Lateralization and unilateral transfer of spatial memory in marsh tits: are two eyes better than one?

Two previous experiments on food storing and one-trial associative learning in marsh tits (Clayton 1992a; Clayton and Krebs 1992) demonstrate that information coming into the brain from the left eye disappears from the left eye system between 3 and 24 h after memory formation, whereas that coming into the brain from the right eye remains stable within the right eye system for at least 51 h after memory formation. Performance after a 7 h retention interval appears to represent an intermediate stage in which the information is no longer accessible to the left eye system but is not yet available to the right eye system, suggesting a unilateral transfer of memory. The experiments reported here further investigated lateralization and unilateral transfer of memory in food-storing marsh tits, Parus palustris, using the technique of monocular occlusion. Birds were tested for their ability to retrieve stored seeds after retention intervals of 3, 7 and 24 h under 4 different occlusion treatments. Two predictions were tested: (a) with right eye occlusion during storage, birds should show better memory performance after 3 and 24 h than after 7 h and (b) memory should be more accurate when both eyes are used during storage than with monocular occlusion. The first prediction, which arises from the fact that memory is transferred from the left to the right eye system at about 7 h and is inaccessible during the transfer, was supported by the data. The second prediction, however, was not supported. Previous work has shown that in marsh tits the two eye systems remember preferentially different aspects of the stimulus: the left eye system responds to spatial position and the right eye system to object-specific cues. It is possible that the failure to find superior performance in binocular tests was because the task could be solved by either spatial or object-specific memory.     

Habituation of mechanoreceptive interneurons in the crayfish

The effect of repetition of sensory stimuli was studied on the responses of mechanoreceptive interneurons in the optic tract of the crayfish (Procambarus bouvieri (Ortmann)). The number of spikes recorded from a given unit gradually decreased during a train of stimuli. The decrease showed a negative exponential time course, with a curvature dependent upon the frequency of stimulation, the intensity of stimuli, and the hour of the day. Habituation is selective for the intensity and rate of stimulation, and the particular spot of receptive field stimulated. Locomotor excitation results in a dimminution of the rate of decay. The effect of a single train of stimuli when leading to pronounced habituation may persist for periods longer than 24 hr.     

Modifications of acoustic habituation by interruption of visual input in quipazine treated cats

The influence of interruption of the visual input on acoustic habituation was studied in cats before and following the administration of quipazine, 3 mg/kg iv. The characteristics of acoustic habituation were analyzed through the magnitude and temporal course of multiunit activity (MUA) responses elicited in the mesencephalic reticular formation (MRF) by repetitive acoustic stimuli (70 db, 50 Hz trains of 2 sec duration) in 6 freely moving cats with cortical electrodes over the parietal cortex and bipolar electrodes chronically implanted in MRF and basolateral amygdala (AMN). The cats were submitted to repetitive acoustic stimulation during one 30 min period before, and three 30 min periods after drug administration in the following conditions: a) with unmasked eyes; b) with masked eyes by means of dark contact lenses. Persistent attentive behavior, catatonic attitudes, hypersynchronous (6 Hz, 100-150 microV) EEG activity and significant increase of spontaneous MUA in FRM and AMN were induced by quipazine both in the cats tested with unmasked and with masked eyes. This increase of MUA was higher immediately following drug administration and progressively decreased, although MUA values remained significantly higher than controls 110 min after quipazine administration. Acoustic habituation, evidenced through the progressive decrease of MUA responses of MRF to acoustic stimuli, was observed before quipazine administration when the cats were tested with unmasked and with masked eyes; as well as in cats tested with unmasked eyes following drug administration. However, the MUA responses to acoustic stimuli did not decrease in cats with masked eyes during acoustic stimulation periods 0-30 min and 40-70 min after quipazine administration.(ABSTRACT TRUNCATED AT 250 WORDS)     

Habituation and associative learning during exploratory behavior of the crab Chasmagnathus

Summary Chasmagnathus crabs placed in a choice-chamber device (a dark compartment, DC, and a light one, LC, of identical size separated by a central partition with a sliding door) display an exploratory activity that declines over time (training session). Such decrement persists at the testing session, 24 h later, and meets the criterion of stimulus specificity, so that it is accounted for in terms of a long-term habituation. Alternative explanations involving far-reaching effects of handling, change of context or isolation during the training session, are excluded. If animals are allowed to find food in LC during training, no decrease in the exploratory activity is shown and the enhanced effect on exploring is retained for at least 24 h. This result is interpreted as an instance of associative learning, appetitively motivated. Performances are analysed measuring the latencies to pass from DC to LC, so that crabs given food in training show in testing shorter latencies than controls. In addition, unlike controls, trained crabs often display at testing a feeding behavior despite the absence of food or odor of food in the choice-chamber. The possible use of both exploratory habituation and appetitive learning in studies on memory modulation is discussed.     

Habituation of sexual response in male Heliothis moths

It has been generally hypothesized that habituation mediates the effects of pheromone‐based disruption strategies used in the management of moth pests. The current study demonstrates that pheromone‐mediated sexual response in the tobacco budworm moth, Heliothis virescens (F.) (Lepidoptera: Noctuidae), can in fact be modulated by conditions consistent with the production of habituation. An ethogram was used to measure response strength in a wind tunnel experiment where male moths were allowed to respond freely to one of two different blends of female pheromone in 16 trials over 4 days. Post‐test measures were collected to investigate stimulus specificity and long‐term effects. In conditions appropriate to the formation of habituation, habituation will develop and disrupt male sexual response to female sex pheromone. Males repeatedly exposed to plumes of synthetic pheromone blends display a habituated response lasting up to 96 h. Habituation rate and spontaneous recovery of response strength are greater with less intense stimuli. Additionally, males habituated to one blend express no habituation of sexual response when exposed to a different blend. This indicates a high degree of stimulus specificity, which could facilitate outbreeding, and that moths attend to the configuration of the pheromone blend, not simply to its elements.     

Parallel pathways for habituation in repetitively stimulated PC12 cells

Habituation was investigated in neuronally differentiated PC12 cells by measuring the decrease in cellular secretion of norepinephrine with repetitive stimulation by either membrane depolarization or acetylcholine. When these two types of repetitive stimulation were applied to the same cells, habituation occurred independently to each, showing that two pathways for habituation can be utilized simultaneously in single cells. The two pathways apparently process stimuli in parallel, without competition between common intermediates.     

Age-related deficits of long-term memory in the crab Chasmagnathus

Short and long-term memory in adult crabs Chasmagnathus granulatus of different age are evaluated in two learning paradigms: habituation to a visual danger stimulus and appetitive conditioning. No difference between young, middle-aged and aged animals is found in short-term habituation with 15 training trials. A good level of retention of the habituated response at 24 h is exhibited by young and middle-aged crabs but a poor one by aged crabs. When the training-to-testing interval is lengthened to 48 h or the training session reduced to 7 trials, young and middle-aged crabs continue to show long-term habituation but aged individuals exhibit no retention at all. As regards appetitive conditioning, young, middle-aged and aged crabs present similar short-term memory with 5 training trials and similar long-term memory when tested at 24 h, but an age-related deficit in long-term retention is exhibited when the intersession interval is lengthened to 48 h or the training reduced to 3 trials. Thus, a reduction of long-term memory related to age is demonstrated in the crab Chasmagnathus. Since it is shown in two different learning paradigms, the possibility of explaining the deficit in terms of a failure in memory mechanisms due to aging rather than as a consequence of ontogenetic shift in the crab's behavior is discussed.     

Long-term retention of behavioural habituation in the rat

The orienting response in rats was measured by the interruption in licking that occurred during the presentation of a tone stimulus. Habituation occurred after a mean of 6·3 presentations and there was complete retention of habituation for 72 hr, and 70 per cent retention after 288 hr. This long-term storage involved in habituation distinguishes it from fatigue and supports the view that it must be regarded as a type of learning.     

Transfer of habituation between stimulation sites of the siphon withdrawal reflex in Aplysia californica

Habituation of the siphon withdrawal reflex (SWR) can be evoked by iterative tactile stimuli presented to one of several sites, including the siphon and gill. The SWR evoked at an arbitrary "test" site did not habituate when stimuli were presented at 20-min intervals. However, there was a large decrease in the reflex evoked at the test site when the trial was preceded by 10 repetitive stimuli (interstimuli interval = 30 s) presented to the opposite "habituation" site. Transfer of habituation occurred from gill to siphon stimulation sites, and vice versa. There was a concomitant decrease in the excitatory input evoked in the central siphon motor neurons LDS1 and LDS3. Moreover, transfer of habituation occurred after the abdominal ganglion (central nervous system) was removed. There was little change in the magnitude of the control responses or transfer of habituation after deganglionation. Since transfer of habituation between stimulation sites of the SWR was similar to that reported previously for the gill withdrawal reflex, it was suggested that a common mechanism may underlie the two behaviors.     

Memory for the location of stored food in marsh tits

Marsh tits store several hundred food items per day, in separate locations within their territory, and recover most items within 24 h. Experiments in the laboratory determined that marsh tits return accurately to the sites of stored sunflower seeds 3 h and 24 h after storage. The proportion of returns exceeded chance encounter and initial preferences for those sites. The lack of interocular transfer in birds for some visual tasks provided a test for the hypothesis that memory is used to relocate stored food. After storing food with one eye covered, marsh tits did not return to storage sites when using only the ‘naive’ eye, but did so when using only the eye uncovered during storage. It seems likely that recovery of stored food by marsh tits and other birds occurs by memory of storage sites, not by chance encounter during foraging.     

Non-associative learning and anxiety in rats treated with a single systemic administration of the gastrin-releasing peptide receptor antagonist RC-3095

The gastrin-releasing peptide receptor (GRPR) has been implicated in the modulation of emotionally-motivated memory. In the present study, we investigated the role of the GRPR on non-emotional, non-associative memory, and anxiety. Adult male Wistar rats were given a systemic injection of the GRPR antagonist [D-Tpi⁶, Leu¹³ psi(CH₂NH)-Leu¹⁴] bombesin (6–14) (RC-3095) (0.2, 1.0 or 5.0 mg/kg) 30 min before exposure to an open field or an elevated plus maze. Habituation to the open field was tested in a retention trial carried out 24 h after the first exposure to the open field. Rats given RC-3095 at the doses of 1.0 or 5.0 mg/kg showed impaired habituation. Animals treated with 5.0 mg/kg of RC-3095 spent significantly more time in the closed arms of the elevated plus maze. No effects of RC-3095 on locomotion or exploratory behavior were observed. The results implicate the GRPR in the regulation of non-emotional, non-associative memory as well as in anxiety.     

Habituation of postsynaptic unit responses of the cat motor cortex to stimuli of different modalities

Habituation (extinction) of postsynaptic unit responses of the cat motor cortex to repetitive electrodermal, photic, acoustic, and combined bimodal stimulation was investigated by intracellular recording. Habituation was shown by a decrease in the number of spikes per grouped discharge and a decrease in the amplitude and duration of the EPSPs, and sometimes IPSPs, on repetition of the stimulus. The way in which the course of habituation depends on the modality and duration of stimulation (at a constant frequency of 1/sec) is examined. Habituation of postsynaptic responses to sensory stimuli is observed with neurons of different functional groups, namely identified neurons of pyramidal tract and unidentified neurons, some of which were evidently pyramidal neurons and interneurons. The hypothesis is put forward that the habituation of PSPs of the cortical neurons is based on processes taking place mainly at the subcortical level.A. A. Zhdanov Leningrad State University. Translated from Neirofiziologiya, Vol. 4, No. 5, pp. 545–553, September–October, 1972.     

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.     

Habituation of mechanoreceptive interneurons in the crayfish.

The effect of repetition of sensory stimuli was studied on the responses of mechanoreceptive interneurons in the optic tract of the crayfish (Procambarus bouvieri (Ortmann)). The number of spikes recorded from a given unit gradually decreased during a train of stimuli. The decrease showed a negative exponential time course, with a curvature dependent upon the frequency of stimulation, the intensity of stimuli, and the hour of the day. Habituation is selective for the intensity and rate of stimulation, and the particular spot of receptive field stimulated. Locomotor excitation results in a dimminution of the rate of decay. The effect of a single train of stimuli when leading to pronounced habituation may persist for periods longer than 24 hr.     

High stimulus specificity characterizes anti-predator habituation under natural conditions

Habituation is one of the most fundamental learning processes that allow animals to adapt to dynamic environments. It is ubiquitous and often thought of as a simple form of non-associative learning. Very little is known, though, about the rules that govern habituation and their significance under natural conditions. Questions about how animals incorporate habituation into their daily behaviour and how they can assure only to habituate to non-relevant stimuli are still unanswered. Animals under threat of predation should be particularly selective about which stimuli they habituate to, since ignoring a real threat could be fatal. In this study, we tested the response of fiddler crabs, Uca vomeris, to repeatedly approaching dummy predators to find out whether these animals habituate to potential predators and to test the selectivity of the habituation process. The crabs habituated to model predators, even though they were confronted with real predators during the same habituation process. They showed remarkable selectivity towards the stimulus: a simple change in the approach distance of the stimulus led to a recovery in their responses. The results strongly indicate that in the context of predator avoidance, habituation under natural conditions is highly selective and a stimulus is not defined just by its current sensory signature, but also its spatio-temporal history.     

Habituation and prepulse inhibition of acoustic startle in rodents

The acoustic startle response is a protective response, elicited by a sudden and intense acoustic stimulus. Facial and skeletal muscles are activated within a few milliseconds, leading to a whole body flinch in rodents(1). Although startle responses are reflexive responses that can be reliably elicited, they are not stereotypic. They can be modulated by emotions such as fear (fear potentiated startle) and joy (joy attenuated startle), by non-associative learning processes such as habituation and sensitization, and by other sensory stimuli through sensory gating processes (prepulse inhibition), turning startle responses into an excellent tool for assessing emotions, learning, and sensory gating, for review see( 2, 3). The primary pathway mediating startle responses is very short and well described, qualifying startle also as an excellent model for studying the underlying mechanisms for behavioural plasticity on a cellular/molecular level(3). We here describe a method for assessing short-term habituation, long-term habituation and prepulse inhibition of acoustic startle responses in rodents. Habituation describes the decrease of the startle response magnitude upon repeated presentation of the same stimulus. Habituation within a testing session is called short-term habituation (STH) and is reversible upon a period of several minutes without stimulation. Habituation between testing sessions is called long-term habituation (LTH)(4). Habituation is stimulus specific(5). Prepulse inhibition is the attenuation of a startle response by a preceding non-startling sensory stimulus(6). The interval between prepulse and startle stimulus can vary from 6 to up to 2000 ms. The prepulse can be any modality, however, acoustic prepulses are the most commonly used. Habituation is a form of non-associative learning. It can also be viewed as a form of sensory filtering, since it reduces the organisms' response to a non-threatening stimulus. Prepulse inhibition (PPI) was originally developed in human neuropsychiatric research as an operational measure for sensory gating(7). PPI deficits may represent the interface of "psychosis and cognition" as they seem to predict cognitive impairment(8-10). Both habituation and PPI are disrupted in patients suffering from schizophrenia(11), and PPI disruptions have shown to be, at least in some cases, amenable to treatment with mostly atypical antipsychotics(12, 13). However, other mental and neurodegenerative diseases are also accompanied by disruption in habituation and/or PPI, such as autism spectrum disorders (slower habituation), obsessive compulsive disorder, Tourette's syndrome, Huntington's disease, Parkinson's disease, and Alzheimer's Disease (PPI)(11, 14, 15) Dopamine induced PPI deficits are a commonly used animal model for the screening of antipsychotic drugs(16), but PPI deficits can also be induced by many other psychomimetic drugs, environmental modifications and surgical procedures.     

Individual variation in behavioural plasticity: direct and indirect effects of boldness,exploration and sociability on habituation to predators in lizards

Little is known about the factors causing variation in behavioural plasticity and the interplay between personality and plasticity. Habituation to predators is a special case of behavioural plasticity. We investigated the direct and indirect effects of boldness, exploration and sociability traits on the habituation ability of Iberian wall lizards, considering exposure and sex effects. Individual boldness was consistent across several non-habituation contexts, but it did not significantly affect habituation. Exploration had a strong direct effect on habituation, with more exploratory individuals being able to habituate faster than less exploratory ones, probably because of their ability to assess risk better. Individual variation in habituation was also affected by sociability, but this was an indirect effect mediated by exposure to the predator. Less social individuals avoided refuges with conspecific cues, increasing exposure to the predator and eventually habituation. Finally, the direct effects of sex (females habituated faster than males) were opposite to its indirect effects through exposure. We conclude that risk assessment, instead of the proactivity–reactivity gradient usually considered in the literature, can affect behavioural plasticity through complex interactions between direct and indirect effects, including exploratory behaviour, degree of exposure to the predator and sex, which represent novel mechanisms generating inter-individual variation in plasticity.     

Habituation of Salmonella spp. at reduced water activity and its effect on heat tolerance

The effect of habituation at reduced water activity (a(w)) on heat tolerance of Salmonella spp. was investigated. Stationary-phase cells were exposed to a(w) 0.95 in broths containing glucose-fructose, sodium chloride, or glycerol at 21 degrees C for up to a week prior to heat challenge at 54 degrees C. In addition, the effects of different a(w)s and heat challenge temperatures were investigated. Habituation at a(w) 0.95 resulted in increased heat tolerance at 54 degrees C with all solutes tested. The extent of the increase and the optimal habituation time depended on the solute used. Exposure to broths containing glucose-fructose (a(w) 0.95) for 12 h resulted in maximal heat tolerance, with more than a fourfold increase in D(54) values. Cells held for more than 72 h in these conditions, however, became as heat sensitive as nonhabituated populations. Habituation in the presence of sodium chloride or glycerol gave rise to less pronounced but still significant increases in heat tolerance at 54 degrees C, and a shorter incubation time was required to maximize tolerance. The increase in heat tolerance following habituation in broths containing glucose-fructose (a(w) 0.95) was RpoS independent. The presence of chloramphenicol or rifampin during habituation and inactivation did not affect the extent of heat tolerance achieved, suggesting that de novo protein synthesis was probably not necessary. These data highlight the importance of cell prehistory prior to heat inactivation and may have implications for food manufacturers using low-a(w) ingredients.     

CS-US delay does not impair appetitive conditioning in Chasmagnathus

Habituation and appetitive conditioning have been already described in the crab Chasmagnathus. The purpose of this work is to study whether associative learning can be obtained despite a long conditioned stimulus-unconditioned stimulus interval. Results of the first experiment show that the weakening of temporal contiguity does not prevent appetitive conditioning to occur while after a long 4-h delay, conditioning wanes completely. A second experiment was conducted, after one and three days of training respectively, confirming the above results. Though initially neutral the context trace may be still available immediately after training and for the period of two but not after 4:00 h, demonstrating a forward limit for the conditioning window. After 3 days of training, a further decrease in the exploratory activity suggested that a longer training could increase the relative weight of habituation. Conditioning and habituation seem to work as opponent processes in the crab CHASMAGNATHUS GRANULATUS: if habituation training in the box is followed by the administration of reinforcement after a short period of time, appetitive conditioning will take place. However, as this interval is increased, habituation prevails. A persistent effect of the exposure to a given environment that may underlie trace conditioning in this crab is discussed in adaptive terms.