A dissociation between one-trial overshadowing and the effect of a distractor on habituation

Rats drank a novel vinegar flavour and were subsequently tested either for habituation of neophobia to vinegar or for the conditioning of an aversion to vinegar when it was followed 4 hr later by an injection of lithium chloride. If they drank a sucrose distractor immediately after their first vinegar trial, habituation of neophobia was disrupted but conditioning was not. Sucrose consumed 3.5 hr after the initial vinegar trial, on the other hand, had less of an effect on habituation, but did disrupt conditioning. An incidental finding, replicated in two subsequent experiments, was that the immediate sucrose distractor had no effect on habituation when animals were tested 48 hr after their initial habituation trial. We interpret these results to suggest that distractors affect habituation by a process of generalization decrement but overshadow conditioning through a process of associative competition.     

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.     

Differential role of inhibition in habituation of two independent afferent pathways to a common motor output

Many studies of the neural mechanisms of learning have focused on habituation, a simple form of learning in which a response decrements with repeated stimulation. In the siphon-elicited siphon withdrawal reflex (S-SWR) of the marine mollusk Aplysia, the prevailing view is that homosynaptic depression of primary sensory afferents underlies short-term habituation. Here we examined whether this mechanism is also utilized in habituation of the tail-elicited siphon withdrawal reflex (T-SWR), which is triggered by an independent, polysynaptic afferent pathway that converges onto the same siphon motor neurons (MNs). By using semi-intact preparations in which tail and/or siphon input to siphon MNs could be measured, we found that repeated tail stimuli administered in the presence of a reversible conduction block of the nerves downstream of the tail sensory neurons (SNs) completely abolished the induction of habituation. Subsequent retraining revealed no evidence of savings, indicating that the tail SNs and their immediate interneuronal targets are not the locus of plasticity underlying T-SWR habituation. The networks closely associated with the siphon MNs are modulated by cholinergic inhibition. We next examined the effects of network disinhibition on S-SWR and T-SWR habituation using an Ach receptor antagonist d-tubocurarine. We found that the resulting network disinhibition disrupted T-SWR, but not S-SWR, habituation. Indeed, repeated tail stimulation in the presence of d-tubocurarine resulted in an initial enhancement in responding. Lastly, we tested whether habituation of T-SWR generalized to S-SWR and found that it did not. Collectively, these data indicate that (1) unlike S-SWR, habituation of T-SWR does not involve homosynaptic depression of SNs; and (2) the sensitivity of T-SWR habituation to network disinhibition is consistent with an interneuronal plasticity mechanism that is unique to the T-SWR circuit, since it does not alter S-SWR.     

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.     

Contrasting effects of imidacloprid on habituation in 7- and 8-day-old honeybees (Apis mellifera)

We examined the effects of sublethal doses (0.1, 1, and 10 ng per animal) of a new neonicotinoid insecticide, Imidacloprid, on habituation of the proboscis extension reflex (PER) in honeybees (Apis mellifera) reared under laboratory conditions. In untreated honeybees, the habituation of the proboscis extension reflex is age-dependent and there is a significant increase in the number of trials required for habituation in older bees (8-10 days old) as compared to very young bees (4-7 days old). Imidacloprid alters the number of trials needed to habituate the honeybee response to multiple sucrose stimulation. In 7-day-old bees, treatment with Imidacloprid leads to an increase in the number of trials necessary to abolish the response, whereas in 8-day-old bees, it leads to a reduction in the number of trials for habituation (15 min and 1 h after treatment), and to an increase 4 h after treatment. The temporal effects of Imidacloprid in both 7- and 8-day-old bees suggest that 4h after treatment the observed effects are due to a metabolite of Imidacloprid, rather than to Imidacloprid itself. Our results suggest the existence of two distinct subtypes of nicotinic receptors in the honeybee that have different affinities to Imidacloprid and are differentially expressed in 7- and 8-day-old individuals.     

Intermittent exposure to social defeat and open-field test in rats: acute and long-term effects on ECG,body temperature and physical activity

This study investigated the effects of exposure to an intermittent homotypic stressor on: (i) habituation of acute autonomic responsivity (i.e. cardiac sympathovagal balance and susceptibility to arrhythmias), and (ii) circadian rhythmicity of heart rate, body temperature, and physical activity. After implantation of a transmitter for the radiotelemetric recording of electrocardiogram (ECG), body temperature and physical activity, adult male rats (Rattus norvegicus, Wild Type Groningen strain) were repeatedly exposed (10 consecutive times, on alternate days) to either a social stressor (defeat by a con-specific, n = 15) or an open-field, control challenge (transfer to a new cage; n = 8). ECGs, body temperature and physical activity were continuously recorded in baseline, test and recovery periods (each lasting 15 min), at the 1st and 10th episodes of both defeat and open-field challenge. The circadian rhythms of heart rate, body temperature and physical activity were monitored before (5 days), during (16 days) and after (21 days) the intermittent stress protocol. This study indicates that there is no clear habituation of either acute cardiac autonomic responsivity (as estimated by means of time-domain indexes of heart rate variability) or arrhythmia occurrence to a brief, intermittent, homotypic challenge, regardless of the nature of the stressor (social or non-social). On the other hand, rats exposed to social challenge also failed to show adaptation of acute temperature and activity stress responsiveness, whereas rats facing open-field challenge developed habituation of activity and sensitization of temperature responses. Repeated social challenge produced remarkable reductions of the heart rate circadian rhythm amplitude (this effect being significantly greater than that produced by intermittent open-field), but only minor changes in the daily rhythms of body temperature and physical activity.     

Activity of cGMP-dependent protein kinase (PKG) affects sucrose responsiveness and habituation in Drosophila melanogaster

The cGMP-dependent protein kinase (PKG) has many cellular functions in vertebrates and insects that affect complex behaviors such as locomotion and foraging. The foraging (for) gene encodes a PKG in Drosophila melanogaster. Here, we demonstrate a function for the for gene in sensory responsiveness and nonassociative learning. Larvae of the natural variant sitter (for(s)) show less locomotor activity during feeding and have a lower PKG activity than rover (for(R)) larvae. We used rover and sitter adult flies to test whether PKG activity affects (1) responsiveness to sucrose stimuli applied to the front tarsi, and (2) habituation of proboscis extension after repeated sucrose stimulation. To determine whether the differences observed resulted from variation in the for gene, we also tested for(s2), a sitter mutant produced on a rover genetic background. We found that rovers (for(R)) were more responsive to sucrose than sitters (for(s) and for(s2)) at 1-, 2-, and 3-wk old. This was true for both sexes. Differences in sucrose responsiveness between rovers and sitters were greater after 2 h of food deprivation than after 24 h. Of flies with similar sucrose responsiveness, for(R) rovers showed less habituation and generalization of habituation than for(s) and for(s2) sitters. These results show that the PKG encoded by for independently affects sensory responsiveness and habituation in Drosophila melanogaster.     

The effects of sound on pupil size and the pupil light reflex

The effects of auditory stimulation on pupil size and the pupil light reflex were investigated in 33 male volunteers. A 95dB tone caused pupillary dilation and a reduction in the amplitude of the light reflex. Although the light reflex amplitude was positively correlated with pupil size in the resting state the effects of noise on the two measures were independent since the pupillary dilation response showed a marked habituation after two presentations of the tone whereas the effect on the light reflex remained the same. People showing high impulsivity scores on the EPQ tended to have smaller pupils (i.e. low arousal). There was also a relationship between impulsivity and light reflex amplitude, but this was probably a secondary consequence of the relationship between the latter measure and pupil size in the resting state.     

Conditioning the unconditioned response: modification of the rabbit's (Oryctolagus cuniculus) unconditioned nictitating membrane response

Conditioning-specific reflex modification (CRM) occurs when classical conditioning modifies responding to an unconditioned stimulus (US) in the absence of a conditioned stimulus (CS). Three experiments monitored rabbit nictitating (Oryctolagus cuniculus) membrane unconditioned responses to 5 intensities and 4 durations of periorbital electrical stimulation before and after CS or US manipulation. CRM occurred after 12 days of CS-US pairings but not following unpaired CS/US presentations or restraint. CRM survived CS-alone and CS/US-unpaired extinction of the conditioned response (CR) but not presentations of the US alone, although CRs remained intact. Thus, CRs could be weakened without eliminating CRM and CRM could be weakened without eliminating CRs. Data indicate CRM is a reliable, associative effect that is more than a generalized CR and may not be explained by habituation, stimulus generalization, contextual conditioning, or bidirectional conditioning.     

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.     

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.     

Conscious contents as reflexive processes: Evidence from the habituation of high-level cognitions

Reflexes are often insuppressible, predictable, and susceptible to external control. In contrast, conscious thoughts have been regarded as whimsical, ‘offline,’ and shielded from external control. Recent advances suggest that conscious thoughts are more reflex-like and susceptible to external control than previously thought. In one paradigm, high-level conscious thoughts (subvocalizations) are triggered by external control, as a function of external stimuli and experimenter-induced action sets. It has been hypothesized that these conscious contents are activated involuntarily and in a reflex-like manner. If such is the case, then these activations should possess a well-known property of the reflex: habituation. Accordingly, we found that involuntary high-level cognitions (subvocalizations) habituated (i.e., were less likely to arise) after repeated stimulation. As in the case of the habituation of a reflex, this novel effect was stimulus-specific. We discuss the implications of this finding for theories about consciousness and about psychopathological phenomena involving undesired, involuntary cognitions.     

Gastric secretion as a function of acute and chronic stress in the gastric fistula rat.

In Experiment 1 rats exposed to signaled and unsignaled grid shock secreted more gastric acid after shock stress (chronic stress) for 8 days compared to the first 12 hr. of shock stress (acute stress). However, Experiment 2 indicated that the higher gastric acid values under chronic stress were not significantly greater than prestress baseline values. The results are interpreted to reflect an inhibition of gastric acid secretion as a function of acute stress. During chronic stress this inhibition is followed by a habituation of gastric secretory processes which is observed as a return of secretion volume to baseline levels.     

Habituation of orienting responses as a function of “instructional set”

Electrodermal and plethysmographic recordings were obtained from three groups of alcoholic patients. The groups differed with respect to instructions given for response to a series of words spoken by the experimenter. Group A was told to report verbally their first associations for each word presented. Group B received instructions to think of an association for each word without reporting it. Group C was to respond to each word by repeating it after it was spoken by the experimenter. The instructions did not have the predicted differing effects upon rate of EDR habituation. However, the over-all amplitude of EDR was lower for Group B than for Group A or C. We observed very little habituation of the plethysmographic OR as measured by per cent of subjects responding to each word. As with the EDR data, Group B shows less responsivity, i.e., this group produced significantly fewer plethysmographic responses over all words than did either of the other two groups. The relative importance of association and of verbal responding to a stimulus word for eliciting autonomic responses was considered.     

Effects of monotonous stimulation on cortical alertness in fast and slow habituation groups

The present study investigated cortical alertness in Ss displaying fast and slow habituation of the evoked skin conductance response (SCR). From Sokolov's statement (Perception and the conditioned reflex, 1963, Pergamon) that the final stage of habituation is sleep, it was predicted that during monotonous stimulation, Ss displaying rapid habituation of the evoked SCR would show a more rapid decline in cortical alertness than Ss displaying slow habituation. Quantified EEG and electrodermal measures of cortical alertness were obtained from fast and slow habituation groups tested under conditions of either repetitive auditory stimulation or reduced sensory input. The results indicated that 8–13 Hz EEG abundance declined more rapidly in fast than in the slow habituation groups under both conditions of monotonous stimulation. No differences were obtained for the lower EEG frequencies (4–8 and 2–4 Hz) or for tonic electrodermal measures.     

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.     

Retention of a classically conditioned reflex response in spinal cat

Retention of classically conditioned flexion reflex facilitation was examined in unanesthetized, decerebrate, acute spinal cats. Flexion reflex facilitation, recorded from the tibialis anterior muscle, was obtained by pairing saphenous nerve stimulation (the conditioned stimulus) with superficial peroneal nerve stimulation (the unconditioned stimulus). The flexion reflex declined in control animals receiving the same number of nerve stimuli over the same time span, but in an explicitly unpaired sequence. To investigate retention, conditioned stimuli were presented at 5-min intervals following acquisition for a 2 1/2-h period. During this time a significant difference between conditioning and control groups was maintained even to the last trial, with no indication that the difference was subsiding over time. The results support the possibility that a classical conditioning paradigm applied to the spinal cord can induce alterations in spinal reflexes of long duration. Furthermore, the results appear to rule out post-tetanic potentiation as a mechanism producing the observed long-term effects.     

The lateral tongue reflex in human neonates

We undertook an investigation of the lateral tongue reflex to determine whether reflex sensitivity was systematically related to selected perinatal factors. The subjects were 24 male and 27 female newborns with a mean age of 28.9 hr. (SD = 16.8, range 5--72 hr.). The lateral tongue reflex was elicited by applying tactile stimulation of varying intensity to the lateral edge of the tongue approximately 1 cm off midline. Eight different stimuli from the Semmes-Weinstein esthesiometer were used; forces ranged from 68 mg to 3.6 gm. A total of 32 stimulations were given in two repetitions of 16 each (8 on the right side and 8 on the left side). The mean number of positive responses was 19.9 (SD = 3.2, range 13--25), with a 5% response at the lowest level of stimulation and a 100% response at the highest level. There were not differences in total number of positive responses or thresholds on the right and left sides, or in Repetitions I and II. There were no differences between males and females, vaginally and caesarian delivered infants, or resuscitated and non-resuscitated infants. No systematic differences were observed as a function of length of labor, obstetric medications, postnatal age at time of testing, Apgar scores, birth weight, or gestational age. The results suggest that the lateral tongue reflex is a stable and reproducible response that could be used to measure oral sensation, both in normal neonates and in subjects with various anatomical and/or neurosensory deficits.     

Paired comparison scaling of reaction potential from simultaneous measurements of GSR and looking time

Thurstone’s method of scaling from paired comparison data was employed to obtain estimates of reaction potential on eight successive presentations of randomly generated polygons. One set of scale values was based upon the magnitude of the GSR made by each of 40 Ss to the onset of each stimulus. Another set of scale values was based upon the Ss looking times, when the S was instructed to press a switch to terminate the stimulus after he finished looking at it. Following termination of each stimulus, a 20-sec period of no stimulation intervened prior to the next stimulus. The GSR reduced in size from trial to trial, describing a typical habituation curve, while looking time increased from trial to trial. Across trials the two sets of scale values were significantly negatively correlated (r=?0.91). The failure to find habituation of looking time was explained on the assumption that the 20-sec period between stimuli was noxious to the Ss, which resulted in longer and longer looking times across trials. These results were interpreted as indicating that habituation of the GSR is not merely a matter of reduced attention in the cognitive sense. In addition, it was pointed out that the use of orienting reflex concepts in dealing with attentional and other cognitive phenomena may be unjustified.     

Effects of vestibular stimulation on motor development and stereotyped behavior of developmentally delayed children

Four developmentally delayed babies were given semicircular canal stimulation in an effort to facilitate their motor and reflex development. Each of the children also exhibited abnormal stereotyped movements. The theory was advanced that these movements are related to motor development and that significant improvements in motor abilities will produce changes in the intensity and/or form of stereotypic responding. Semicircular canal stimulation was provided by rotating the children in a motor-driven chair at a velocity of about 17 rpm for 10 minutes daily over a period of 2 weeks. Standard motor and reflex measures were taken before, during, and after the rotation treatment period. Daily observations were made of the children's stereotyped movements. Over the course of the study all of the children showed motor and/or reflex changes that were attributable to the vestibular stimulation. In addition, some evidence was obtained linking changes in stereotypic responding to the vestibular stimulation.This work was supported by PHS Grant Nos.HD15051 and HD13344.