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.     

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.     

Serotonin Depletion Does Not Prevent Intrinsic Sensitization in the Leech

Intrinsic sensitization is a form of behavioral facilitation that is distinct from the extrinsic sensitization normally studied. To examine whether intrinsic and extrinsic sensitization are mediated by different physiological processes, the effects of 5,7-dihydroxytryptamine-induced serotonin (5-HT) depletion on intrinsic sensitization of the leech whole-body shortening response were observed. Previous experiments have shown that 5-HT depletion disrupts dishabituation and extrinsic sensitization of this behavior in the leech. Intrinsic sensitization was observed in preparations from both control and 5-HT-depleted animals, indicating that this form of behavioral facilitation was not affected by 5-HT depletion. The differences in the effects of 5-HT depletion on intrinsic versus extrinsic sensitization suggest that there are distinct neurophysiological processes mediating these two forms of behavioral facilitation. In addition, 5-HT depletion appeared to disrupt a putative extrinsic form of habituation of the shortening reflex. These data support the hypothesis that both intrinsic and extrinsic processes of neuromodulation mediate habituation and sensitization.     

Regulation of distinct attractive and aversive mechanisms mediating benzaldehyde chemotaxis in Caenorhabditis elegans

Olfactory-mediated chemotaxis in nematodes provides a relatively simple system to study biological mechanisms of information processing. Analysis of the kinetics of chemotaxis in response to 100% benzaldehyde revealed an initial attractive response that is followed by a strong aversion to the odorant. We show that this behavior is mediated by two genetically separable attraction- and aversion-mediating response pathways. The attraction initially dominates behavior but with prolonged exposure habituation leads to a behavioral change, such that the odorant becomes repulsive. This olfactory habituation is susceptible to dishabituation, thereby re-establishing the attractive response to the odorant. Re-examination of the putative olfactory adaptation mutant adp-1(ky20) revealed that the phenotype observed in this line is due to a supersensitivity to a dishabituating stimulus, rather than a defect in the adaptation to odorants per se. A modified benzaldehyde chemotaxis assay was developed and used for the isolation of a mutant with a specific defect in habituation kinetics, expressed as a persistence of the attractive response.     

Perception of individuality in bat vocal communication: discrimination between, or recognition of, interaction partners?

Different cognitive processes underlying voice identity perception in humans may have precursors in mammals. A perception of vocal signatures may govern individualised interactions in bats, which comprise species living in complex social structures and are nocturnal, fast-moving mammals. This paper investigates to what extent bats recognise, and discriminate between, individual voices and discusses acoustic features relevant for accomplishing these tasks. In spontaneous presentation and habituation–dishabituation experiments, we investigated how Megaderma lyra perceives and evaluates stimuli consisting of contact call series with individual-specific signatures from either social partners or unknown individuals. Spontaneous presentations of contact call stimuli from social partners or unknown individuals elicited strong, but comparable reactions. In the habituation–dishabituation experiments, bats dishabituated significantly to any new stimulus. However, reactions were less pronounced to a novel stimulus from the bat used for habituation than to stimuli from other bats, irrespective of familiarity, which provides evidence for identity discrimination. A model separately assessing the dissimilarity of stimuli in syllable frequencies, syllable durations and inter-call intervals relative to learned memory templates accounted for the behaviour of the bats. With respect to identity recognition, the spontaneous presentation experiments were not conclusive. However, the habituation–dishabituation experiments suggested that the bats recognised voices of social partners as the reaction to a re-habituation stimulus differed after a dishabituation stimulus from a social partner and an unknown bat.     

Sensitization and habituation regulate reinforcer effectiveness

We argue that sensitization and habituation occur to the sensory properties of reinforcers when those reinforcers are presented repeatedly or for a prolonged time. Sensitization increases, and habituation decreases, the ability of a reinforcer to control behavior. Supporting this argument, the rate of operant responding changes systematically within experimental sessions even when the programmed rate of reinforcement is held constant across the session. These within-session changes in operant responding are produced by repeated delivery of the reinforcer, and their empirical characteristics correspond to the characteristics of behavior undergoing sensitization and habituation. Two characteristics of habituation (dishabituation, stimulus specificity) are particularly useful in separating habituation from alternative explanations. Arguing that habituation occurs to reinforcers expands the domain of habituation. The argument implies that habituation occurs to biologically important, not just to neutral, stimuli. The argument also implies that habituation may be observed in “voluntary” (operant), not just in reflexive, behavior. Expanding the domain of habituation has important implications for understanding operant and classical conditioning. Habituation may also contribute to the regulation of motivated behaviors. Habituation provides a more accurate and a less cumbersome explanation for motivated behaviors than homeostasis. Habituation also has some surprising, and easily testable, implications for the control of motivated behaviors.     

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.     

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.     

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.     

Evolution of Nonassociative Learning: Behavioral Analysis of a Phylogenetic Lesion

A recent phylogenetic analysis of two learning-related neuromodulatory traits in mechanosensory neurons of species related to the marine molluskAplysia californicaidentified one species,Dolabrifera dolabrifera,which lacked both neuromodulatory traits. Since these traits are thought to contribute importantly to certain forms of learning and memory in the defensive withdrawal reflexes ofAplysia,in the present study, I tested the prediction that facilitatory nonassociative learning would be reduced or absent inDolabrifera.I tested the tail-mantle withdrawal reflex inDolabriferaand size-matchedAplysiafor three forms of nonassociative learning and memory: dishabituation and short- and long-term sensitization. I found that the same protocols that produced significant dishabituation, short-term sensitization, and long-term sensitization inAplysiafailed in all three cases to produce significant learning inDolabrifera.Thus, the prediction from the prior mechanistic analysis is confirmed: Dishabituation and short- and long-term sensitization are significantly reduced and perhaps abolished inDolabrifera.Although not conclusive, this phylogenetic correlation between the absence of behavioral changes and the absence of neural mechanisms thought to underlie the behavioral changes gives support to the contemporary neuromodulatory model of dishabituation and sensitization inAplysia.Furthermore, these results raise the possibility that evolutionary alteration of two specific neuromodulatory mechanisms may have directly contributed to evolutionary change in behavioral plasticity.     

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.     

Habituation contributes to within-session changes in free wheel running.

Three experiments tested the hypothesis that habituation contributes to the regulation of wheel running. Rats ran in a wheel for 30-min sessions. Experiment 1 demonstrated spontaneous recovery. Rats ran more and the within-session decreases in running were smaller after 2 days of wheel deprivation than after 1 day. Experiment 2 demonstrated dishabituation. Running rate increased immediately after the termination of a brief extra event (application of the brake or flashing of the houselight). Experiment 3 demonstrated stimulus specificity. Rats completed the second half of the session in either the same wheel as the first half, or a different wheel. Second-half running was faster in the latter case. Within-session patterns of running were well described by equations that describe data from the habituation, motivation, and operant literatures. These results suggest that habituation contributes to the regulation of running. In fact, habituation provides a better explanation for the termination of wheel running than fatigue, the variable to which this termination is usually attributed. Overall, the present findings are consistent with the proposition that habituation and sensitization contribute to the regulation of several forms of motivated behavior.     

Sensitization and dishabituation of infant visual fixation

Dishabituation is defined as the renewed response to a familiarized stimulus upon its retest after the introduction of a novel-stimulus. Two experiments tested an account of dishabituation of infant visual fixation based on the hypothesis that a general, state-dependent sensitization produced by the novel-stimulus energizes responding to any subsequent stimulus. However, this sensitization is thought to be time-dependent, so that increasing delays between the termination of the novel stimuli and the onset of the retest should lead to diminished dishabituation. In Experiment 1, the time between the end of familiarization and the start of the retest of the familiarized pattern was held constant and the temporal location in that inverval of 2 novel stimulus presentations was manipulated. Significant dishabituation was observed only when the novel stimuli occurred shortly before the retest. In Experiment 2, the number of novel-stimulus presentations was systematically manipulated and the magnitude of dishabituation was observed. Significant dishabituation occurred after 2 or 4, but not after 6, novel-stimulus presentations. These findings were consistent with the sensitization explanation of dishabituation, and cast doubt on an explanation of this form of dishabituation based on schema-change.     

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.     

The evolutionary significance of habituation and sensitization across phylogeny: A behavioral homeostasis model

The phenomenon of habituation may be interpreted as a process that has evolved for filtering out iterative stimuli of little present relevance. That habituation is seen in aneural as well as neural organisms throughout phylogeny with remarkably similar characteristics suggests that its role is an important one in animal survival. If habituation is to be viewed as a process to filter out iterative stimuli that have no significant consequences, then how is sensitization to be viewed? One way of viewing these two behavioral changes, i.e. habituation and sensitization, is that they are homeostatic processes which optimize an organism’s likelihood of detecting and assessing the significance of a stimulus in a new iterative series or a change in it. If one views the level of initial responsiveness to a new stimulus as a function of an organism’s threshold just prior to stimulus occurrence, then “high responders” (i.e. those who initially react more strongly) are assumed to have a lower threshold for detecting and assessing the significance of this stimulus than are the “low responders” (i.e. those who initially react more weakly). Thus, high-responders would initially receive more sensory input and progressively decrease their responsiveness to a non-threatening stimulus (habituation). Likewise, initial low-responders would receive less sensory input followed by a decreased threshold and an increased response to the next stimulus occurrence (sensitization). The level of responsiveness achieved in both habituaters and sensitizers, as an asymptote is approached, is a balance between being too sensitive to an unimportant stimulus (and possibly missing other significant stimuli) and being too insensitive, and missing a change in the relevance of the present stimulus. These response changes can be taken as indices of the organism’s mechanisms for achieving an appropriate threshold level to an iterative stimulus in order to accurately assess its present significance and then eventually to asymptote at an optimal stable response level. This approach toward an asymptote is a behavioral homeostatic process that reflects the accumulated significance of the iterative stimulus at each occurrence. The purpose of adding “behavioral” to the term “homeostasis” is to extend the usual meaning of the concept from primarily internal processes to also include (a) iterative external stimulation, (b) the organism’s initial threshold to the initial stimulus as well as (c) the behavior which results from it. Since we are discussing organisms that range from intact, single-celled protozoa to intact mammals, as well as surgically simplified preparations, the termsstimulus, response andbehavior will be used broadly. While other investigators have focused on specific cellular mechanisms underlying habituation and sensitization in a given organism, this paper focuses on the adaptive significance of these two behavioral processes viewed across phylogeny.     

Sensitization and habituation of motivated behavior in overweight and non-overweight children

The rate of habituation to food is inversely related to energy intake, and overweight children may habituate slower to food and consume more energy. This study compared patterns of sensitization, as defined by an initial increase in operant or motivated responding for food, and habituation, defined by gradual reduction in responding, for macaroni and cheese and pizza in overweight and non-overweight 8- to 12-year-old children. Non-overweight children habituated faster to both foods than overweight children (p = .03). All children recovered motivated responding for a new food (chocolate). Overweight children consumed more energy than non-overweight children (p = .0004). Children who showed a sensitization in responding consumed more food (p = .001), and sensitization moderated the effect of overweight on habituation, with slower habituation for overweight children who sensitized (p < .001). This study replicates previous data on overweight/non-overweight differences in habituation of food and energy intake, and provides new information that individual differences in sensitization and habituation of motivated responding to obtain food may be associated with a sustained motivation to eat, resulting in greater energy intake.     

Delayed-onset sensitization emerges after dishabituation in developing Aplysia.

A recent study of the development of nonassociative learning in the siphon withdrawal reflex of Aplysia showed that dishabituation (facilitation of an habituated response) and sensitization (facilitation of a nonhabituated response) emerge according to different developmental timetables: dishabituation precedes sensitization by approximately 60 days (Rankin & Carew, 1988). Both forms of facilitation of the reflex were observed within 90 s of an electrical shock to the tail. However, more recent work by Marcus and colleagues (1988) in adult animals revealed that sensitization can have a delayed onset of 20-30 min after a strong tail shock. Since the developmental study of Rankin and Carew (1988) only tested the reflex for 10 min after tail shock, it is possible that sensitization was in fact present at earlier developmental stages, but was undetected. To examine this question, in the present study we utilized a longer (40-50 min) post-shock observation period to determine whether delayed-onset sensitization is exhibited in juvenile Aplysia, and if so, when it is expressed during development. In our first experiment, we found that Early Stage 12 juveniles (80-95 days after metamorphosis) showed significant delayed-onset sensitization 30-50 min after a strong tail shock. In a second experiment, we found that delayed-onset sensitization was absent in Stage 11 animals (20-70 days after metamorphosis). Thus delayed-onset sensitization emerges in Early Stage 12. The fact that the birthdate of delayed-onset sensitization is at least 30 days after that of dishabituation (Rankin & Carew, 1987, 1988) supports the hypothesis that these two forms of nonassociative learning may have at least partly different underlying mechanisms.     

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.     

Olfaction as a model system for the neurobiology of mammalian short-term habituation

Olfaction represents an ideal model system for the study of mammalian habituation given that it is an anatomically relatively simple system with strong reciprocal connections to the limbic system, driving both reflexive and non-reflexive (motivated) behaviors that are easily quantifiable. Data are reviewed here demonstrating short-term habituation of the odor-evoked heart-rate orienting reflex described according to the criteria for habituation outlined by Thompson and Spencer [Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Reviews, 73(1), 16–43]. A necessary and sufficient mechanism of short-term habituation is then described, which involves a metabotropic glutamate receptor mediated depression of afferent input to the piriform (primary olfactory) cortex. Finally, evidence for, and a mechanisms of, dishabituation of the orienting reflex and cortical adaptation are described.     

Novelty,familiarity, and infant reasoning

Where stimuli are possibly discriminable but do not elicit spontaneous differential looking it is customary to use one or other variation of the habituation–dishabituation method in order to investigate their discriminability, and the literature abounds with such studies. However, there are many variations on habituation–dishabituation procedures, varying both within and between the sensory modalities investigated. Additionally, infant attention is a dynamic process which is likely to change over time, and given the great variations in procedures it can often be difficult to know whether infants are giving a familiarity or a novelty preference at test, which can make interpretation of results a difficult, and often controversial problem. Houston‐Price and Nakai give some clear examples of the changing nature of infant preferences, and relate them particularly to the amount of familiarisation prior to testing. The model they favour (and which receives a good deal of support) is that put forward by (among others) Hunter and Ames (1988) in which preferences change over the course of familiarisation time, from preference for neither familiarity or novelty, to familiarity, to no preference, to a novelty preference. They suggest that ‘If an attentional shift from what is familiar to what is novel is always found as the encoding of a familiar stimulus… is completed… then the pattern of change in preference over time should provide crucial information regarding the identity of the obtained effect’. I will argue that this attentional shift is not always found, and that in many instances we need converging evidence in order to clarify experimental findings. Copyright © 2004 John Wiley & Sons, Ltd.