Exploring the mechanism of dishabituation

In this study we explored elicitation and habituation of the orienting reflex (OR) in the context of indifferent and significant stimuli, particularly aiming to clarify the mechanism driving dishabituation. An in-depth analysis of the mechanisms of electrodermal habituation and dishabituation was conducted, focusing on the role of state measures as determinants of the phasic response profile. Twenty-four young adult participants completed an auditory dishabituation task while electrodermal activity was recorded. Participants listened to a series of 10 innocuous tones of the same frequency (standards), followed by a deviant tone of a different frequency, and succeeded by 2-4 tones of the same frequency as the initial 10 stimuli. All stimuli had a random stimulus onset asynchrony of 5-7 s. Participants completed an indifferent condition in which there was no task in relation to the stimuli, and a significant condition where instruction was given to count the stimuli silently; order was counterbalanced between participants. As predicted, both skin conductance responses (SCRs) and skin conductance levels (SCLs) were larger for the significant than the indifferent condition. The initial phasic ORs were dependent on pre-stimulus arousal level, and there were significant decreases in both SCR and SCL over the first 10 standards in both conditions. Phasic response recovery was apparent to the deviant stimulus, and dishabituation to the following standard stimulus; both effects were enhanced in the significant condition. Sensitisation was apparent in SCL following the initial and deviant stimuli, but the extent of this was confounded with incomplete resolution of the preceding phasic OR in the significant condition. In the indifferent condition, dishabituation was independent of deviant-related sensitisation; this could not be tested in the significant condition. These findings suggest that dishabituation is not a process of sensitisation, but rather, a disruption of the habituation process.     

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.     

Habituation in children within a behavior suppression paradigm

Using an instrumental response suppression paradigm, Experiment 1 demonstrated habituation and long-term retention of habituation to a tone stimulus in third-grade children, but specificity of habituation was not obtained when a new tone stimulus was presented. In Experiment 2 first graders showed specificity of habituation to auditory stimuli on the response suppression measure whereas fifth graders did not. However, both age groups evidenced specificity when a skin conductance measure was employed. In addition, specificity of habituation was not affected by amount of training at either age level. Experiment 3 demonstrated specificity of habituation in fifth graders on the response suppression measure when a cross-modality stimulus change was introduced. Implications of these data for analyses of habituation and traditional learning are discussed.     

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.     

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.     

Effects of a violation of an expected increase or decrease in intensity on detection of change within an auditory pattern

An infrequent physical increase in the intensity of an auditory stimulus relative to an already loud frequently occurring “standard” is processed differently than an equally perceptible physical decrease in intensity. This may be because a physical increment results in increased activation in two different systems, a transient and a change detector system (signalling detection of an increase in transient energy and a change from the past, respectively). By contrast, a decrease in intensity results in increased activation in only the change detector system. The major question asked by the present study was whether a psychological (rather than a physical) increment would continue to be processed differently than a psychological decrement when both stimuli activated only the change detector system. Participants were presented with a sequence of 1000 Hz tones that followed a standard rule-based alternating high-low intensity pattern (LHLHLH). They were asked to watch a silent video and thus ignore the auditory stimuli. A rare “deviant” was created by repeating one of the stimuli (e.g., LHLHLLLH. The repetition of the high intensity stimulus thus acted as a relative, psychological increment compared to what the rule would have predicted (the low intensity); the repetition of the low intensity stimulus acted as a relative, psychological decrement compared to what the rule would have predicted (the high intensity). In different conditions, the intensity difference between the low and high intensity tones was either 3, 9 or 27 dB. A large MMN was elicited only when the separation between the low and high intensities was 27 dB. Importantly, this MMN peaked significantly earlier and its amplitude was significantly larger following presentation of the psychological increment. Thus, a deviant representing an increment in intensity relative to what would be predicted by the auditory past is processed differently than a deviant representing a decrement, even when activation of the transient detector system is controlled. The psychological increment did not however elicit a later positivity, the P3a, often thought to reflect the interruption of the central executive and a forced switching of attention.     

Pure-tone perception and ear advantages in dichotic listening

A same-different matching task was used to investigate how subjects perceived a dichotic pair of pure tones. Pairs of stimulus tones in four frequency ranges (center frequencies of 400–1,700 Hz), with separations between 40 and 400 Hzt were tested. Five types of test tones were matched to the stimulus pair: the stimulus pair presented again (control) or crossed over (same tones, different ears), the geometric mean of the two tones, or a binaural tone of the low or high tone of the pair. In the lowest frequency range and the highest with maximum separation, the crossed-over test tones were perceived as different from the same stimulus tones. A bias for perceiving the higher tone of a pair was evident in the frequency ranges with separations of 40-200 Hz. In the lowest frequency range, the bias was for perceiving the higher tone in the right ear. This restricted ear advantage in the perception of pure tones was not significantly related to the right-ear advantage in dichotic word monitoring.     

Effects of a violation of an expected increase or decrease in intensity on detection of change within an auditory pattern

An infrequent physical increase in the intensity of an auditory stimulus relative to an already loud frequently occurring “standard” is processed differently than an equally perceptible physical decrease in intensity. This may be because a physical increment results in increased activation in two different systems, a transient and a change detector system (signalling detection of an increase in transient energy and a change from the past, respectively). By contrast, a decrease in intensity results in increased activation in only the change detector system. The major question asked by the present study was whether a psychological (rather than a physical) increment would continue to be processed differently than a psychological decrement when both stimuli activated only the change detector system. Participants were presented with a sequence of 1000 Hz tones that followed a standard rule-based alternating high-low intensity pattern (LHLHLH). They were asked to watch a silent video and thus ignore the auditory stimuli. A rare “deviant” was created by repeating one of the stimuli (e.g., LHLHLLLH. The repetition of the high intensity stimulus thus acted as a relative, psychological increment compared to what the rule would have predicted (the low intensity); the repetition of the low intensity stimulus acted as a relative, psychological decrement compared to what the rule would have predicted (the high intensity). In different conditions, the intensity difference between the low and high intensity tones was either 3, 9 or 27 dB. A large MMN was elicited only when the separation between the low and high intensities was 27 dB. Importantly, this MMN peaked significantly earlier and its amplitude was significantly larger following presentation of the psychological increment. Thus, a deviant representing an increment in intensity relative to what would be predicted by the auditory past is processed differently than a deviant representing a decrement, even when activation of the transient detector system is controlled. The psychological increment did not however elicit a later positivity, the P3a, often thought to reflect the interruption of the central executive and a forced switching of attention.     

Habituation and dishabituation of the electrodermal orienting reflex in relation to extraversion and neuroticism

Orienting reflex (OR) habituation and dishabituation may be influenced by individual difference variables, including Eysenck's Extraversion (E) and Neuroticism (N) dimensions. Ninety subjects formed nine groups based on the crossover of high, medium, and low E and N. Each subject received, at each of two auditory stimulus intensities, two blocks of tone presentations. The last standard stimulus trial was followed by a novel stimulus and four repetitions of the standard stimulus. Using square root SCR, extraverts showed smaller initial response amplitudes than introverts at the low intensity of stimulation, while the reverse was true at high intensity. E and N were unrelated to SCR habituation rate. However, extraverts showed no dishabituation, while introverts did dishabituate.     

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.     

Extraversion and neuroticism in orienting reflex dishabituation

The present study examined the effects of extraversion (E) and neuroticism (N) as individual difference dimensions and of stimulus intensity on electrodermal orienting response habituation, test response, and dishabituation. Subjects were 162 college students selected from a screening sample of 860 as representing extreme groups of high, medium, and low E crossing with high, medium, and low N. Subjects in all nine resulting groups were habituated to criterion on auditory stimuli of 60, 80, and 100 db. A novel (test) stimulus and a dishabituating standard stimulus followed criteron habituation at each intensity. Results indicated that response amplitude for initial, test, and dishabituation responses was a direct function and that habituation rate (trials-to-criterion) was an inverse function of stimulus intensity. Extraverts habituated more rapidly than introverts at high intensity and gave smaller test and dishabituation responses. Some results differed when regression coefficients defined habituation rate and when first stimulus intensities alone were examined. Correlations among initial, test, and dishabituation responses and between each of these and the two measures of habituation rate are also reported. Results were interpreted as partially supportive of Eysenck's theory.     

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.     

Influence of dorsal hippocampal lesions and MMP inhibitors on spontaneous recovery following a habituation/classical conditioning head–shake task

The present investigation combined a classical conditioning paradigm with a head–shake response (HSR) habituation task in order to evaluate the importance of dorsal hippocampal neural plasticity to spontaneous recovery. In the first experiment animals exhibited rapid HSR habituation (air stimulus to the ear) and an 85% level of spontaneous recovery following a 24 h inter-session interval. The addition of a brief tone prior to the air stimulus produced a similar pattern of habituation during the first session, but the level of spontaneous recovery was reduced (44%) during Session II. In a second experiment dorsal hippocampal lesioned rats placed on this tone/HSR paradigm responded with an 87% level of spontaneous recovery during Session II; while neocortex lesioned control rats indicated significantly reduced levels of spontaneous recovery (55%). In a third experiment bilateral injections of a general MMP inhibitor, FN-439, into the dorsal hippocampus resulted in high levels of spontaneous recovery (81%); while control rats injected with artificial cerebrospinal fluid displayed a significant attenuation of spontaneous recovery (45%). Finally, animals bilaterally injected with a specific MMP-3 inhibitor into the dorsal hippocampus indicated very similar results to those obtained following FN-439 injection. These findings indicate that animals prepared with dorsal hippocampal lesions, or injections with an MMP inhibitor, revealed an impaired association between the tone and air stimulus thus maximum spontaneous recovery was present 24 h later. Thus, it appears that the dorsal hippocampus influences habituation by conserving responses and reducing spontaneous recovery when a temporally contingent signaling cue is present.     

Binocular disparity as a discriminable stimulus parameter for young infants

The ability of 8-week-old infants to discriminate between projected stereograms with and without retinal disparity was tested with an habituation-dishabituation paradigm. Infants in two experimental groups received six trials with either the disparity or the nondisparity stimulus and then were given two trials with the other display. Infants in two control groups viewed the same stimulus, either disparity or nondisparity, on all eight trials. There was a suggestion of some response decrement over time in both cardiac deceleration and sucking suppression, although this effect was not significant. However, significant increment was obtained on the dishabituation trials for heart rate in the group that was shifted from the nondisparity to the disparity stimulus. These results were interpreted as indicating that the infants could discriminate between stimuli when the only difference between them was binocular disparity.     

Habituation and dishabituation during object play in kennel-housed dogs

Domestic dogs are reported to show intense but transient neophilia towards novel objects. Here, we examine habituation and dishabituation to manipulable objects by kennel-housed dogs. Labrador retrievers (N?=?16) were repeatedly presented with one toy for successive 30-s periods until interaction ceased. At this point (habituation), a different toy was presented that contrasted with the first in both colour and odour (since the dog’s saliva would have accumulated on the first), colour alone, or odour alone. No effect of the type of contrast was detected in the number of presentations to habituation, the difference in duration of interaction between the first presentation of the first toy and the presentation of the second toy (recovery), or the duration of interaction with the second toy (dishabituation). Varying the time interval between successive presentations of the first toy up to habituation between 10?s and 10?min had no effect on the number of presentations to habituation, nor did it alter the extent of dishabituation. Varying the delay from habituation to presentation of the second toy, between 10?s and 15?min, affected neither the recovery nor the dishabituation. Overall, the study indicates that loss of interest in the object during object-orientated play in this species is due to habituation to the overall stimulus properties of the toy rather than to any single sensory modality and is also atypical in its insensitivity to the interval between presentations.     

Temporal pattern and spectral complexity as stimulus parameters for eliciting a cardiac orienting reflex in human fetuses

The purpose of this study was to determine whether temporal pattern and/or spectral complexity were important stimulus parameters for eliciting a cardiac orienting reflex (OR) in low-risk human fetuses. Each of 28 term fetuses was exposed to four sounds formed from the four different combinations of temporal pattern (pulsed, continuous) and spectral complexity (sine wave, /a/). The fetal cardiac electrical signal was captured transabdominally at a rate of 1024 Hz, and fetal R-waves were extracted by using adaptive signal-processing techniques. We found that pulsed sounds elicited a significantly greater decrease in heart rate (HR) than did continuous sounds. However, the HR response was relatively unaffected by spectral complexity. For the pure tone and the phoneme used in this study, our results indicate that temporal characteristics were more effective at eliciting a cardiac OR in human fetuses than was spectral complexity.     

Measuring human aversion to sound without verbal descriptors

High school students tapped rapidly on a telegraph key to reduce the intensity of a continuous acoustic stimulus presented through earphones. Failure to respond resulted in an intensity increase of 1 dB every 4 sec. In Experiment 1, a group of 19 students responded to three pure tones (125, 1,000, and 8,000 Hz) and a white noise. The different asymptotic levels observed after 4 min were taken as a measure of equal aversion levels for the stimuli. In Experiment 2, the effect of the starting intensity level (45, 70, and 90 dB SPL) was determined for a 1,000-Hz tone. Differences in the asymptotic intensity levels observed after 6 rain were not significant. In Experiment 3, no significant effect was found upon varying the number of responses required to produce a 1-dB intensity decrement in a 1,000-Hz tone. Together, the experiments demonstrated the feasibility of determining equal-aversion levels for sounds.     

A behavioral and genetic dissection of two forms of olfactory plasticity in Caenorhabditis elegans: adaptation and habituation

Continuous presentation of an olfactory stimulus causes a decrement of the chemotaxis response in the nematode Caenorhabditis elegans. However, the differences between the learning process of habituation (a readily reversible decrease in behavioral response) and other types of olfactory plasticity such as adaptation (a decrement in response due to sensory fatigue, which cannot be dishabituated) have not been addressed. The volatile odorant diacetyl (DA) was used within a single paradigm to assess the distinct processes of olfactory adaptation and habituation. Preexposing and testing worms to 100% DA vapors caused a chemotaxis decrement that was not reversible despite the presentation of potentially dishabituating stimuli. This DA adaptation was abolished in worms with an odr-10 mutation (encoding a high-affinity DA receptor on the AWA neuron), even though naive chemotaxis remained unaffected. Conversely, DA adaptation remained intact in odr-1 mutants (defective in AWC neuron-mediated olfactory behavior), even though naive chemotaxis to DA decreased. Surprisingly, exposure to vapors of intermediate concentrations of DA (0.01% and 25%) did not cause worms to exhibit any response decrement. In contrast to preexposure to high DA concentrations, preexposure to low DA concentrations (0.001%) produced habituation of the chemotaxis response (a dishabituating stimulus could reverse the response decrement back to baseline levels). The distinct behavioral effects produced by DA preexposure highlight a concentration-dependent dissociation between two decremental olfactory processes: adaptation at high DA concentrations versus habituation at low DA concentrations.     

Dishabituation in Aplysia can involve either reversal of habituation or superimposed sensitization

Dishabituation has been thought to be due either to reversal of the process of habituation or to a second process equivalent to sensitization superimposed on habituation. One way to address this question is by testing whether dishabituation and sensitization can be dissociated. Previous studies using this approach in Aplysia have come to different conclusions about the nature of dishabituation, perhaps because those studies differed in many respects, including (1) whether they also observed transient behavioral inhibition, and (2) whether they used test stimuli that activated the LE siphon sensory neurons or as yet unidentified sensory neurons. To attempt to resolve the apparent contradictions between the previous studies, we have explored the importance of these two factors by performing a parametric study of dishabituation and sensitization of gill withdrawal in a simplified preparation that does not exhibit transient behavioral inhibition, using two different test stimuli that are known to activate the LE (Touch) or unidentified (Not Touch) sensory neurons. We find that dishabituation and sensitization in this preparation have similar time courses and generally similar functions of shock intensity. However, under one condition, with the Not Touch stimulus 2.5 min after the shock, dishabituation has a reverse effect of shock intensity. Additional analyses suggest that dishabituation with the Not Touch stimulus 2.5 min after the shock is due to reversal of habituation, whereas 12.5 min after the shock, dishabituation is due to superimposed sensitization. These results thus suggest that dishabituation may involve either process in the same preparation, and begin to define the conditions that favor one or the other.