Habituation in normal and Down's syndrome fetuses.

The ability of ten normal and two Down's syndrome fetuses to habituate to a repeated auditory stimulus was assessed. The normal fetuses were assessed on two separate occasions during the final trimester of pregnancy. The number of trials to habituate and latency to respond were recorded. The results demonstrated that all normal fetuses exhibited a decrement in response to repeated presentations of the stimulus, a 250-Hz sine wave. This was the result of habituation and not fatigue since fetuses recovered responding upon presentation of a new (500 Hz) stimulus and habituated faster on re-presentation of the original stimulus. The performance of fetuses remained stable over the two testing periods. The response of the Down's syndrome fetuses was different to that of normal fetuses rarely overlapping indices of habituation exhibited by normal fetuses. The study concludes that habituation may be a powerful tool to examine the behavioural and sensory development of the fetus and may be of use in the antenatal assessment of the existence and severity of neural abnormality.     

Fetal habituation performance: Gestational age and sex effects

Habituation is the decrement in response to repeated stimulation. Fetal habituation performance may reflect the functioning of the central nervous system (CNS) prenatally. However, basic characteristics of the prenatal habituation phenomena remain unclear, such as the relationship with gestational age (GA) and fetal sex. The current study investigated the relationship between habituation performance and both fetal sex and advancing gestational age, by comparing habituation performance at 31 and 35 weeks GA within a sample of 74 singleton pregnancies, all with normal neonatal outcomes. A vibroacoustic stimulus was used to habituate the fetus and motor responses were monitored via ultrasound. The criterion for habituation was defined as no response to five consecutive stimulus presentations. Prenatal habituation performance was found to demonstrate a developmental trend, with an increased proportion of fetuses habituating with advancing gestational age and requiring fewer stimulus presentations to satisfy the habituation criterion. Fetal sex also appears to have a moderating influence on gestational changes in habituation performance. Hence, the ongoing maturation of the fetal CNS does appear to be reflected in fetal habituation performance, indicating the need to consider the composition of fetal samples in terms of both gestational age and sex. Variability in interfetal performance was found to be high and clinical applications remain speculative.     

Sex differences in fetal habituation

There is some evidence for sex differences in habituation in the human fetus, but it is unknown whether this is due to differences in central processing (habituation) or in more peripheral processes, sensory or motor, involved in the response. This study examined whether the sex of the fetus influenced auditory habituation at 33 weeks of gestation, and whether this was due to differences in habituation or in the sensory or motor components using a set of four experiments. The first experiment found that female fetuses required significantly fewer stimulus presentations to habituate than males. The second experiment revealed no difference in the spontaneous motor behaviour of male and female fetuses. The third experiment examined auditory intensity thresholds for the stimuli used to habituate the fetus. No differences in thresholds were found between males and females, although there was inter-individual variability in thresholds. A final experiment, using stimuli individualized for that particular fetus' auditory intensity threshold, found that female fetuses habituated faster than males. In combination, the studies reveal that habituation in the human fetus is affected by sex and this is due to a difference in central 'information processing' of the stimuli rather than peripheral aspects of the response. It is argued that male and female fetuses present different neurobehavioural developmental trajectories, with females more advanced at 33 weeks than males. This study suggests that research examining prenatal behaviour should consider the factor of fetal sex. This may be particularly pertinent where there is an intention to use the results diagnostically.     

Habituation in the rat fetus.

Rat fetuses exhibit motor and cardiac responses to chemosensory stimulation on Days 20 and 21 of gestation. The first experiment demonstrated that fetuses exhibit an increase in overall motor activity and decrease in heartrate in response to an initial intraoral infusion of a lemon solution. After a series of nine exposures, however, fetuses no longer exhibit motor or cardiac responses to lemon infusion, suggesting the existence of a habituation-like process. Responsiveness recovers spontaneously following a 3- to 9-min period without stimulation. In a second experiment, a dishabituation treatment was administered to distinguish habituation, which is a centrally mediated decrement in response, from effector fatigue, sensory adaptation, and other peripheral mechanisms that can result in reduced responsiveness. A single infusion of mint following a series of nine lemon exposures was effective in reinstating fetal motor responses to lemon on both Days 20 and 21, but reinstated cardiac responses only on Day 21. Rat fetuses habituate to repeated chemosensory stimulation, suggesting the utility of the habituation paradigm in measuring CNS development during the perinatal period.     

Habituation in the rat fetus

Rat fetuses exhibit motor and cardiac responses to chemosensory stimulation on Days 20 and 21 of gestation. The first experiment demonstrated that fetuses exhibit an increase in overall motor activity and decrease in heartrate in response to an initial intraoral infusion of a lemon solution. After a series of nine exposures, however, fetuses no longer exhibit motor or cardiac responses to lemon infusion, suggesting the existence of a habituation-like process. Responsiveness recovers spontaneously following a 3-to 9-min period without stimulation. In a second experiment, a dishabituation treatment was administered to distinguish habituation, which is a centrally mediated decrement in response, from effector fatigue, sensory adaptation, and other peripheral mechanisms that can result in reduced responsiveness. A single infusion of mint following a series of nine lemon exposures was effective in reinstating fetal motor responses to lemon on both Days 20 and 21, but reinstated cardiac responses only on Day 21. Rat fetuses habituate to repeated chemosensory stimulation, suggesting the utility of the habituation paradigm in measuring CNS development during the perinatal period.     

Developmental change in fetal response to repeated low-intensity sound

The aim of this study was to investigate developmental changes in heart rate response to repeated low-intensity (85 dB) sound stimulation in fetuses between 32 and 37 weeks of gestation. We measured amplitude changes in heart rate as our index of fetal response. At 35 to 37 weeks of gestation, the majority of fetuses showed a deceleratory response at the first trial. Amplitude decreased with further trials using the same stimulus before recovering when exposed to another type of stimulation. In contrast, responses in fetuses at 32 to 34 weeks of gestation were variable across trials and there was no recovery with exposure to another type of stimulation. Our results suggest that fetal habituation of cardiac response changes with developmental age.     

Elicitation and Inhibition of Competitive Fighting in Food Deprived Mice

Habituation as an index of the intrasensory and intersensory integration of form was investigated in nine-year-old children. In Habituation Period One, Ss were habituated to either a visual or a haptic 14″-perimeter standard stimulus. During Habituation Period Two, groups were subdivided and presented with one of the following stimuli: (a) 14″ visual, (b) 16″ visual, (c) 14″ haptic, or (d) 16″ haptic. The dependent variables were GSR frequency and amplitude, visual fixation time, and touching time. Subjects required more trials to habituate to the different stimulus presented in Habituation Period Two than Ss who received repeated presentations of the same stimulus. GSR frequency and amplitude habituated more consistently than did fixation and touching response measures. The results supported the use of the habituation paradigm for the study of intersensory and intrasensory integration, as well as providing support for extending Sokolov's theory to intersensory functions.     

Auditory habituation in the fetus and neonate: an fMEG study

Habituation – the most basic form of learning – is used to evaluate central nervous system (CNS) maturation and to detect abnormalities in fetal brain development. In the current study, habituation, stimulus specificity and dishabituation of auditory evoked responses were measured in fetuses and newborns using fetal magnetoencephalography (fMEG). An auditory habituation paradigm consisting of 100 trains of five 500 Hz tones, one 750 Hz tone (dishabituator) and two more 500 Hz tones, respectively, were presented to 41 fetuses (gestational age 30–39 weeks) and 22 newborns or babies (age 6–89 days). A response decrement between the first and fifth tones (habituation), an increment between the fifth tone and the dishabituator (stimulus specificity) and an increment between the fifth (last tone before the dishabituator) and seventh tones (first tone after the dishabituator) (dishabituation) were expected. Fetuses showed weak responses to the first tone. However, a significant response decrement between the second and fifth tones (habituation) and a significant increment between the fifth tone and the dishabituator (stimulus specificity) were found. No significant difference was found for dishabituation nor was a developmental trend found at the group level. From the neonatal data, significant values for stimulus specificity were found. Sensory fatigue or adaptation was ruled out as a reason for the response decrement due to the strong reactions to the dishabituator. Taken together, the current study used fMEG to directly show fetal habituation and provides evidence of fetal learning in the last trimester of pregnancy.     

Habituation and the human evoked potential

Habituation of human scalp-recorded cerebral evoked potentials was studied in response to auditory and visual repetitive stimuli of different intensities. Changes in magnitudes of evoked potentials with stimulus repetition were examined according to the parametric characteristics of habituation, generalization, and dishabituation. In addition, tests of the predictions of two theories of habituation were made regarding the degree and direction of intensity generalization of habituation. Both auditory and visual evoked potentials exhibited decrements in response magnitudes across the repetitive stimuli consistent with the parametric criteria of habituation. Early evoked potential peak components showed a pattern of intensity generalization of habituation consistent with the predictions of the dual-process theory of habituation. Intensity generalization of late evoked potential peak components occurred in a manner more consistent with the predictions of the stimulus comparator theory of habituation. These results provide further evidence that evoked potentials can be used as electrophysiological indexes of plasticity in humans.     

Offspring of anxious parents: reactivity, habituation, and anxiety-proneness

Reactivity and habituation patterns were examined in the offspring of anxious and non-anxious parents. Although no differences emerged for magnitude of response to either fear-relevant visual or auditory stimuli, offspring of anxious parents displayed significantly more electrodermal activity during resting baseline and during the inter-trial intervals of these stimulus presentations. Differences also were observed for the number of children per group achieving habituation to the fear-relevant visual and auditory stimuli, where offspring of anxious parents were less likely to habituate to either stimuli. The same pattern of group differences emerged after excluding children diagnosed with an anxiety disorder, indicating that even offspring of anxious parents who did not have an anxiety disorder differ from offspring of normal controls with respect to their pattern of psychophysiological reactivity. It is hypothesized that these features might serve as an indication of anxiety proneness and risk for the development of anxiety disorders.     

Habituation and sensitization of acoustic startle: opposite influences of dopamine D1 and D2-family receptors

The startle response evoked by repeated presentation of a loud acoustic stimulus is regulated by the independent processes of sensitization and habituation. While schizophrenia is associated with information processing impairments, there is conflicting evidence regarding the existence of habituation deficits in schizophrenic patients. Recent clinical evidence, however, indicates that patients with schizophrenia display exaggerated startle sensitization and diminished habituation. Given the linkage between dopaminergic abnormalities and schizophrenia, the goal of the present investigation was to examine the effect of deleting D₁ and D₂-like dopamine receptors on sensitization and habituation of the acoustic startle reflex in mice. For these experiments, the acoustic startle reflex was assessed in dopamine D₁, D₂, and D₃ receptor wild-type (WT) and knockout (KO) mice on a C57BL/6J background, using a methodology that can measure both sensitization and habituation. Mice lacking the D₁ receptor gene displayed enhanced sensitization, along with a decrease in the amount of habituation that occurs in response to repetitive presentations of a startling stimulus. Conversely, the loss of the dopamine D₂ or D₃ receptor gene produced a sensitization deficit and a significant increase in habituation. The behavioral phenotype exhibited by D₁ receptor KO mice is clearly distinct from that of the D₂ and D₃ receptor KO mice. The findings in D₁ receptor KO mice are reminiscent of the abnormalities observed in schizophrenic patients tested in comparable startle paradigms, and indicate that D₁ agonists may possess therapeutic efficacy against the information processing deficits associated with schizophrenia.     

Habituation, response to novelty, and dishabituation in human infants: tests of a dual-process theory of visual attention

Two experiments were conducted to test a dual-process theory of infants' performance on visual habituation-dishabituation tasks. The findings demonstrate that (a) infant habituation functions are often nonmonotonic, with fixation increasing before the eventual response waning; (b) this initial increment in responding is related to stimulus "complexity"; (c) response to novelty is enhanced by increasing the "complexity" of the novelty-test stimulus; and (d) dishabituation, followed by decay, occurs for familiarized patterns when retested after the introduction of a "complex" stimulus, but not after introduction of a "simple" stimulus. Following P. Groves and R. Thompson (1970, Psychological Review, 77, 419-450) we propose that infant visual attention to repeated presentations of a stimulus involves two processes, habituation and sensitization.     

Heart-rate and electrodermal orienting responses to visual stimuli differing in complexity

Orienting response (OR) theory predicts that amount of information in the stimulus, or stimulus complexity, should be an important determinant of OR elicitation and habituation, more intense and more slowly habituating ORs being expected to complex than to simple stimuli. This prediction was tested in an experiment where subjects were exposed to simple and complex visual stimuli in randomized order, while heart-rate and skin conductance were measured. Complex stimuli evoked a more pronounced deceleratory heartrate response than did simple stimuli. However, the two conditions did not differ in rate of habituation of this response. For skin conductance responses, on the other hand, the complex stimulus took more trials than the simple stimulus to reach habituation, whereas the two conditions did not differ in response magnitude. Thus, the hypothesis of more intense orienting to complex stimuli was supported by the heart-rate data, and that of slower habituation to complex stimuli, of the skin conductance data.     

Touch and vision in normal and Down's syndrome babies

Two experiments are reported with young Down's syndrome and normal children matched for mental age, sex, and social class. In one, Down's syndrome children performed at chance level on two tactual--visual cross-modal tasks, and only the oldest succeeded with one of two visual--visual within-modal tasks. The modal children performed at above chance level on the visual--visual tasks, and on the tactual--visual tasks the oldest succeeded on two and the youngest on one of the tasks. These results suggest that Down's syndrome children may have some sort of difficulty involving tactual perception. The second experiment examined the effect of touch on visual behaviour. Down's syndrome children and their matched controls looked at pairs of shapes which sometimes could be touched and sometimes could not. In the former condition the Down's syndrome children touched less, and looking and touching was less coordinated than that of normal children. However, both groups made fewer but longer looks when they could touch the shapes. In the light of these results the role of tactual perception in Down's syndrome children is discussed.     

Generalization of Habituation and Intrinsic Sensitization in the Leech

Using the shortening reflex of the medicinal leech Hirudo medicinalis we examined stimulus generalization of habituation learning. Preparations received mechanosensory stimulus at two positions on the leech body wall, one site used to carry out habituation training and a second novel site to test for generalization of habituation. After training, the specific mechanosensory neurons activated by each stimulus were assessed using intracellular recordings. As expected, the closer the two sites were to each other, the greater the degree of generalization of habituation at the novel site and the more sensory cells were shared. However, a form of behavioral facilitation was observed at the trained site that resembled behavioral sensitization, but differed from the standard sensitization process in several respects. (1) Facilitation was induced by stimulation of the novel site before habituation training at the trained site, although the stimulus intensity at the novel site was equivalent to the training stimuli and was not the strong, noxious stimuli that normally induce sensitization. (2) The magnitude of the facilitating effect was proportional to the proximity of the novel and trained stimulation sites. (3) Although behavior at the trained site was facilitated, behavior at the novel site was habituated, indicating that the induced behavioral facilitation did not generalize throughout the animal, as normally occurs during sensitization, but was limited to a single stimulus–response pathway.     

Habituation to repeated stress: get used to it

Habituation, as described in the landmark paper by Thompson et al. [Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review, 73(1), 16–43], is a form of simple, nonassociative learning in which the magnitude of the response to a specific stimulus decreases with repeated exposure to that stimulus. A variety of neuronal and behavioral responses have been shown to be subject to habituation based on the criteria presented in that paper. It has been known for several decades that the magnitude of hypothalamic–pituitary–adrenal (HPA) activation occurring in response to a stressor declines with repeated exposure to that same stressor. For some time this decline has been referred to as “habituation” in the stress neurobiology literature. However, how this usage compares to the definition proposed by Thompson and Spencer has not been systematically addressed. For this special issue, we review the stress neurobiology literature and examine the support available for considering declines in HPA response to repeated stress to be response habituation in the sense defined by Thompson and Spencer. We conclude that habituation of HPA activity meets many, but not all, important criteria for response habituation, supporting the use of this term within the context of repeated stress. However, we also propose that response habituation can, at best, only partially explain the phenomenon of HPA habituation, which also involves well-known negative feedback mechanisms, activation of broad stress-related neural circuitry and potentially more complex associative learning mechanisms.     

Locus of habituation in the human newborn

There is some controversy concerning the youngest age at which an infant will habituate to a visual stimulus or will prefer a novel to a familiar pattern. One suggestion has been that apparently successful reports of habituation and dishabituation in the newborn baby are attributable to retinal adaptation. This interpretation was tested in two experiments. In both experiments monocular conditions of viewing were used: newborns were habituated with one eye as the 'seeing' eye, and posthabituation novelty preferences investigated with the other eye. Significant preferences were found both for a novel colour (experiment 1) and for a novel shape (experiment 2), which implies that a retinal-adaptation model can be ruled out. It is suggested that the habituation effects and the subsequent novelty preferences found in the experiments are most reasonably interpreted as a function of memory formation, and evidence is presented for the storage of visual experience from birth. The results also demonstrate some form of binocular interaction in the newborn.     

Habituation in songbirds

Songbirds respond to initial playback of a recorded conspecific song in numerous ways, from changes in gene expression in the brain to changes in overt physical activity. When the same song is presented repeatedly, responses have been observed to habituate at multiple levels: molecular, cellular and organismal. Core criteria of habituation have been established at each level, although in no case have all the formal parameters been rigorously measured. At the level of overt behavior, classical field studies showed that territorial birds respond to the song of a potential challenger with a variety of behaviors, and many (but not all) of these behaviors decline with repeated stimulus presentation. More recent laboratory studies have defined analogous responses to song presentation in the zebra finch (Taeniopygia guttata), the dominant species in current molecular and neurobiological research and one that does not use song for territorial defense. Studies in the zebra finch have also demonstrated activation followed by habituation of responses measured at both electrophysiological and molecular (gene expression and signal transduction) levels. In all cases, habituation is specific for a very particular stimulus – an individual song presented in a particular context. There are strong correlations between habituation measurements made at these different levels, but some dissociations have also been observed, implying that molecular, electrophysiological and behavioral habituations are not equivalent manifestations of a single core process.