve cell and the dendron of the next; also, the gap between a nerve cell and a muscle cell

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