Control of gill reflex habituation and the rate of EPSP decrement of L7 by a common source in the CNS of Aplysia

It was found in older Aplysia that the rate of decrement of the EPSP evoked in L₇ by repeated tactile stimulation of the gill was dependent on the strength of the applied stimulus and that the rate of decrement paralleled the rate of gill reflex habituation. As the stimulus intensity was increased both rates slowed. In contrast, it was found in young Aplysia that the rate of EPSP decrement and the rate of gill reflex habituation were independent of the strength of the stimulus applied to the gill. Neither rate changed as the stimulus intensity was changed. Moreover, L₇'s of young animals are more responsive to tactile stimuli applied to the gill than are L₇'s of older animals and the difference in excitability is not due to any differences in passive membrane properties between the L₇'s in young and older Aplysia. These findings are fully consistent with and supportive of the proposal that a common neuronal source in the parieto-visceral ganglion of Aplysia controls the rate of gill reflex habituation, the synaptic input to L₇, and the rate of decrement of this input, evoked by repeated tactile stimulation of the gill. Additinally, it was proposed that this common source is developed in completely in the young. As a consequence of this incomplete development, young Aplysia exhibit less adaptability to changing stimulus conditions and, in general, less ability to suppress their behavior. It may thus be possible to study directly developmental changes in the nervous system which act to transform juvenile behavior to adult behavior.     

Neurophysiological mechanisms underlying habituation of the tentacle retraction reflex in the land slug Ariolimax

Habituation of the tentacle retraction reflex was studied at the following response levels: (1) Muscle tension elicited in the tentacle retractor muscle by repeated stimulation of a cerebral nerve (at 60-sec intervals) declined in parallel with evoked activity of the largest unit in the tentacle retractor nerve. (2) The largest unit in the tentacle retractor nerve (L₄) showed spontaneous recovery and dishabituation. The rate of response decrement was inversely related to the strength of stimulus, and an optimal interstimulus interval ca. 60 s was found. Retention of habituation for 24 h was exhibited. (3) The major retractor motoneurons (L₂, L₃, L₄) all showed habituation, dishabituation, and spontaneous recovery. The decline of L₄ activity was parallelled by a decline in muscle response. (4) Compound EPSPs elicited in the retractor motoneurons by stimulation of sensory pathways showed habituation and dishabituation. (5) Unitary EPSPs elicited by stimulation of cerebral nerves and connectives with minimal stimulus strengths also showed habituation and were unaffected by spontaneously occurring EPSPs. Dishabituation by another pathway was also shown. (6) Depolarization of L₄ by a constant current produced spike trains of constant firing rate and evoked a constant level of muscle tension in repeated trials, suggesting the absence of habituation in a peripheral nerve net or at the neuromuscular junction.     

Responsiveness to sucrose and habituation of the proboscis extension response in honey bees

In honey bees, complex behaviours such as associative learning correlate with responsiveness to sucrose. In these behaviours, the subjective evaluation of a sucrose stimulus influences the behavioural performance. Habituation is a well-known form of non-associative learning. In bees, the proboscis extension response can be habituated by repeatedly stimulating the antennae with a low sucrose concentration. A high sucrose concentration can dishabituate the response. This study tests whether habituation correlates with responsiveness to sucrose in bees of different behavioural states and in bees which are habituated with different sucrose concentrations. Habituation and dishabituation in newly emerged bees, 5-day-old bees and foragers strongly correlated with responsiveness to sucrose. Bees with high responsiveness to sucrose displayed a lower degree of habituation and showed greater dishabituation than bees with low responsiveness. The degree of habituation and dishabituation also depended on the concentration of the habituation stimulus. These experiments demonstrate for the first time in a non-associative learning paradigm that the subjective strength of a sucrose stimulus determines the behavioural performance. Non-associative learning shares this property with associative learning, which suggests that the two processes might rely on similar neural mechanisms.Abbreviations: GRS Gustatory response score - PER Proboscis extension response     

Activity and habituation in the brain of the polyclad flatworm Freemania litoricola.

1. A variety of spontaneously active units was measured in the brain of the polyclad flatworm Freemania litoricola. Following application of MgCl2 there was both a decrease in number of active units and a decrease in frequency of firing of those cells which persisted in their activity. 2. Receptors which respond to vibration stimuli evoke potentials in the posterior part of the brain. Repetitive stimulation leads to habituation, the extent of which is dependent on both the number of times stimulated and the strength of the stimulus. Weaker stimuli habituate more rapidly than strong stimuli. Habituated responses can be dishabituated by tactile stimuli and also by stronger intensity stimuli of the same modality. The vibration-evoked potentials appear to occur in at least second-order cells, since vibration responses are abolished by the application of MgCl2. 3. Tactile responses can also be elicited from the posterior portion of the brain when the stimulus is applied to the periphery of the animal. These responses are insensitive to MgCl2. 4. Both vibration and tactile evoked responses are able to evoke further barrages of spike activity. 5. The presence of a dual sensitizing and inhibitory system during habituation is discussed.     

Decrease in excitability of LG following habituation of the crayfish escape reaction

Crayfish escapes from threatening stimuli to the abdomen by tailflipping upwards and forwards. This lateral giant (LG)-mediated escape reaction habituates readily upon repetitive sensory stimulation. Using an isolated abdominal nerve cord preparation, we have analyzed the change in LG activity by applying additional sensory stimulation after different periods following habituation to characterize the retention of LG habituation. Results show that the LG mediated response habituates more quickly, but the retention time is shorter, as repetitive sensory stimulation is applied at progressively shorter inter-stimulus time intervals. The spike response of LG recovers quickly, within several minutes after habituation, but they fail to spike when an additional stimulus is applied after specific long periods following habituation. The critical period of the delay for this decrease in excitability of LG is dependent on the inter-stimulus time interval of the initial repetitive stimulus. As the inter-stimulus interval became longer, the delay needed for decrease in excitability became shorter. Furthermore, the local injection of 10^–6 mol l^–1 octopamine into the neuropil just following habituation promotes the achievement of decrease in excitability. No effects were observed when 10^–6 mol l^–1 serotonin and tyramine were injected. These results suggested octopamine promotes decrease in excitability of LG following habituation.     

Dual pathways for tactile sensory information to thoracic interneurons in the cockroach

The escape system of the American cockroach is both fast and directional. In response to wind stimulation both of these characteristics are largely due to the properties of the ventral giant interneurons (vGIs), which conduct sensory information from the cerci on the rear of the animal to type A thoracic interneurons (TI_As) in the thoracic ganglia. The cockroach also escapes from tactile stimuli, and although vGIs are not involved in tactile-mediated escapes, the same thoracic interneurons process tactile sensory information. The response of TI_As to tactile information is typically biphasic. A rapid initial depolarization is followed by a longer latency depolarization that encodes most if not all of the directional information in the tactile stimulus. We report here that the biphasic response of TI_As to tactile stimulation is caused by two separate conducting pathways from the point of stimulation to the thoracic ganglia. Phase 1 is generated by mechanical conduction along the animal's body cuticle or other physical structures. It cannot be eliminated by complete lesion of the nerve cord, and it is not evoked in response to electrical stimulation of abdominal nerves that contain the axons of sensory receptors in abdominal segments. However, it can be eliminated by lesioning the abdominal nerve cord and nerve 7 of the metathoracic ganglion together, suggesting that the relevant sensory structures send axons in nerve 7 and abdominal nerves of anterior abdominal ganglia. Phase 2 of the TI_As tactile response is generated by a typical neural pathway that includes mechanoreceptors in each abdominal segment, which project to interneurons with axons in either abdominal connective. Those interneurons with inputs from receptors that are ipsilateral to their axon have a greater influence on TI_As than those that receive inputs from the contralateral side. The phase 1 response has an important role in reducing initiation time for the escape response. Animals in which the phase 2 pathway has been eliminated by lesion of the abdominal nerve cord are still capable of generating a partial startle response with a typically short latency even when stimulated posterior to the lesion. © 1995 John Wiley & Sons, Inc.     

Response decrement in an auditory neurone of the locust

An identified interneurone (SA3) of the suboesophageal ganglion has an axon in both circumoesophageal connectives ascending to the brain. This is a novel morphology for a cell in the auditory system of the locust. The neurone is also novel for its physiological responses to sound in that it displays side-dependent response decrement (habituation). Responses to a tone directed at one ear decrement without affecting responses from the other ear. The responses on the decremented side recover when the opposite ear is stimulated. The decrement is the result of a diminishing amplitude of the compound excitatory post-synaptic potential but no inhibition is seen. Response decrement does not occur if the stimulus frequency is varied.     

Primitive nervous systems: Peripheral habituation in decerebrate polyclad flatworms

The response to a vibration stimulus recorded from the cords of the ventral submuscular plexus of the polyclad flatworm, Notoplana acticola, consists of a burst of action potentials. The response can be abolished by the application of MgCl₂ to the sea water bathing the preparation. With repeated application of the stimulus, decreasing numbers of action potentials can be measured. This waning responsiveness can be dishabituated by applying a more intense vibration stimulus or with electrical shocks applied directly to the ventral nerve plexus. With electrical stimuli a number of shocks have to be applied before the response can be dishabituated. Changes in responsiveness can be measured simultaneously in a number of sites in the plexus even after the nerves between recording sites have been severed. With different interstimulus intervals the extent of habituation changes. As interstimulus intervals increase from 1 to 5 sec, there appears to be a decrease in responsiveness which recovers when interstimulus intervals become longer than 5 sec.     

Neural cell adhesion molecule (NCAM-/-) null mice show impaired sensitization of the startle response

The neural cell adhesion molecule (NCAM) plays important roles in development of the nervous system and in synaptic plasticity and memory formation in the adult. The present study sought to further investigate the role of NCAM in learning by testing habituation and footshock sensitization learning of the startle response (SR) in NCAM null mutant (NCAM-/-) and wildtype littermate (NCAM+/+) mice. Whereas habituation is a form of non-associative learning, footshock sensitization is induced by rapid contextual fear conditioning. Habituation was tested by repetitive presentation of acoustic and tactile startle stimuli. Although NCAM-/- mice showed differences in sensitivity in both stimulus modalities, habituation learning was intact in NCAM-/- mice, suggesting that NCAM does not play a role in the mechanisms underlying synaptic plasticity in the startle pathway. Footshock sensitization was elicited by presentation of electric footshocks between two series of acoustic stimuli. In contrast to habituation, footshock sensitization learning was attenuated in NCAM-/- mice: the acoustic SR increase after the footshocks was lower in the mutant than in wildtype mice, indicating that NCAM plays an important role in the relevant brain areas, such as amygdala and/or the hippocampus.     

The integration of antagonistic reflexes revealed by laser ablation of identified neurons determines habituation kinetics of the Caenorhabditis elegans tap withdrawal response

Previously, we described the circuitry that underlies the tap withdrawal response of the nematode Caenorhabditis elegans. In response to a light mechanosensory stimulus a worm will withdraw, usually by initiating backward locomotion, but occasionally with increased forward locomotion. The form of an animal's response is a product of the balance between two antagonistic reflexes: backward locomotion (reversals) triggered by anterior mechanosensory input and forward locomotion (accelerations) triggered by posterior mechanosensory input. During habituation of this reflex, the frequency of forward and backward locomotion in response to tap is modulated by both experience and interstimulus interval; reversals are more frequent early in a habituation series and at longer Inter stimulus intervals. Single-cell laser microsurgery was used to study each of the subcomponents of the intact behavior during habituation training. Groups of intact or laserablated worms were habituated at either a 10-s or a 60-s inter stimulus interval and the kinetics of habituation in each group was analyzed. We demonstrate that each component of the behavior habituates and does so with kinetics that are consistent with the decrement observed in the intact animal.Abbreviations ALM anterior lateral microtubule - AVM anterior ventral microtubule - ISI interstimuls interval - NGM nematode growth medium - PLM posterior lateral microtubule - PVC posterior ventral interneuron C     

Novelty stress and reproductive state alters responsiveness to sensory stimuli and 5-HT neuromodulation in crayfish

Sensory stimuli can produce varied responses depending on the physiological state of an animal. Stressors and reproductive stage can result in altered biochemical status that changes the responsiveness of an animal to hormones and neuromodulators, which affects whole animal behavior in relation to sensory stimuli. Crayfish serve as a model for examining the effects of neuromodulators at the neuromuscular junctions (NMJs) and for alterations in stereotypic behaviors for particular stimuli. Thus, we used crayfish to examine the effect of novelty stressors in males and the effect of being gravid in female crayfish to exogenous application of serotonin (5-HT). The responsiveness of neuromuscular junctions to 5-HT revealed that stressed as well as gravid crayfish have a reduced response to 5-HT at NMJs. The stressed crayfish were not fatigued since the basal synaptic responses are large and still showed a pronounced response to 5-HT. Using intact animals to examine a tail flip behavior, we showed that the rate of habituation in tail flipping to a strong repetitive stimulus on the telson is reduced in stressed males. Gravid females show no tail flipping behavior upon telson stimulation.     

Central neuronal pathways of the cardioinhibitory reflex in the isopod crustacean Bathynomus doederleini

We have already identified central neurons for cardioinhibition and cardioacceleration in Bathynomus, an isopod crustacean. The 1st thoracic ganglion (TG1) has cardioinhibitory neurons, which we call CIs, while the 2nd and 3rd thoracic ganglia (TG2 and TG3) have cardioacceleratory neurons, which we call CA1s and CA2s. We examined neuronal pathways for cardioinhibitory reflexes in whole animal preparations, using intracellular and extracellular recording methods. Cardiac inhibition in response to a variety of external stimuli was mediated by activation of CIs and inhibition of both CAs. When preparations had the ventral nerve cord intact, CIs were activated by excitatory postsynaptic potentials and CAs were inhibited by inhibitory postsynaptic potentials in response to tactile stimuli applied to sensilla setae on appendages and afferent stimuli applied to ganglionic roots of the thoracic ganglia. However, stimulation of ganglionic nerve roots of TG2 and TG3, or tactile stimulation of the body surface, failed to evoke inhibition of CAs in preparations in which both the cerebral ganglion and TG1 had been excised. These results suggest that TG1 is an indispensable central region for the excitation of CI and for inhibition of CA neurons, induced by tactile stimuli and by stimuli applied to nerve roots of TG2 and TG3.     

Behavioral olfactory discrimination of mixtures in the spiny lobster (Panulirus argus) based on a habituation paradigm

A habituation paradigm was used to examine behavioral aspectsof discrimination of stimulus quality in olfaction in the spinylobster (Panulirus argus). Magnitude of search response to twoconcentrations of artificial mixtures of crab, oyster, mulletand shrimp and to artificial seawater was measured in five lobstersbefore and immediately after habituation to crab mixture. Habituationto crab mixture was accomplished through 2-min presentationsof 5 ml of alternating concentrations (0.05 and 0.5 mM) of crabmixture stimulus, repeated every 5 min for a total durationof at least 3 h. This procedure resulted in at least a 42% decreasein response to any mixture, but the decrease was greatest forcrab mixture, the habituating stimulus. A habituation index,measured as post-habituation response relative to pre-habituationresponse, was used to evaluate discrimination between crab andeach of the other three mixtures. The habituation index wassignificantly greater for crab (90%) than for oyster (49%) andfor mullet (47%) mixtures. The habituation index for shrimpmixture (65%) was intermediate to these three mixtures. Thus,shrimp mixture is perceived by lobsters as being more similarto crab mixture than is either oyster or mullet mixture. Thesepatterns of discrimination parallel those reported for associativelyconditioned lobsters (Fine-Levy et al., 1987, 1988) and fora population of olfactory receptor cells (Girardot and Derby,1988).     

Sensitization and habituation of the swimming behavior in ascidian larvae to light

Ascidian larvae of Ciona intestinalis change their photic behavior during the course of development. Newly hatched larvae show no response to a light stimulus at any intensity. At 4 hr after hatching, larvae were induced to start to swimming upon the cessation of illumination, and to stop swimming upon the onset of illumination. At a weaker light intensity (5.0 x 10(-3) J/m (2).s), the larvae showed similar responses to either a single stimulus or repeated stimuli of onset and cessation of light until 10 hr after hatching. At a stronger light intensity (3.2 x 10(-1) J/m(2).s), when the stimulus was repeated, they showed sensitization and habituation of the swimming response. At 3 hr after hatching the larvae failed to show any response to an initial stimulus at any intensity of light, but after several repeated stimuli (sensitization) they showed a swimming response at light intensities above 4.0 x 10(-2) J/m (2).s. At 5 hr and with intensity above 1.0 x 10 (-2) J/m(2).s, the larvae showed photoresponses to the first stimulus, but after several repetitions the larvae failed to stop swimming upon the onset of light (habituation). A repeated series of stimuli at stronger intensities of light caused greater habituation; this habituation was retained for about 1 min. Since the larval central nervous system in Ciona is comprised of only about 100 neurons, learning behavior in ascidian larvae should provide insights for a minimal mechanism of memory in vertebrates.     

Interrelationship between grape snail alimentary and defense behavior command neurons]

Food stimulus (carrot juice), releasing feeding behaviour in intact snails, evoked spike discharges in giant meta-erebral cells (considered to be command neurones of feeding behaviour) and subthreshold EPSPs in giant parietal cells (command neurones of avoidance behaviour) of a half-intact preparation. Tactile stimulation, eliciting avoidance reactions in intact snails, evoked hyperpolarization in command neurones of feeding behaviour and a spike discharge in command neurones of avoidance behaviour. Spikes induced into either of command neurones produced no changes in activity of other command cells. Inhibition of command neurones of feeding behaviour is assumed to be the basis of behavioural choice when food and tactile stimulus are presented simultaneously.     

Fast habituation of the long-latency auditory evoked potential in the awake albino rat

Fast habituation of the long-latency, vertex-recorded auditory evoked potential (AEP) peaks in humans was first described by Callaway (1973) as a reduction in AEP amplitude that occurs to the second of a pair of acoustic stimuli when both stimuli are presented with an interstimulus interval (ISI) of no more than 10 sec. When acoustic stimuli are presented in pairs with an ISI of 2 sec and an interpair interval (IPI) of approximately 10 sec, reduction in amplitude to the second tone occurs by as much as 30–50%. Fast habituation may depend somewhat on a subject's anticipation of the stimulus and on other factors related to attention and orienting. Studies in our laboratory have demonstrated this amplitude decrement to the second tone of a pair in human infants, children and adults and have explored the implications of this finding with respect to attentional processes and the allocation of cerebral resources. In the present investigation we describe an animal model of fast habituation. Here, vertex-recorded AEPs were obtained to paired tone stimuli delivered to awake adult male Sprague-Dawley rats chronically implanted with skull electrodes. Findings showed: (a) an AEP wave form with 8 distinct peaks, (b) for one component there was a marked decrement in amplitude from tone 1 to tone 2 in recordings obtained from an electrode placed slightly to the right of midline, and (c) that there were no significant differences in peak latencies across tones. This methodology may further our understanding of fast habituation in humans and may prove useful for studies of attention, orienting, and resource allocation using techniques that are not possible for use with human subjects.     

Temperature dependent plasticity of habituation in the crayfish

To determine the effects of thermal preconditioning on a simple form of learning and memory, habituation, we preconditioned crayfish with extreme temperatures and subsequently analysed their effects on mechanosensory input that evokes a response in the lateral giant interneurons, within the normal temperature range of the animal. We found that repetitive stimulation with a 1 s interstimulus interval led to habituation of the response the lateral giant in control animals at 22°C. Neither heat nor cold preconditioning had any effect on the probability of evoking a response in the lateral giant nor on the rate at which habituation occurred. With a 1 min interstimulus interval, however, the rate of habituation of the lateral giant in the heat-preconditioned group was less than either the control or cold-preconditioned animals. The effect of heat or cold pre-exposure was specific to the input to the lateral giant at control temperatures. For example, at 22°C prior heat and cold preconditioning had no effect on spontaneous reductor motor neurone activity. They did, however, provide thermoprotection at extreme temperatures, with the probability of spontaneous activity higher in the cold-preconditioned group at low temperatures but higher in the heat-preconditioned group at higher temperatures.     

Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon of aplysia

The siphon withdrawal response evoked by a weak tactile (water drop) or light stimulus is mediated primarily by neurons in the siphon. Central neurons (abdominal ganglion) contribute very little since the response amplitude and latency are not changed following removal of the abdominal ganglion. Similarly, habituation and dishabituation of this withdrawal response are not different after removal of the abdominal ganglion, indicating that the peripheral neural circuit in the isolated siphon can mediate habituation itself, and thus has many of the properties attributed to central neurons. Responses evoked by electrical stimulation of the siphon nerve habituate, depending upon the stimulus intensity and interval. These habituated responses may be dishabituated by tactile or light stimulation of the siphon. These results show that each neural system, peripheral and central, has an excitatory modulatory influence on the other. Normally adaptive siphon responses must be shaped by the integrated activity of both of these neural systems.     

Habituation and dishabituation mediated by the peripheral and central neural circuits of the siphon of Aplysia.

The siphon withdrawal response evoked by a weak tactile (water drop) or light stimulus is mediated primarily by neurons in the siphon. Central neurons (abdominal ganglion) contribute very little since the response amplitude and latency are not changed following removal of the abdominal ganglion. Similarly, habituation and dishabituation of this withdrawal response are not different after removal of the abdominal ganglion, indicating that the peripheral neural circuit in the isolated siphon can mediate habituation itself, and thus has many of the properties attributed to central neurons. Response evoked by electrical stimulation of the siphon nerve habituate, depending upon the stimulus intensity and interval. These habituated responses may be dishabituated by tactile or light stimulation of the siphon. These results show that each neural system, peripheral and central, has an excitatory modulatory influence on the other. Normally adaptive siphon responses must be shaped by the integrated activity of both of these neural systems.     

A feedforward model of suppressive and facilitatory habituation effects

 Simple exposure to repeatitive stimulation is known to induce short-term learning effects across a wide range of species. These effects can be both suppressive and facilitatory depending on stimulus conditions: repeatitive presentation of a weak stimulus decreases the strength of the response (habituation), whereas presentation of a tonic stimulus following a series of weak stimuli transiently increases the response strength (dishabituation). Although these phenomena have been comprehensively characterized at both behavioral and cellular levels, most existing models of nonassociative learning focus exclusively on the suppressive or facilitatory changes in response, and do not attempt to relate cellular events to behavior. I propose here a feedforward model of habituation effects that explains both suppressive and facilitatory changes in response relying on the interaction between excitatory and inhibitory processes that develop in parallel on two different timescales. The model's properties are used to explain the rate sensitivity property of habituation and recovery and stimulus dishabituation. Received: 1 June 2001 / Accepted in revised form: 4 December 2001