Neurogenetic approaches to habituation and dishabituation in Drosophila

We review work in the major model systems for habituation in Drosophila melanogaster, encompassing several sensory modalities and behavioral contexts: visual (giant fiber escape response, landing response); chemical (proboscis extension reflex, olfactory jump response, locomotory startle response, odor-induced leg response, experience-dependent courtship modification); electric (shock avoidance); and mechanical (leg resistance reflex, cleaning reflex). Each model system shows several of Thompson and Spencer’s [Thompson, R. F., & Spencer, W. A. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychological Review, 73, 16–43] parametric criteria for habituation: spontaneous recovery and dishabituation have been described in almost all of them and dependence of habituation upon stimulus frequency and stimulus intensity in the majority. Stimulus generalization (and conversely, the delineation of stimulus specificity) has given insights into the localization of habituation or the neural architecture underlying sensory processing.The strength of Drosophila for studying habituation is the range of genetic approaches available. Mutations have been used to modify specific neuroanatomical structures, ion channels, elements of synaptic transmission, and second-messenger pathways. rutabaga and dunce, genes of the cAMP signal pathway that have been studied most often in the reviewed experiments, have also been implicated in synaptic plasticity and associative conditioning in Drosophila and other species including mammals. The use of the Gal4/UAS system for targeting gene expression has enabled genetic perturbation of defined sets of neurons. One clear lesson is that a gene may affect habituation differently in different behaviors, depending on the expression, processing, and localization of the gene product in specific circuits. Mutations of specific genes not only provide links between physiology and behavior in the same circuit, but also reveal common mechanisms in different paradigms of behavioral plasticity. The rich repertoire of models for habituation in the fly is an asset for combining a genetic approach with behavioral, anatomical and physiological methods with the promise of a more complete understanding.     

Learning of letter names and sounds and their contribution to word recognition

This study investigated knowledge of letter names and letter sounds, their learning, and their contributions to word recognition. Of 123 preschoolers examined on letter knowledge, 65 underwent training on both letter names and letter sounds in a counterbalanced order. Prior to training, children were more advanced in associating letters with their names than with their sounds and could provide the sound of a letter only if they could name it. However, children learned more easily to associate letters with sounds than with names. Training just on names improved performance on sounds, but the sounds produced were extended (CV) rather than phonemic. Learning sounds facilitated later learning of the same letters' names, but not vice versa. Training either on names or on sounds improved word recognition and explanation of printed words. Results are discussed with reference to cognitive and societal factors affecting letter knowledge acquisition, features of the Hebrew alphabet and orthography, and educational implications.     

Investigating the dynamics of affect: Psychological mechanisms of affective habituation to pleasurable stimuli

Affective habituation (i.e., reductions in stimulus-evoked affective reactions as a result of previous exposure) may serve a functional purpose. However, little is know about the psychological mechanisms underlying this process. To elucidate the characteristics of affective habituation, two experiments that examined affective reactions to repeated exposures of pleasurable stimuli were conducted. Results of these experiments indicated that habituation trajectories are characterized by linear decreases in affect. Results also demonstrated that habituation can be slowed by the introduction of novel stimuli (i.e., “novelty effects”), effects that are dimensional (rather than taxonic) in nature. Experiment 2 demonstrated that habituation is mediated by conceptual rather than perceptual processes. Depressed and anhedonic individuals were not more susceptible to habituation in either experiment. The current findings and previous theorizing suggest that habituation may be an important component of an adaptive affective processing system that promotes effective responses to salient stimuli and prevents compulsive reward-seeking behavior.

Audiovisual matching of lips and non-canonical sounds in 8-month-old infants

Japanese 8-month-olds were tested to investigate the matching of particular lip movements to corresponding non-canonical sounds, namely a bilabial trill (BT) and a whistle (WL). The results showed that the infants succeeded in lip-voice matching for the bilabial trill, whereas they failed to do so for the whistle.     

Fast and unintentional evaluation of emotional sounds: evidence from brief segment ratings and the affective Simon task

In the present study, we raised the question of whether valence information of natural emotional sounds can be extracted rapidly and unintentionally. In a first experiment, we collected explicit valence ratings of brief natural sound segments. Results showed that sound segments of 400 and 600?ms duration—and with some limitation even sound segments as short as 200?ms—are evaluated reliably. In a second experiment, we introduced an auditory version of the affective Simon task to assess automatic (i.e. unintentional and fast) evaluations of sound valence. The pattern of results indicates that affective information of natural emotional sounds can be extracted rapidly (i.e. after a few hundred ms long exposure) and in an unintentional fashion.     

Comparing different kinds of words and word-word relations to test an habituation model of priming

Huber and O'Reilly (2003) proposed that neural habituation exists to solve a temporal parsing problem, minimizing blending between one word and the next when words are visually presented in rapid succession. They developed a neural dynamics habituation model, explaining the finding that short duration primes produce positive priming whereas long duration primes produce negative repetition priming. The model contains three layers of processing, including a visual input layer, an orthographic layer, and a lexical-semantic layer. The predicted effect of prime duration depends both on this assumed representational hierarchy and the assumption that synaptic depression underlies habituation. The current study tested these assumptions by comparing different kinds of words (e.g., words versus non-words) and different kinds of word-word relations (e.g., associative versus repetition). For each experiment, the predictions of the original model were compared to an alternative model with different representational assumptions. Experiment 1 confirmed the prediction that non-words and inverted words require longer prime durations to eliminate positive repetition priming (i.e., a slower transition from positive to negative priming). Experiment 2 confirmed the prediction that associative priming increases and then decreases with increasing prime duration, but remains positive even with long duration primes. Experiment 3 replicated the effects of repetition and associative priming using a within-subjects design and combined these effects by examining target words that were expected to repeat (e.g., viewing the target word ‘BACK' after the prime phrase ‘back to'). These results support the originally assumed representational hierarchy and more generally the role of habituation in temporal parsing and priming.     

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

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

The organization of words and environmental sounds in the second year: Behavioral and electrophysiological evidence

The majority of research examining early auditory‐semantic processing and organization is based on studies of meaningful relations between words and referents. However, a thorough investigation into the fundamental relation between acoustic signals and meaning requires an understanding of how meaning is associated with both lexical and non‐lexical sounds. Indeed, it is unknown how meaningful auditory information that is not lexical (e.g., environmental sounds) is processed and organized in the young brain. To capture the structure of semantic organization for words and environmental sounds, we record event‐related potentials as 20‐month‐olds view images of common nouns (e.g., dog) while hearing words or environmental sounds that match the picture (e.g., “dog” or barking), that are within‐category violations (e.g., “cat” or meowing), or that are between‐category violations (e.g., “pen” or scribbling). Results show both words and environmental sounds exhibit larger negative amplitudes to between‐category violations relative to matches. Unlike words, which show a greater negative response early and consistently to within‐category violations, such an effect for environmental sounds occurs late in semantic processing. Thus, as in adults, the young brain represents semantic relations between words and between environmental sounds, though it more readily differentiates semantically similar words compared to environmental sounds.     

Rate and duration memory of naturalistic sounds

Research has shown that the tempi of familiar songs are remarkably well-remembered with a high degree of accuracy. The goal of the present research was to determine whether this ability generalizes to various types of ecological sounds and, if so, how rate information is encoded into the cognitive system. Across three experiments, participants were familiarized with a set of sounds and later asked to remember the rate of each. Experiment 1 revealed that the inherent rate of sounds is incidentally learned such that subsequent recognition is comparable across both prospective and retrospective paradigms. Experiment 2 confirmed these findings through an adjustment task and further demonstrated that memory for event rate remains highly accurate regardless if attending is initially directed toward a sound's rate and/or pitch qualities. Lastly, Experiment 3 assessed the ability to recognize event rate vs. duration when the two dimensions systematically co-vary with one another and revealed that rate variations influence duration recognition but not vice versa. These overall findings are discussed relative to a framework that emphasizes the role of event structure in time judgment behavior.     

Hearing living symbols and nonliving icons: Category specificities in the cognitive processing of environmental sounds

The neurocognitive processing of environmental sounds and linguistic stimuli shares common semantic resources and can lead to the activation of motor programs for the generation of the passively heard sound or speech. We investigated the extent to which the cognition of environmental sounds, like that of language, relies on symbolic mental representations independent of the acoustic input. In a hierarchical sorting task, we found that evaluation of nonliving sounds is consistently biased toward a focus on acoustical information. However, the evaluation of living sounds focuses spontaneously on sound-independent semantic information, but can rely on acoustical information after exposure to a context consisting of nonliving sounds. We interpret these results as support for a robust iconic processing strategy for nonliving sounds and a flexible symbolic processing strategy for living sounds.     

The reminiscence bump is blind to blindness: Evidence from sound- and odor-evoked autobiographical memory

The reminiscence bump is the disproportionally high reporting of autobiographical memories from adolescence and early adulthood and is typically observed when memories are evoked by cues, such as words, pictures, and sounds. However, when odors are used the bump shifts to early childhood. Although these findings indicate that sensory modality affects the bump, the influence of the individual’s sensory function on the reminiscence bumps is unknown. We examined the reminiscence bumps of sound- and odor-evoked autobiographical memories of early blind and sighted individuals, since early blindness implies considerable effects on sensory experience. Despite differences in sensory experience between blind and sighted individuals, the groups displayed similar age distributions of both sound- and odor-evoked memories. The auditory bump spanned the first two decades of life, whereas the olfactory bump was once again found in early childhood. These results demonstrate that the reminiscence bumps are robust to fundamental differences in sensory experience.     

Learning letter names and sounds: Effects of instruction, letter type, and phonological processing skill

Preschool-age children (N = 58) were randomly assigned to receive instruction in letter names and sounds, letter sounds only, or numbers (control). Multilevel modeling was used to examine letter name and sound learning as a function of instructional condition and characteristics of both letters and children. Specifically, learning was examined in light of letter name structure, whether letter names included cues to their respective sounds, and children’s phonological processing skills. Consistent with past research, children receiving letter name and sound instruction were most likely to learn the sounds of letters whose names included cues to their sounds regardless of phonological processing skills. Only children with higher phonological skills showed a similar effect in the control condition. Practical implications are discussed.     

The long-term effects of mild head injury on short-term memory for visual form, spatial location, and their conjunction in well-functioning university students

Research has suggested the presence of subtle long-term cognitive changes in otherwise well-functioning individuals who have previously sustained a mild head injury (MHI). This paper investigated the long-term effects of MHI on visual, spatial, and visual-spatial short-term memory in well-functioning university students. Sixteen students who reported having sustained a MHI were compared to 16 controls on tests of short-term memory (STM) for abstract polygons in haphazardly arranged locations. The three tests differed only in the requirements for recall (shapes for the visual task, locations for the spatial task, and the shapes in their respective locations for the visual-spatial task). MHI participants were selectively impaired on spatial memory, suggesting that tasks of spatial STM may be more sensitive, compared to tasks of visual STM, to the subtle long-term cognitive changes that may be present after a MHI.     

Behavioral and genetic characterization of habituation using Caenorhabditis elegans

This review surveys the literature that investigates the behavioral characterization and cellular and molecular mechanisms of habituation using the model organism Caenorhabditis elegans. In 1990, C. elegans was first observed to show habituation to a non-localized mechanical tap. The parameters that govern this behavioral plasticity in C. elegans were subsequently characterized, which lead to the important hypothesis that habituation is mediated by multiple mechanisms. Many tools are available to C. elegans researchers that allow for relatively easy genetic manipulation. This has lead to a number of recent genetic studies that have begun to identify key genes and molecules that play a role in the mechanisms of habituation. Some of these genes include a vesicular glutamate transporter, a glutamate receptor subunit, a dopamine receptor and downstream intracellular signaling molecules, such as G proteins and kinases. Some of these genes only affect certain parameters of habituation, but not others supporting the hypothesis that multiple mechanisms mediate habituation. The field of research has also led to the dissection of different phases of memory (short-term vs. long-term memory for habituation), which are triggered by different training paradigms. The differences in mechanism between these various forms of memory are also beginning to be revealed.     

Behavioral and neuronal attributes of short- and long-term habituation in the crab Chasmagnathus

Investigations using invertebrate species have led to a considerable progress in our understanding of the mechanisms underlying learning and memory. In this review we describe the main behavioral and neuronal findings obtained by studying the habituation of the escape response to a visual danger stimulus in the crab Chasmagnathus granulatus. Massed training with brief intertrial intervals lead to a rapid reduction of the escape response that recovers after a short term. Conversely, few trials of spaced training renders a slower escape reduction that endures for many days. As predicted by Wagner’s associative theory of habituation, long-term habituation in the crab proved to be determined by an association between the contextual environment of the training and the unconditioned stimulus. By performing intracellular recordings in the brain of the intact animal at the same time it was learning, we identified a group of neurons that remarkably reflects the short- and long-term behavioral changes. Thus, the visual memory abilities of crabs, their relatively simple and accessible nervous system, and the recording stability that can be achieved with their neurons provide an opportunity for uncovering neurophysiological and molecular events that occur in identifiable neurons during learning.