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.     

Prenatal expression of species-typical action patterns in the rat fetus (Rattus norvegicus)

We investigated sensory and behavioral responsiveness of the rat fetus. On Days 19, 20, or 21 of gestation, rat fetuses received intraoral infusions of a biologically important stimulus, milk, or a novel chemical stimulus, lemon. Using a technique to directly observe behavior in utero, we found that rat fetuses discriminate between intraoral infusions of milk and lemon, exhibiting different levels and patterns of overall activity after infusion. Milk was found to evoke a low magnitude, delayed increase in overall fetal activity from Day 19 through Day 21, whereas lemon evoked a high-magnitude, spiked pattern of activity that diminished from Day 19 to Day 21. Late in gestation these two stimuli elicited species-typical action patterns. Milk infusions elicited a stretch response much like the one shown by pups at the nipple; lemon infusions elicited face wiping typical of older pups and adults exposed to aversive gustatory stimuli.     

Association between chemosensory stimuli and cesarean delivery in rat fetuses: neonatal presentation of similar stimuli increases motor activity

Recent studies conducted in this laboratory indicated that prenatal chemosensory stimulation followed by cesarean delivery strongly affected postnatal responsiveness to odors derived from the administered substances. The present experiments were performed in order to examine if an associative process was responsible for such effects. In Experiment 1 rat fetuses during Gestational Day 21 were exposed to a tenuous alcohol solution or to a lemon-containing solution either 40 or 10 min prior to cesarean delivery. All subjects were subsequently tested in terms of changes in neonatal motor activity when confronted with the odor of alcohol or lemon. Rats experiencing prenatal cues 10 min prior to delivery exhibited higher and differential responsiveness to the smell of these cues when compared to those experiencing similar solutions 40 min prior to delivery. In Experiment 2 each fetus sequentially experienced both cues. Subsequent tests confirmed that the delay between prenatal sensory experience and birth induction was critical in terms of significantly affecting olfactory-mediated motor responses. The results suggest that consequences related with cesarean delivery act as an unconditioned stimulus capable of being associated with orosensory cues present in the amniotic fluid.     

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.     

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.     

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.     

Effects of voluntary wheel running on heart rate, body temperature, and locomotor activity in response to acute and repeated stressor exposures in rats

Stress often negatively impacts physical and mental health but it has been suggested that voluntary physical activity may benefit health by reducing some of the effects of stress. The present experiments tested whether voluntary exercise can reduce heart rate, core body temperature and locomotor activity responses to acute (novelty or loud noise) or repeated stress (loud noise). After 6 weeks of running-wheel access, rats exposed to a novel environment had reduced heart rate, core body temperature, and locomotor activity responses compared to rats housed under sedentary conditions. In contrast, none of these measures were different between exercised and sedentary rats following acute 30-min noise exposures, at either 85 or 98 dB. Following 10 weeks of running-wheel access, both groups displayed significant habituation of all these responses to 10 consecutive daily 30-min presentations of 98 dB noise stress. However, the extent of habituation of all three responses was significantly enhanced in exercised compared to sedentary animals on the last exposure to noise. These results suggest that in physically active animals, under some conditions, acute responses to stress exposure may be reduced, and response habituation to repeated stress may be enhanced, which ultimately may reduce the negative and cumulative impact of stress.     

An exploratory investigation of coffee and lemon scents and odor identification

Fragrance sellers often provide coffee beans to their customers as a "nasal palate cleanser," to reduce the effects of olfactory adaptation and habituation. To test this idea, college students smelled three fragrances multiple times, rating odors each time. After completing nine trials, participants sniffed coffee beans, lemon slices, or plain air. Participants then indicated which of four presented fragrances had not been previously smelled; Coffee beans did not yield better performance than lemon slices or air.     

Extraversion and the orienting reaction habituation rate to visual stimuli

Eysenck's (1967) proposal that introversion is characterized by increased levels of activity in the cortico-reticular loop was treated in a series of experiments which compared high, middle, and low extraversion groups on the basis of OR habituation rate to visual stimulation. Generally, introverts were observed to have longer OR habituation rates to chromatic and word stimulation than extraverts as evidenced by cardiac, electrodermal, and vasomotor indices of habituation rate, a result which endorses Eysenck's hypothesis. Results are also discussed from the standpoint of individual differences in autonomic response.     

Habituation of the proleg withdrawal reflex in Manduca sexta does not involve changes in motoneuron properties or depression at the sensorimotor synapse

Larvae of the hawkmoth, Manduca sexta, exhibit a defensive proleg withdrawal reflex in which deflection of mechanosensory hairs on the proleg tip (the planta) evokes retraction of the proleg. A previous behavioral study showed that this reflex habituates in response to repeated planta hair deflection and exhibits several other defining features of habituation. In a semi-intact preparation consisting of a proleg and its associated segmental ganglion, repeated deflection of a planta hair or electrical stimulation of its sensory neuron causes a neural correlate of habituation, manifested as a decrease in the number of action potentials evoked in the proleg motor nerve. Monosynaptic connections from planta hair sensory neurons to the principal planta retractor motoneuron exhibit several forms of activity-dependent plasticity. In the present study we recorded intracellularly from this motoneuron during repetitive electrical stimulation of a planta hair sensory neuron. The number of action potentials evoked in the motoneuron decreased significantly, representing a neural correlate of habituation. The motoneuron's resting membrane potential, input resistance. and spike threshold measured before and after repetitive stimulation did not differ between the stimulated group and a control group. Furthermore, the amplitude of the monosynaptic excitatory postsynaptic potential, as well as the magnitude of paired-pulse facilitation, evoked in the motoneuron by the sensory neuron did not change after repetitive stimulation. These results suggest that depression at the sensorimotor synapse does not contribute to reflex habituation. Rather, other mechanisms in the ganglion of the stimulated segment, such as changes in polysynaptic reflex pathways, appear to be responsible.     

Interactions between perinatal and neonatal associative learning defined by contiguous olfactory and tactile stimulation

Tactile stimulation of the neonate, as performed by the mother during and after delivery, has been described as an effective unconditioned stimulus during early ontogeny (Leon, 1987; Ronca & Alberts, 1994). The present experiments examined the interaction between perinatal and neonatal learning determined by the explicit association between alcohol odor and vigorous body stimulation of the perinatal organism. In Experiment 1, rat fetuses were exposed to either alcohol or saline 10 min prior to cesarean delivery. The alcohol administration procedure here employed was sufficient to provide sensory contamination of the amniotic fluid but avoid fetal alcohol intoxication. Pups in the two prenatal treatments later experienced the smell of alcohol, tactile stimulation, or both stimuli explicitly paired or unpaired. Other postnatal groups were composed of pups that had no explicit experience with either experimental stimulus. Pups subjected to alcohol odor in utero displayed more overall motor activity in response to that odor than saline controls. The increased motor responses were further potentiated in pups that experienced additional postnatal alcohol odor paired with tactile stimulation. In Experiment 2, pups were exposed to alcohol in the amniotic fluid 10 or 30 min prior to birth. As previously demonstrated the memory acquired in utero appears highly dependent upon contingency between exposure to this particular scent and delivery procedures. Pups in both prenatal treatment groups were then exposed to alcohol odor paired or unpaired with tactile stimulation. Some control animals received no further experience with either stimuli. Those pups exposed to alcohol odor paired with tactile stimulation both pre- and postnatally later showed maximum motor activity elicited by the odor of alcohol. The results support the notion of fetal associative learning comprising alcohol's chemosensory cues and behaviorally activating stimuli. Furthermore, the conditioned response under analysis is potentiated whenever neonates are reexposed to contingent presentations of the elements that defined the original associative memory.     

Cardiac and behavioral responses to rocking stimulations in one- and three-month-old infants

Cardiac and behavioral reactions to lateral rocking stimulations were analysed at two different ages (1 and 3 months) and at two speeds of motion for the younger infants. Sixteen 1- and 3-mo.-old infants received 12 10-sec. trials of four complete cycles of vestibulokinesthetic stimulation (rapid rocking) and another group of 10 1-mo.-olds received one complete cycle in the same time period (slow rocking) provided by a motorized cradle. Stimulations were given when infants were in an alert state. Rapid and slow rocking induced similar cardiac responses in younger infants; these responses varied according to the type of motor reaction observed at stimulus onset. Cardiac acceleration was shown with motor activation and cardiac deceleration with motor quieting. In 3-mo.-olds, cardiac deceleration appeared with both types of motor reaction. A strong link between cardiac and behavioral responses in younger infants may prevent the occurrence of the usual simple cardiac index of orienting (heart-rate deceleration). In older infants, cardiac deceleration to rocking stimulation appeared even when it produced concomitant behavioral arousal. Vestibulokinesthetic stimulation is interpreted as having an important homeostatic effect on the young organism.     

A sensory basis for the lateral difference in the newborn infant's response to somesthetic stimulation

To determine whether lateral differences in the newborn infant's response to somesthetic stimulation are a consequence of lateral differences in sensitivity or whether they are the result of lateral differences in motor tendencies, cardiac response to stimulation of the left and right perioral region was examined. Cardiac acceleration occurred significantly more frequently to stimulation of the right than to stimulation of the left. Ipsilateral head turning also occurred more reliably to stimulation of the infant's right side than to stimulation of his left side. Evidence of reliable lateral differences in cardiac acceleration responses even under conditions in which the effects of lateral differences in head turning were removed suggested that the laterally differentiated cardiac responsiveness was not merely a function of increased motor activity consequent upon stimulation of the infant's right side but reflected a difference in sensitivity at the infant's two sides as well.     

The role of metabotropic glutamate receptors and cortical adaptation in habituation of odor-guided behavior

Decreases in behavioral investigation of novel stimuli over time may be mediated by a variety of factors including changes in attention, internal state, and motivation. Sensory cortical adaptation, a decrease in sensory cortical responsiveness over prolonged stimulation, may also play a role. In olfaction, metabotropic glutamate receptors on cortical afferent pre-synaptic terminals have been shown to underlie both cortical sensory adaptation and habituation of odor-evoked reflexes. The present experiment examined whether blockade of sensory cortical adaptation through bilateral infusion of the group III metabotropic glutamate receptor antagonist cyclopropyl-4-phosphonophenylglycine (CPPG) into the anterior piriform cortex could reduce habituation of a more complex odor-driven behavior such as investigation of a scented object or a conspecific. The results demonstrate that time spent investigating a scented jar, or a conspecific, decreases over the course of a continuous 10 minute trial. Acute infusion of CPPG bilaterally into the anterior piriform cortex significantly enhanced the time spent investigating the scented jar compared to investigation time in control rats, without affecting overall behavioral activity levels. Infusions into the brain outside of the piriform cortex were without effect. CPPG infusion into the piriform cortex also produced an enhancement of time spent investigating a conspecific, although this effect was not significant.     

Contextual control of long-term habituation in rats

This study examined contextual control of long-term habituation and whether such effects are dependent on the habituating response system. Habituation of the acoustic startle response transferred from the home cage to the testing context, whereas habituation of lick suppression was context specific (Experiments 1 and 2). Contextual control of habituation was demonstrated between 2 experimental contexts for lick suppression to a tone (Experiment 3) and bar-press suppression to a light (Experiment 4). Experiment 5 extinguished habituation of lick suppression and the orienting response to a tone with 27 exposures to the habituation context. Context specificity of both responses also was found. Previous failures to demonstrate contextual control of habituation may be due to the choice of response system and to less sensitive procedures to detect response recovery. The habituation mechanism for startle is independent from the process or processes that underlie habituation in other response systems, but the nature of these mechanisms is not yet known.     

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 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.     

Cardiac deceleration in newborns: habituation, dishabituation, and offset responses.

Twenty healthy, 1–4 day-old infants were selected from a sample of 135 neonates on the basis of alertness during testing. The infants were presented mild intensity colored light with gradual onset and offset while heart rate was monitored. Half the infants received six exposures to blue light followed by two exposures to blue-green light, whereas remaining subjects received colors in reverse order. Stimulus duration was 20 sec and variable periods between stimuli averaged 30 sec. Results of trend analysis of variance of the second-by-second cardiac data indicated that for infants older than the median age, the decelerative responses to both stimulus onset and offset were significant. Further, these subjects' onset decelerations significantly habituated within the six stimulus repetitions and significantly dishabituated with change in the stimulus color. Offset decelerations incremented over habituation trials and decremented with change in stimulus color. Responses of younger subjects were more variable which probably reflects their less complete recovery from the effects of maternal medication and the birth process.     

Investigating the dynamics of affect: Psychological mechanisms of affective habituation to pleasurable stimuli

Affective habituation (i.e., reductions in stimulus-evoked affective reactions as a result of previous exposure) may serve a functional purpose. However, little is know about the psychological mechanisms underlying this process. To elucidate the characteristics of affective habituation, two experiments that examined affective reactions to repeated exposures of pleasurable stimuli were conducted. Results of these experiments indicated that habituation trajectories are characterized by linear decreases in affect. Results also demonstrated that habituation can be slowed by the introduction of novel stimuli (i.e., “novelty effects”), effects that are dimensional (rather than taxonic) in nature. Experiment 2 demonstrated that habituation is mediated by conceptual rather than perceptual processes. Depressed and anhedonic individuals were not more susceptible to habituation in either experiment. The current findings and previous theorizing suggest that habituation may be an important component of an adaptive affective processing system that promotes effective responses to salient stimuli and prevents compulsive reward-seeking behavior.