Synonyms

Familiarization; Nonassociative learning

Definition

Habituation is a process of diminishing responsiveness due to the presentation of a repeated stimulus.

Introduction

Habituation constitutes an essential process of behavioral adaptation, as it assists in filtering out the large amounts of information received from the surrounding environment that are likely irrelevant or less important, thus shifting attention to more important to survival or urgent information. The latter gives an evolutionary advantage as a result.

Theoretical Background

Several influential nonassociative theories have historically been proposed Thompson (2009). These theories constitute the early work of Sokolov (1960) and Wagner’s (1979) revision of Konorski’s Gnostic Hypothesis, and Groves and Thompson’s (1970) dual process theory.

Sokolov (1960) was the first to propose a comprehensive theory of habituation (“Stimulus-Model Comparator Theory”). In short, Sokolov’s theory stated that when a stimulus appears repetitively, the brain cortex forms a model (or a memory) of the stimulus. Each incoming stimuli were compared to the model and if the incoming stimulus matched the model, responding was inhibited; otherwise, an orienting response was evoked. The exertion of inhibition was thought to yield habituation; thus, habituation was perceived as purely inhibitory. Even though Sokolov’s work intrigued a great bulk of follow-up investigations in habituation in the human kind, the theory was not applicable to animals who do not possess a cortex, contrary to the dual process theory.

Another comparator theory constitutes the work of Konorski’s on habituation which shared many similarities with Sokolov’s theory. Wagner (1979) revisited Konorski’s ideas but he concentrated on the roles of short-term memory and associative mechanisms. A stimulus is carried by afferent/sensory neurons toward a memory system, the Gnostic assembly, and to the arousal system. With repeated stimulation, a gnostic unit is formed, that is a near accurate neuronal model or memory of the stimulus. As this model develops, it increasingly activates an inhibitory system that inhibits the arousal system, consequently causing habituation. Wagner added a process mediator, an associative network where contextual cues have to pass through in order to excite stimulus models in memory and a process of transient memory (short-term memory). In short, what these scientists advocated is that long-term habituation requires the storage of a stimulus in long-term memory and that it is associated with external cues for retrieval from long-term memory.

Finally, the most prominent nonassociative learning theory was proposed by Groves and Thompson (1970). Neurophysiological concepts were combined with concerns of human ethology and evolution to create the dual process theory. This theory advocated that repeated stimulation would produce two independent processes that could both be active at the same time; decreased responsiveness (habituation) or increased responsiveness (sensitization). The authors believed that the two processes take place in different parts of the nervous system. Scientists believed that habituation took place in the so-called S-R system (reflex arc) that controls reflexes whereas sensitization occurred in the “state system” which is responsible for the level of readiness to respond. The state system requires arousal to become activated while the S-R system is activated with the presentation of an eliciting stimulus. Further, habituation is thought to be stimulus specific and involves learning, in contrast to sensitization which is not highly specific and does not require learning. However, both are of relative permanence; they are expected to decay at the absence of stimulation. Contrary to Sokolov’s model, the dual process theory does not propose an inhibitory system.

Nevertheless, all these studies of cellular processes which facilitate learning and memory, which were mostly held in invertebrates, most certainly add to the understanding of the underlying physiological processes of learning in the majority of living animal organisms, but mechanisms such as habituation and sensitization are far more complex and necessitate further exploration.

The Nature of Habituation

Habituation constitutes an essential process of behavioral adaptation, as it assists in filtering out the large amounts of information received from the surrounding environment that are likely irrelevant or less important, thus shifting attention to more important to survival or urgent information. The latter gives an evolutionary advantage as a result. Habituation is the simplest form of nonassociative learning and it can be defined as a decline in behavioral responsiveness to the continual presentation of a stimulus. While there is a strong response initially, the strength of the response reduces and eventually disappears with repeated stimulation. The reduction in responsiveness is neither the result of motor (muscle) fatigue nor sensory adaptation; however, it is likely to be disrupted when another strong stimulus appears (dishabituation). Other factors influencing habituation include stimulus repetition, interstimulus interval, and stimulus intensity. These factors are determinant of whether short- or long-term habituation will occur. Short-term habituation is characterized by rapid stimulations with short intervals in between, habituation is observed early; however, it is short-lived as soon as stimulation ceases. On the other hand, long-term habituation is characterized by fewer stimulations over longer periods; habituation is slower but its effects are long-lived as recovery is delayed.

In addition, in earlier writings, habituation was thought to only have short-term effects (Hinde 1970); however, existing literature has demonstrated that its effects can last long. Apart from its simplicity, habituation is thought to be ubiquitous; it is both a highly automated yet learned phenomenon occurring in the central nervous system (CNS) of all animal species, ranging from single-celled protozoans to humans Thompson (2009), with studies demonstrating its occurrence in plants as well Gagliano, Renton, Depczynski, Mancuso (2014). Thompson and Spencer (1966) presented a list of nine parameters of habituation, shared by all species. A tenth parameter was added to the list of behavioral characteristics of habituation by Rankin et al. (2009) and are all presented as follows:

  1. 1.

    Given that a particular stimulus produces a response, repetitive applications of that stimulus will result in a reduced response (habituation). Most of the times, the decrease is a negative exponential function of the number of stimulus presentations.

  2. 2.

    If the stimulus is withheld, the response tends to recover over time (“spontaneous recovery”).

  3. 3.

    After a multiple series of stimulus repetitions and spontaneous recoveries, habituation becomes more rapid (“potentiation of habituation”).

  4. 4.

    The more rapid the frequency of stimulation, the more rapid and/or more pronounced is habituation.

  5. 5.

    The weaker the stimulus, the more rapid and/or more pronounced is habituation. Stronger stimulation might yield no significant habituation.

  6. 6.

    The effects of habituation training may proceed beyond the zero or asymptotic (minimum level of response) response level.

  7. 7.

    Habituation of response to a stimulus displays stimulus generalization to other stimuli.

  8. 8.

    Presentation of another strong stimulus results in disruption or recovery of the habituated response (“dishabituation”).

  9. 9.

    After repeated application of the dishabituatory stimulus, the amount of dishabituation produced habituates (“habituation of dishabituation”).

  10. 10.

    Some stimulus repetition protocols may result in properties of the response decrement that last hours, days, or weeks. This persistence of aspects of habituation is termed long-term habituation.

Importantly, the aforementioned characteristics of habituation were observed and collected through numerous studies on a variety of species; therefore, they do not imply particular theories or inferences. They could be considered, however, as a detailed definition of habituation.

Several scientists who have studied the process of habituation provide valuable information regarding the underlying mechanisms of habituation and associated processes, demonstrating at the same time its complexity Thompson (2009). It has been noted that the occurrence of habituation is determined and/or influenced by variations in interstimulus interval and by the organisms’ ability to generalize and discriminate between the presented stimuli. Additionally, spontaneous recovery is another process thought to influence habituation’s maintenance. All these concepts are further analyzed in the section “Interstimulus Interval” that follows.

Interstimulus Interval

The concept of interstimulus interval is frequently encountered within processes of nonassociative learning, specifically habituation and sensitization Petrinovich (1984). Interstimulus interval can be defined as the time interval between the end of one stimulus presentation and the onset of another stimulus presentation. Interstimulus interval experiments were extensive under the work of Davis (1970) on habituation of the acoustic-startle response in the rat. Generally, through Davis’s series of experimental studies, it was demonstrated that the length of interstimulus interval, as well as variability (regularity), determines habituation in animals. The author compared the responsiveness of two groups of rats to a 50-ms, 120-db tone of 4000 Hz during pretest, training, and posttest periods. During both the pretest and the posttest periods, both groups of subjects received 300 tone exposures at intervals of 2, 4, 8, and 16 s, the intervals being scheduled in an irregular order. During the training period, both groups received 1000 tone exposures; however, the interval between stimuli was 16 s in one group and 2 s in the other group. Among other findings, greater reduction in responsiveness was observed in the group who received stimulation every 2 s.

In the second experiment, startle responsiveness was lower following training with regular as opposed to variable interstimulus intervals. Simply put when interstimulus interval is longer and constant, habituation is greater. Also Davis (1970) reported a quite an interesting finding; when rats were tested at 1 min or 24 h later with a variety of interstimulus intervals, habituation was greater for the group that was trained on the 16 s interstimulus interval schedule suggesting, thus, that short- and long-term habituation processes may be distinguishable on the basis of the presentation and the intervals between stimuli. Specifically, it was demonstrated that short interstimulus intervals were involved in the progression of short-term habituation, while long interstimulus intervals were involved in the promotion of long-term habituation. Also, apart from the fact that high-frequency stimulation leads to more rapid response decrement, it results in faster spontaneous recovery as well Leaton (1976).

Similarly, Groves and Thompson (1970) noted that increased frequency should lead to increased habituation in the “S-R” pathway, but in the “state” pathway, it would lead to increased sensitization. All the aforementioned experiments considered together are indicative of the importance of interstimulus interval making it obvious that it can have a major effect on learning; it may delay or improve learning. Lastly, the organism’s ability to determine the interval and duration of sensory stimulation is central to sensory processing; therefore, impairments in that domain are likely to interfere with the process of learning.

Variations in the time between the presentations of one stimulus to the next have a determinant effect on the forms of nonassociative learning; habituation and sensitization and the occurrence of long- and short-term habituation are dependent upon the length of interstimulus intervals Leaton (1976). Further manipulation of interstimulus intervals will provide valuable information regarding disruptions in learning processes or even suggestions as to how to enhance learning.

Stimulus Generalization and Discrimination

The concepts of stimulus generalization and stimulus discrimination are encountered within the context of associative and nonassociative learning. Stimulus generalization refers to a set of stimuli sharing similar properties with the original stimulus that provoked a response. Stimulus discrimination is the ability of an organism to respond only to the original stimulus and not to other similar stimuli.

Both concepts are inherent mechanisms in the processes of associative and nonassociative learning, and for both processes to take place, it is essential that a stimulus model should be stored in memory in order for comparisons with new stimuli to take place.

To begin with, generalization occurs when an organism produces the same response to different stimuli. Stimuli who exhibit analogous properties to the stimulus that was originally presented and provoked habituation, are more likely to provoke a similar response, that is habituation. There could be variations in terms of the level of pitch, brightness, loudness, and so on; however, if these variations deviate significantly from the properties of the original stimulus, generalization will not occur; hence, it is more likely that habituation will not occur either Teyler, Chiaia, DiScenna, Roemer (1984). Stimulus generalization of habituation can only be determined when a second habituation series is done with the use of a novel stimulus. With a comparison of the rates of habituation between the original and the novel stimulus, the amount of generalization will be demonstrated. More rapid habituation in the second series would be indicative of generalization, whereas similar rates between the two series would be indicative of a lack of generalization Petrinovich and Widaman (1984).

On the other hand, if stimuli are rather dissimilar than similar, the opposite process of stimulus generalization, the so-called stimulus discrimination, will be activated. In stimulus discrimination, the organism shows the ability to differentiate between similar stimuli and only to respond to a specific stimulus; hence, the organism responds differently to the two stimuli. Stimulus discrimination is particularly important in the process of habituation, as it can be used to dismiss sensory adaptation and fatigue as an alternative explanation of the occurrence of habituation. Further, dishabituation is indicative of the ability to discriminate, therefore ending habituation Thompson & Spencer (1966). It is important to clarify, however, that dishabituation occurs due to repetitive stimulation of a completely irrelevant stimulus and should not be thought of as the same as stimulus discrimination. Finally, stimulus generalization is useful because it allows for learning to take place quickly in new situations that share similarities with past experiences and promotes the transfer of skills into similar situations thus saving time and effort. Stimulus discrimination offers assistance in a practical level as well.

Stimulus generalization and discrimination are crucial processes in learning and both are of paramount importance to adaptation. Clearly any organism that lacks such abilities would have minimal chances of survival. There are well-known experiments undergone within the concept of conditioning (Pavlov’s and Watson’s experiments) that illustrate the stimulus generalization and the stimulus discrimination concepts more elaborately.

Spontaneous Recovery

Spontaneous recovery refers to the recovery of a habituated response. When a sequence of stimulus presentations is interrupted, the object at hand will return to its earlier stage, the behavior will recover over time. In a series of experiments undergone by Rankin and Broster (1992) on the nematode Caenorhabditis elegans, mechanical stimuli were delivered at four interstimulus intervals (2, 10, 30, and 60 s) in order to investigate the effect of interstimulus intervals in the development and maintenance of habituation. Results indicated that recovery from habituation was dependent on some factors. One of these factors is the length of interstimulus intervals; it was observed that recovery from habituation was faster when short interstimulus intervals were applied rather than longer interstimulus intervals. That is, long-term habituation prevents recovery. Also, the rate of recovery varied according to which response level each subject exhibited on the habituation curve. The recovery of animals on the lowest response level appeared to be determined by interstimulus interval and not by the further addition of stimuli. Interstimulus interval recovery rates did not differ even though the number of stimuli the worms received was significantly bigger (60 vs. 10) in the second group. In short what was evident is that the frequency of stimulation during habituation training was the one to determine the rate of spontaneous recovery.

Moreover, Rankin et al. (2009) upon revisiting the characteristics of habituation, originally described by Thompson and Spencer (1966), revised a point concerning spontaneous recovery. It is described in the characteristics that when a sequence of stimulus presentations is interrupted, the object at hand will return to its earlier stage, the behavior will recover over time. Rankin et al. (2009) revised this characteristic by adding that sometimes the response recovers completely, but sometimes it recovers only partially depending on the time frame that recovery was examined.

Further, when stimulus presentations and spontaneous recoveries are given repeatedly, the phenomenon of potentiation of habituation is observed. Here, the decrement in response that follows spontaneous recovery (i.e., habituation) becomes gradually more rapid with each application of spontaneous recovery. Moreover, the process of spontaneous recovery can be disrupted with the presentation of a new, strong stimulus, i.e., sensitization.

Lastly, it is crucial to note the importance of spontaneous recovery; it is the second way, with stimulus discrimination being the first way, to distinguish sensory adaptation and fatigue from habituation. With regards to learning, this process demonstrates that even though a response might disappear, it does not necessarily mean that it has been withdrawn from memory and that it will never reoccur.

Experiments on the lowest living forms illustrate the phenomenon of spontaneous recovery and those indicate that spontaneous recovery is highly determined by the frequency of stimulus presentation. These experiments provided a special insight on the underlying processes of habituation.

Conclusion

Habituation is one of the simplest forms of nonassociative learning, it is found in all animal species, and it is a highly complex yet essential process of the evolution of learning. It has been demonstrated that underlying processes as interstimulus interval, stimulus generalization, and discrimination, and spontaneous recovery are interconnected and influence the occurrence and maintenance of habituation.

Cross-References