Responses of high-frequency movement detector neurons in dragonfly larvae to motion of single objects

Neurons of the class described respond by a discharge with a frequency of 150–250/sec to motion of single objects in a large receptive field. The response depends directly on the size of the object. The neurons are selectively sensitive to motion of dark objects. Widening a dark border (bringing a black disc closer) evokes a stronger response than narrowing a dark border (moving a white disc further away). The response to uniform movement consists of high-frequency volleys of discharges separated by pauses. Repeated movements along the same trajectory induce habituation; after cessation of the movements sensitivity is restored with a time constant of about 30 sec. The role of lateral inhibition and local habituation in the identification of the specific features of optical stimuli is discussed.     

A comparison of the effects of testosterone on aggressive responses by the domestic chick to the human hand and to a large sphere

In young male chicks a single injection of testosterone oenanthate leads to a long-lasting facilitation of behaviour patterns related to adult attack, courtship and copulation. The same responses, in particular facilitated pecking, may be evoked, with a similar time course of facilitation and subsequent waning, by a human hand or a white featureless sphere. The dose-response curve to the androgen is also similar for these two objects. A very simple stimulus thus appears to be capable of evoking at least one major component of aggressive behaviour, as well as other responses normally directed to conspecifics. Pecking of the sphere increases within 4–7 h of a second injection of the androgen, given after facilitation due to the first has disappeared, whereas the first requires 48–72 h to become effective. This rapid effect is not dependent on the age of the animal, nor on prior experience of pecking the sphere—indeed this causes marked habituation of all response to the sphere, whether or not response is facilitated by testosterone during the initial experience. It appears to result from central ‘priming’, perhaps by a process similar to the reversal of refractoriness to central androgen implants by prior systemic priming with testosterone, which has been previously reported for adult castrates.     

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.     

Minireview: Cholinergic and monoaminergic substrates of startle habituation

Research is reviewed arising from the proposition that behavioral habituation is mediated by brain mechanisms operated by the neurotransmitter, acetylcholine. Effects of cholinergic drugs on habituation of the startle response in rats fail to support involvement of acetylcholine. Likewise, serotonergic drug effects do not favor the more recent view that startle habituation depends on brain serotonin, nor is there sufficient evidence for an essential role of either dopamine or noradrenalin. Because of persistence of habituation following challenge with a variety of pharmacological agents, the phenomenon probably depends upon a complex interplay between a number of transmitters and behavioral processes. Contrary to earlier belief, no single transmitter should be seen as crucially responsible for startle habituation.     

Short-term and long-term habituation of exploration in rats,hamsters and gerbils

Short-term (within-session) and long-term (between-session) habituation of exploratory behavior was studied in rats, hamsters and gerbils. Subjects were observed in an open field containing four different objects during three 15-min sessions with an 8–14 h interval between each session. Their exploratory activity was measured by the numbers of contacts they made with these objects. The three species differed from each other in both their long-term and short-term habituation of exploration. Rats showed disrupted between-session habituation because of an important initial burst of activity at the beginning of each session. In contrast, hamsters and gerbils displayed between-session habituation, but within-session habituation occured during the first session only. These results are discussed in relation both to the adaptive value of exploration, and to the natural habitat of each species.     

Habituation Is More Than Learning to Ignore: Multiple Mechanisms Serve to Facilitate Shifts in Behavioral Strategy

Recent work indicates that there are distinct response habituation mechanisms that can be recruited by different stimulation rates and that can underlie different components (e.g., the duration or speed) of a single behavioral response. These findings raise the question: why is “the simplest form of learning” so complicated mechanistically? Beyond evolutionary selection for robustness of plasticity in learning to ignore, it is proposed in this article that multiple mechanisms of habituation have evolved to streamline shifts in ongoing behavioral strategy. Then, speculations are offered regarding the implications of this reconceptualization of habituation for approaching the analysis of mechanisms of more complex forms of learning and memory.     

Integration of auditory and visual information about objects in superior temporal sulcus

Two categories of objects in the environment-animals and man-made manipulable objects (tools)-are easily recognized by either their auditory or visual features. Although these features differ across modalities, the brain integrates them into a coherent percept. In three separate fMRI experiments, posterior superior temporal sulcus and middle temporal gyrus (pSTS/MTG) fulfilled objective criteria for an integration site. pSTS/MTG showed signal increases in response to either auditory or visual stimuli and responded more to auditory or visual objects than to meaningless (but complex) control stimuli. pSTS/MTG showed an enhanced response when auditory and visual object features were presented together, relative to presentation in a single modality. Finally, pSTS/MTG responded more to object identification than to other components of the behavioral task. We suggest that pSTS/MTG is specialized for integrating different types of information both within modalities (e.g., visual form, visual motion) and across modalities (auditory and visual).     

On the Generalization of Habituation: How Discrete Biological Systems Respond to Repetitive Stimuli

Habituation, a form of non‐associative learning, isno longer studied exclusively within the fields of psychology and neuroscience. Indeed, the same stimulus–response pattern is observed at the molecular, cellular, and organismal scales and is not dependent upon the presence of neurons. Hence, a more inclusive theory is required to accommodate aneural forms of habituation. Here an abstraction of the habituation process that does not rely upon particular biological pathways or substrates is presented. Instead, five generalizable elements that define the habituation process are operationalized. The formulation can be applied to interrogate systems as they respond to several stimulation paradigms, providing new insights and supporting existing behavioral data. The model can be used to deduce the relative contribution of elements that contribute to the measurable output of the system. The results suggest that habituation serves as a general biological strategy that any system can implement to adaptively respond to harmless, repetitive stimuli.     

The habituation of event-related potentials to speech sounds and tones

We examined the short- and long-term habituation of auditory event-related potentials (ERPs) elicited by tones, complex tones and digitized speech sounds (vowels and consonant-vowel-consonant syllables). Twelve different stimuli equated in loudness and duration (300 msec) were studied. To examine short-term habituation stimuli were presented in trains of 6 with interstimulus intervals of 0.5 or 1.0 sec. The first 4 stimuli in a train were identical standards. On 50% of the trains the standard in the 5th position was replaced by a deviant probe stimulus, and on 20% of the trains the standard in the 6th position was replaced by a target, a truncated standard that required a speeded button press response.Short-term habituation (STH) was complete by the third stimulus in the train and resulted in amplitude decrements of 50–75% for the N1 component. STH was partially stimulus specific in that amplitudes were larger following deviant stimuli in the 5th position than following standards. STH of the N1 was more marked for speech sounds than for loudness-matched tones or complex tones at short ISI. In addition, standard and deviant stimuli that differed in phonetic structure showed more cross-habituation than did tones or complex tones that differed in frequency. This pattern of results suggests that STH is a function of the acoustic resemblance of successive stimuli.The long-term habituation (LTH) of the ERP was studied by comparing amplitudes across balanced 5.25 m stimulus blocks over the course of the experiment. Two types of LTH were observed. The N1 showed stimulus-specific LTH in that N1 amplitudes declined during the presentation of a stimulus, but returned to control levels when a different stimulus was presented in the subsequent condition. In contrast, the P3 elicited by the deviant stimuli showed non-specific LTH, being reduced across successive blocks containing different stimuli. P3s elicited by target stimuli remained stable in amplitude.     

Tests of the limiting visual resolution of the DCMD system of the lubber grasshopper to rectangular gratings

Visual acuity measurements using the descending contralateral movement detector (DCMD) neuron in the lubber grasshopper, Romalea microptera, show responses to spatial angles as small as 0.3°. Moving, black-white striped objects were viewed on a rear-projection screen.Nonuniformity and spatial sub-harmonic measurements of the object patterns showed that any artifacts which were present were below the resolution limits of the human visual system (and presumably that of Romalea).Nonstationarity in the responses of the DCMD system can be categorized as long-term (sensitivity changes) and short term (habituation). A mathematical model for habituation is used to illustrate how confidence in responses may be lost due to the incorporation of too many samples of habituated data.     

Designating Seasonality Using Rate of Movement

ABSTRACT Traditionally, seasons for animals have been designated based on single external variables such as climate or plant phenology, rather than an animal's response to the dynamic environments within which it lives. By interpreting a rate of movement function of cumulative movement through time we established a method that distinguishes transitions between behaviors limited by winter habitat conditions from those present during summer. Identification of these time periods provides temporal definition to subsequent home-range analyses and use-availability comparisons. We used location data from 32 Global Positioning System-collared female moose (Alces alces) to demonstrate the method. We used model selection (Akaike's Information Criterion) to differentiate between candidate rate of movement response curves. Of 32 moose, 29 clearly conformed to an annual movement pattern described by a logistic curve, with increased rates of movement in summer compared to winter. Conversely, 3 aberrant individuals did not alter their movement rate through the year and were best fit with a linear response curve. The seasonal rate of movement model we developed suggests an average summer period of 122 days (median = 119 days, range = 96–173 days) for moose in northwestern Ontario, Canada. The rate of movement model we applied to individuals indicated 1 May as the median date for the winter-summer transition (range = 2 Apr–24 May), and the median transition from summer to winter was 25 August (range = 1 Aug–23 Oct). Wide variation in timing and duration of summer and winter seasons among individuals demonstrates potential failure of the single external variable approach to capture the suite of factors potentially influencing animal behaviors. By plotting cumulative distance moved throughout the year, we elucidated individual variation in response to known and unknown variables that affect animal movement. Accounting for variability among individuals in designation of biologically significant temporal boundaries is critical to delineation of seasonally important habitats for conservation and sustainability of healthy wildlife populations.     

Stabilisation of walking by intrinsic muscle properties revealed in a three-dimensional muscle-driven simulation

A fundamental question in movement science is how humans perform stable movements in the presence of disturbances such as contact with objects. It remains unclear how the nervous system, with delayed responses to disturbances, maintains the stability of complex movements. We hypothesised that intrinsic muscle properties (i.e. the force–length–velocity properties of muscle fibres and tendon elasticity) may help stabilise human walking by responding instantaneously to a disturbance and providing forces that help maintain the movement trajectory. To investigate this issue, we generated a 3D muscle-driven simulation of walking and analysed the changes in the simulation's motion when a disturbance was applied to models with and without intrinsic muscle properties. Removing the intrinsic properties reduced the stability; this was true when the disturbing force was applied at a variety of times and in different directions. Thus, intrinsic muscle properties play a unique role in stabilising walking, complementing the delayed response of the central nervous system.     

Comparison of electrical thresholds for evoking movements from sensori-motor areas of the cat cerebral cortex and its relation to motor training

Motor maps and electrical thresholds for evoking movements from motor areas of the cerebral cortex were evaluated in normal cats by using intracortical microstimulation techniques. Stainless steel chambers were implanted over craniotomies in adult cats trained to perform reaching and retrieval movements with their forelimbs. Prehensile motor training was continued and movement performance monitored for about 6–10 weeks during which the cortex was progressively explored with sharp tungsten electrodes inserted into cortical gyri (anterior and posterior sigmoid, and coronal) and the banks of sulci (cruciate, presylvian and coronal). Twice weekly, under light general anaesthesia, 3–4 tracks were made in either hemisphere till about 50 tracks were made in each hemisphere. Mean thresholds for evoking forelimb movements from different cytoarchitectonic areas (4γ, 4δ, 6aγ and 3a) were compared and no consistent or significant differences were observed between the different areas. In the animals (4/6) which used either forelimb to perform the tasks, there were no consistent differences in the mean thresholds for evoking forelimb movements from the two hemispheres. However, in 2 animals, which used their right forelimbs predominantly or exclusively to perform all the tasks, mean thresholds for evoking forelimb movements was significantly higher in areas 4γ and 6aγ of the left hemisphere (compared to the right); no consistent differences in the mean thresholds for evoking hindlimb or facial movements were observed between the two hemispheres. These findings suggest that ICMS thresholds for evoking forelimb movements may be similar in different sensorimotor areas of the cat cerebral cortex, and these thresholds could be influenced by motor training.     

Neural correlates of habituation of the proleg withdrawal reflex in larvae of the hawk moth, Manduca sexta

The larval proleg withdrawal reflex of the hawk moth, Manduca sexta, exhibits robust habituation. This reflex is evoked by deflecting one or more mechanosensory planta hairs on a proleg tip. We examined neural correlates of habituation in an isolated proleg preparation consisting of one proleg and its segmental ganglion. Repeated deflection of a single planta hair caused a significant decrease in the number of action potentials evoked in the proleg motor nerve (which carries the axons of proleg retractor motor neurons). Significant response decrement was seen for interstimulus intervals of 10 s, 60 s and 5 min. Response decrement failed to occur in the absence of repetitive stimulation, the decremented response recovered spontaneously following a rest, and electrical stimulation of a body wall nerve facilitated the decremented response (a neural correlate of dishabituation). Adaptation of sensory neuron responses occurred during repeated hair deflections. However, when adaptation was eliminated by direct electrical stimulation of sensory neurons, the response in the proleg motor nerve still decreased significantly. Muscle recordings indicated that the response of an identified proleg retractor motor neuron decreased significantly during habituation training. Thus, habituation of the proleg withdrawal reflex includes a central component that is apparent at the level of a single motor neuron. Accepted: 20 December 1996     

High-throughput behavioral analysis in C. elegans

We designed a real-time computer vision system, the Multi-Worm Tracker (MWT), which can simultaneously quantify the behavior of dozens of Caenorhabditis elegans on a Petri plate at video rates. We examined three traditional behavioral paradigms using this system: spontaneous movement on food, where the behavior changes over tens of minutes; chemotaxis, where turning events must be detected accurately to determine strategy; and habituation of response to tap, where the response is stochastic and changes over time. In each case, manual analysis or automated single-worm tracking would be tedious and time-consuming, but the MWT system allowed rapid quantification of behavior with minimal human effort. Thus, this system will enable large-scale forward and reverse genetic screens for complex behaviors.     

Image Analysis of Geo-Induced Inhibition, Compression, and Promotion of Growth in an Inverted Helianthus annuus L. Seedling

The growth responses of a sunflower seedling (Helianthus annuus L.), subjected to repeated inversion, were characterized by time-lapse recording in conjunction with video image analysis. The investigation revealed a characteristic response pattern and established that the directional movement of the seedling is achieved by both inhibition and stimulation of growth in the normal growing regions. The complex growth changes in contiguous regions of the hypocotyl are such as seem to be inexplicable in terms of an environmentally imposed gradient of a single growth substance.     

Dynamic characteristics of the auditory cortex of guinea pigs observed with multichannel optical recording

The spatiotemporal characteristics of neural activity in the guinea pig auditory cortex are investigated to determine their importance in neural processing and coding of the complex sounds. A multi-channel optical recording system has been developed for observing the cortical field of the mammalian brain in vivo. Using the voltage-sensitive dye: RH795, optical imaging was used to visualize neural activity in the guinea pig auditory cortex. Experimental results reveal a boomerang-shaped pattern of movement of activated neural cell regions for the evoked response to click as complex sounds. Parallel and sequential neural processing structure was observed. Although the exact frequency selectivities of single cells and tonotopical organization observed using microelectrode were not visible, the similar feature to the microelectrode evidences was imaged by extracting the strongly response field from the optical data.     

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     

How does the toad's visual system discriminate different worm-like stimuli?

Behavioral experiments show that toads exhibit stimulus- and locus-specific habituation. Different worm-like stimuli that toads can discriminate at a certain visual location form a dishabituation hierarchy. What is the neural mechanism which underlies these behaviors? This paper proposes that the toad discriminates visual objects based on temporal responses, and that discrimination is reflected in different average neuronal firing rates at some higher visual center, hypothetically anterior thalamus. This theory is developed through a large-scale neural simulation which includes retina, tectum and anterior thalamus. The neural model based on this theory predicts that retinal R2 cells play a primary role in the discrimination via tectal small pear cells (SP) and R3 cells refine the feature analysis by inhibition. The simulation demonstrates that the retinal response to the trailing edge of a stimulus is as crucial for pattern discrimination as the response to the leading edge. The new dishabituation hierarchies predicted by this model by reversing contrast and shrinking stimulus size need to be tested experimentally.     

Greater Physiological and Behavioral Effects of Interrupted Stress Pattern Compared to Daily Restraint Stress in Rats

Repeated stress can trigger a range of psychiatric disorders, including anxiety. The propensity to develop abnormal behaviors after repeated stress is related to the severity, frequency and number of stressors. However, the pattern of stress exposure may contribute to the impact of stress. In addition, the anxiogenic nature of repeated stress exposure can be moderated by the degree of coping that occurs, and can be reflected in homotypic habituation to the repeated stress. However, expectations are not clear when a pattern of stress presentation is utilized that diminishes habituation. The purpose of these experiments is to test whether interrupted stress exposure decreases homotypic habituation and leads to greater effects on anxiety-like behavior in adult male rats. We found that repeated interrupted restraint stress resulted in less overall homotypic habituation compared to repeated daily restraint stress. This was demonstrated by greater production of fecal boli and greater corticosterone response to restraint. Furthermore, interrupted restraint stress resulted in a lower body weight and greater adrenal gland weight than daily restraint stress, and greater anxiety-like behavior in the elevated plus maze. Control experiments demonstrated that these effects of the interrupted pattern could not be explained by differences in the total number of stress exposures, differences in the total number of days that the stress periods encompased, nor could it be explained as a result of only the stress exposures after an interruption from stress. These experiments demonstrate that the pattern of stress exposure is a significant determinant of the effects of repeated stress, and that interrupted stress exposure that decreases habituation can have larger effects than a greater number of daily stress exposures. Differences in the pattern of stress exposure are therefore an important factor to consider when predicting the severity of the effects of repeated stress on psychiatric disorders.