Extrinsic embryonic sensory stimulation alters multimodal behavior and cellular activation

Embryonic vision is generated and maintained by spontaneous neuronal activation patterns, yet extrinsic stimulation also sculpts sensory development. Because the sensory and motor systems are interconnected in embryogenesis, how extrinsic sensory activation guides multimodal differentiation is an important topic. Further, it is unknown whether extrinsic stimulation experienced near sensory sensitivity onset contributes to persistent brain changes, ultimately affecting postnatal behavior. To determine the effects of extrinsic stimulation on multimodal development, we delivered auditory stimulation to bobwhite quail groups during early, middle, or late embryogenesis, and then tested postnatal behavioral responsiveness to auditory or visual cues. Auditory preference tendencies were more consistently toward the conspecific stimulus for animals stimulated during late embryogenesis. Groups stimulated during middle or late embryogenesis showed altered postnatal species-typical visual responsiveness, demonstrating a persistent multimodal effect. We also examined whether auditory-related brain regions are receptive to extrinsic input during middle embryogenesis by measuring postnatal cellular activation. Stimulated birds showed a greater number of ZENK-immunopositive cells per unit volume of brain tissue in deep optic tectum, a midbrain region strongly implicated in multimodal function. We observed similar results in the medial and caudomedial nidopallia in the telencephalon. There were no ZENK differences between groups in inferior colliculus or in caudolateral nidopallium, avian analog to prefrontal cortex. To our knowledge, these are the first results linking extrinsic stimulation delivered so early in embryogenesis to changes in postnatal multimodal behavior and cellular activation. The potential role of competitive interactions between the sensory and motor systems is discussed.     

Octopus vulgaris uses visual information to determine the location of its arm

Octopuses are intelligent, soft-bodied animals with keen senses that perform reliably in a variety of visual and tactile learning tasks. However, researchers have found them disappointing in that they consistently fail in operant tasks that require them to combine central nervous system reward information with visual and peripheral knowledge of the location of their arms. Wells claimed that in order to filter and integrate an abundance of multisensory inputs that might inform the animal of the position of a single arm, octopuses would need an exceptional computing mechanism, and "There is no evidence that such a system exists in Octopus, or in any other soft bodied animal." Recent electrophysiological experiments, which found no clear somatotopic organization in the higher motor centers, support this claim. We developed a three-choice maze that required an octopus to use a single arm to reach a visually marked goal compartment. Using this operant task, we show for the first time that Octopus vulgaris is capable of guiding a single arm in a complex movement to a location. Thus, we claim that octopuses can combine peripheral arm location information with visual input to control goal-directed complex movements.     

Sex differences in the long-term effect of preweanling isolation stress on memory retention

Social experiences during development can powerfully modulate later neuroendocrine and behavioral system. In the present study, male and female rat pups experienced daily bouts of social isolation for 6 h per day or control conditions during the third postnatal week. Performance on a 12-arm radial maze with 8 arms consistently baited with food reward was examined in adulthood. During the social isolation, both male and female pups exhibited a significant increase in plasma corticosterone levels. When tested on the radial arm maze as adults, the performance of female rats that had experienced social isolation during development was not affected; however, male rats in the isolation condition initially exhibited impairments in working memory but not reference memory. Despite achieving comparable asymptotic levels of performance on the maze, male rats that experienced social isolation during the third week demonstrated disruption in working memory retention when radial arm maze trials were interrupted after the fourth arm choice. Thus, while male rats that experience social isolation during the third week of life eventually perform comparably to controls on the standard radial arm maze task, their ability to retain information over a delay remains impaired. These findings highlight an important sex difference in the long-term effects of stress during this period of late preweanling development.     

Contextual control of rats' foraging behaviour in a radial maze

This study demonstrated that with experience rats were able to discriminate the background contextual cues in order to foraging correctly in an eight-arm radial maze if the background contexts signaled to the rats which of two bait patterns was in effect in that context. Four of the eight arms were context-dependent: two arms were baited in the "night" context, while the other two were baited in the "daytime" context. The remaining four arms were context-independent: three of them were never baited, while the remaining one was baited in both contexts. The rats gradually began to avoid the arms that were uniquely baited in the other context, suggesting a contextual or conditional control of arm selection. Interestingly, these rats also showed better performance in avoiding the never-baited arms, compared with control rats. Namely, disambiguating the incentive values of the four arms by contextual cues collaterally facilitated the context-independent arm performance. Another interesting finding of the present study is that the rats did not visit the always-baited arm earlier than the arms uniquely baited in that context.     

Multimodal sensory integration in the strike-feeding behaviour of predatory fishes

The search for useful model systems for the study of sensory processing in vertebrate nervous systems has resulted in many neuroethological studies investigating the roles played by a single sensory modality in a given behaviour. However, behaviours relying solely upon information from one sensory modality are relatively rare. Animals behaving in a complex, three-dimensional environment receive a large amount of information from external and internal receptor arrays. Clearly, the integration of sensory afference arising from different modalities into a coherent 'gestalt' of the world is essential to the behaviours of most animals. In the last several years our laboratory team has examined the roles played by the visual and lateral line sensory systems in organizing the feeding behaviour of two species of predatory teleost fishes, the largemouth bass, Micropterus salmoides, and the muskellunge, Esox masquinongy. The free-field feeding behaviours of these fishes were studied quantitatively in intact animals and compared to animals in which the lateral line and visual systems had been selectively suppressed. All groups of animals continued to feed successfully, but significant differences were observed between each experimental group, providing strong clues as to the relative role played by each sensory system in the organization of the behaviour. Furthermore, significant differences exist between the two species. The differences in behaviour resulting when an animal is deprived of a given sensory modality reflect the nature of central integrative sensory processes, and these behavioural studies provide a foundation for further neuroanatomical and physiological studies of sensory integration in the vertebrate central nervous system.     

Effects of chronic iTBS‐rTMS and enriched environment on visual cortex early critical period and visual pattern discrimination in dark‐reared rats

Early cortical critical period resembles a state of enhanced neuronal plasticity enabling the establishment of specific neuronal connections during first sensory experience. Visual performance with regard to pattern discrimination is impaired if the cortex is deprived from visual input during the critical period. We wondered how unspecific activation of the visual cortex before closure of the critical period using repetitive transcranial magnetic stimulation (rTMS) could affect the critical period and the visual performance of the experimental animals. Would it cause premature closure of the plastic state and thus worsen experience‐dependent visual performance, or would it be able to preserve plasticity? Effects of intermittent theta‐burst stimulation (iTBS) were compared with those of an enriched environment (EE) during dark‐rearing (DR) from birth. Rats dark‐reared in a standard cage showed poor improvement in a visual pattern discrimination task, while rats housed in EE or treated with iTBS showed a performance indistinguishable from rats reared in normal light/dark cycle. The behavioral effects were accompanied by correlated changes in the expression of brain‐derived neurotrophic factor (BDNF) and atypical PKC (PKCζ/PKMζ), two factors controlling stabilization of synaptic potentiation. It appears that not only nonvisual sensory activity and exercise but also cortical activation induced by rTMS has the potential to alleviate the effects of DR on cortical development, most likely due to stimulation of BDNF synthesis and release. As we showed previously, iTBS reduced the expression of parvalbumin in inhibitory cortical interneurons, indicating that modulation of the activity of fast‐spiking interneurons contributes to the observed effects of iTBS. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 19–33, 2016     

Path planning versus cue responding: a bio-inspired model of switching between navigation strategies

In this article, we describe a new computational model of switching between path-planning and cue-guided navigation strategies. It is based on three main assumptions: (i) the strategies are mediated by separate memory systems that learn independently and in parallel; (ii) the learning algorithms are different in the two memory systems—the cue-guided strategy uses a temporal-difference (TD) learning rule to approach a visible goal, whereas the path-planning strategy relies on a place-cell-based graph-search algorithm to learn the location of a hidden goal; (iii) a strategy selection mechanism uses TD-learning rule to choose the most successful strategy based on past experience. We propose a novel criterion for strategy selection based on the directions of goal-oriented movements suggested by the different strategies. We show that the selection criterion based on this “common currency” is capable of choosing the best among TD-learning and planning strategies and can be used to solve navigational tasks in continuous state and action spaces. The model has been successfully applied to reproduce rat behavior in two water-maze tasks in which the two strategies were shown to interact. The model was used to analyze competitive and cooperative interactions between different strategies during these tasks as well as relative influence of different types of sensory cues.     

Do Male and Female Cowbirds See Their World Differently? Implications for Sex Differences in the Sensory System of an Avian Brood Parasite

Background

Male and female avian brood parasites are subject to different selection pressures: males compete for mates but do not provide parental care or territories and only females locate hosts to lay eggs. This sex difference may affect brain architecture in some avian brood parasites, but relatively little is known about their sensory systems and behaviors used to obtain sensory information. Our goal was to study the visual resolution and visual information gathering behavior (i.e., scanning) of brown-headed cowbirds.

Methodology/Principal Findings

We measured the density of single cone photoreceptors, associated with chromatic vision, and double cone photoreceptors, associated with motion detection and achromatic vision. We also measured head movement rates, as indicators of visual information gathering behavior, when exposed to an object. We found that females had significantly lower density of single and double cones than males around the fovea and in the periphery of the retina. Additionally, females had significantly higher head-movement rates than males.

Conclusions

Overall, we suggest that female cowbirds have lower chromatic and achromatic visual resolution than males (without sex differences in visual contrast perception). Females might compensate for the lower visual resolution by gazing alternatively with both foveae in quicker succession than males, increasing their head movement rates. However, other physiological factors may have influenced the behavioral differences observed. Our results bring up relevant questions about the sensory basis of sex differences in behavior. One possibility is that female and male cowbirds differentially allocate costly sensory resources, as a recent study found that females actually have greater auditory resolution than males.     

Appetitive position discrimination in the T-maze

This protocol details a method to perform appetitively motivated tasks in rodents to test cognitive ability. When testing cognition in animals, the simplest paradigms can potentially yield quick results with minimal investment from the experimenter. Although appetitively motivated tasks are generally learnt more slowly than aversively motivated ones, they may be essential for distinguishing the effects of a treatment on learning from its effects on aversive motivation per se. For example, if a treatment improves learning in both types of paradigm, this is better evidence that it affects cognition rather than sensorimotor processes. Rats and mice easily learn position discriminations in a T-maze, especially if multiple cues, such as different objects and floor textures in the goal arms, are provided. To start, the rodent is placed in the maze and it chooses an arm. This Trial 1, however, is the only one on which this arm will be rewarded. From now on, it must always choose the other arm. The rule is simple: for example, always turn left into the arm with diagonal black stripes on the walls and gravel glued to the floor. High levels of correct responding can be achieved within 20-40 trials. The test may therefore be particularly useful with animals of low cognitive ability, such as transgenic mice derived from some 129 or SJL strains. Once the animals are habituated, each trial should take approximately 1 min. Thus, to test ten animals for 40 trials would take around 7 h.     

视觉系统中的性别差异

大脑性别差异一直是神经科学领域中的一个热门话题.以前的性别差异研究往往关注与高级认知相关的脑区结构和功能差异,而对低级感知觉系统中的性别差异没有足够的重视.近年来,越来越多的研究结果表明,男性和女性在视知觉功能上也存在着明显的差异.本文首先回顾和梳理了视觉系统中存在性别差异的行为学和神经生物学证据,然后对视觉系统中性别...     

"Spatial memory in Long Evans and Rattus Norvegicus rats"

Rodents in search of food use visual environmental signals and complex spatial strategies and do not return to previously-visited locations, known as the win-shift strategy. The solution to the Olton Octagonal Maze (OOM) involves Working Memory (WM). A modified OOM was used that allows for measuring WM and Long Term Memory (LTM). The delayed spatial win-shift task consisted of a Training and Test phase separated by a delay. Prior to the Training phase, four arms were chosen at random and blocked, and food pellets were placed in the food cups of the four remaining open arms. Each rat was allowed to retrieve the pellets from the four open arms and then return to its home cage for the delay period (either 5 or 20 min). In the Test phase all 8 lanes were open, and the bait was placed in those blocked in the previous phase. Two experimental groups of rats, Long Evans and Norvegicus, and their corresponding control groups were trained. The experimental subjects performed Training-Delay-Test. The controls were only trained in the Test phase. Revisiting an arm previously explored in the 1st Phase was considered a LTM error. Revisiting an arm in the same trial constituted a WM error. It was concluded that the experimental groups do in fact possess LTM, with differences in favor of Norvegicus. There was no difference with respect to WM errors. The Norvegicus control group changes its strategy from allocentric to egocentric, which did not occur in the Long Evans control group.     

Chronic stress effects on memory: sex differences in performance and monoaminergic activity

Increasing evidence suggests that the time course of advantageous versus deleterious effects of stress on physiologic function is also apparent in some brain functions, including learning and memory. This article reviews the effects of chronic stress on behavioral performance and, more importantly, shows that sex of the subject, as well as duration and intensity of stress, is an important determinant of the functional/behavioral, neurochemical, and anatomical consequences of the stress. Following chronic stress (7-28 days of restraint, 6 h/day), male and female rats were tested on a visual memory task (object recognition) and two spatial memory tasks (object placement and radial arm maze). At 21 days, stress impaired males on all tasks while females were either enhanced (spatial memory tasks) or not impaired (nonspatial memory tasks). Additionally, the influence of the hypothalamic-pituitary-adrenocortical axis in mediating the sex-specific responses to stress is considered. Behavioral and neurochemical assessments following chronic stress in ovariectomized females, with and without estradiol, suggest that estrogen exerts both organizational and activational influences on the observed sex differences in response to stress. Furthermore, stress differentially affected central transmitter levels in the frontal cortex, hippocampus, and amygdala depending on sex. The possible role of these sex-specific changes in neurotransmitter levels in mediating behavioral differences in response to stress is discussed. While these results are thus far limited to a few studies and require both further investigation and verification, chronic stress appears to be associated with distinct, sex-differentiated behavioral/cognitive and neurochemical responses. We conclude that sex differences must be taken into account when investigating or describing stress and associated sequalae.     

Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea)

The sensory systems employed by animals to locate potential mates are diverse. Among insects, chemical and acoustic signals are commonly used over long distances, with visual signals playing a role in close-range orientation and courtship. Within groups that exhibit a scramble competition mating system, selection on mate searching ability will be particularly strong. Clearly, aspects of the species ecology, such as habitat complexity and population density, will be crucial in the evolution of mate searching systems and sexual signals. Praying mantids exhibit both chemical and visual sexual signalling behaviour, and also vary in their ecology. This study employs scanning electron microscopy of antennal sensory morphology and behavioural assays to investigate the relative importance of chemical and visual signalling in two Australian praying mantid species: Pseudomantis albofimbriata and Ciulfina biseriata . As predicted, the high level of habitat complexity, low population density and strong male dispersal capability of P. albofimbriata corresponded to the use of airborne sex pheromones. Conversely, the open habitat, high population density, and poor dispersal of C. biseriata corresponded to a greater reliance on short-range visual cues for mate location.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 307–313.     

Hippocampal and striatal dependent navigation: Sex differences are limited to acquisition

Estrogen has been demonstrated to enhance the use of hippocampal-based place learning while reducing the use of striatal-based motor-response strategy (Korol, D.L., Malin, E.L., Borden, K.A., Busby, R.A., & Couper-Leo, J. (2004). Shifts in preferred learning strategy across the estrous cycle in female rats. Horm. Behav. 45, 330–338). Previous research has focused on task acquisition and the switch from a place to motor-response navigation with training. The current paradigm allowed an examination of the interplay between these two systems by having well-trained animals switch strategies “on demand.” Female and male Sprague–Dawley rats were taught a motor-response task on a plus maze. The rats were then introduced to a place task and taught to switch, by cue, from the motor-response to place strategy. Finally, the rats were trained to continuously alternate between place and motor-responses strategies. The maze configuration allowed for an analysis of cooperative choices (both strategies result in the same goal arm), competitive choices (both strategies result in different goal arms), and single strategy choices (can only use the motor-response strategy). The results indicate that sex and estrogen-related effects on navigation strategy are limited to the initial stages of learning a task. The role of sex and estrogen is diminished once the task is well learned, and presumably, the relative involvement of the hippocampal and striatal systems is established.     

Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator's visual system

Even though the importance of selection for trait evolution is well established, we still lack a functional understanding of the mechanisms underlying phenotypic selection. Because animals necessarily use their sensory system to perceive phenotypic traits, the model of sensory bias assumes that sensory systems are the main determinant of signal evolution. Yet, it has remained poorly known how sensory systems contribute to shaping the fitness surface of selected individuals. In a greenhouse experiment, we quantified the strength and direction of selection on floral coloration in a population of cornflowers exposed to bumblebees as unique pollinators during 4 days. We detected significant selection on the chromatic and achromatic (brightness) components of floral coloration. We then studied whether these patterns of selection are explicable by accounting for the visual system of the pollinators. Using data on bumblebee colour vision, we first showed that bumblebees should discriminate among quantitative colour variants. The observed selection was then compared to the selection predicted by psychophysical models of bumblebee colour vision. The achromatic but not the chromatic channel of the bumblebee's visual system could explain the observed pattern of selection. These results highlight that (i) pollinators can select quantitative variation in floral coloration and could thus account for a gradual evolution of flower coloration, and (ii) stimulation of the visual system represents, at least partly, a functional mechanism potentially explaining pollinators' selection on floral colour variants.     

Selection of visual hierarchical stimuli between global and local aspects in men and women

Sex differences in global-local hemispheric selective processing were examined by hierarchical letter presenting in conditions of their perception and comparison. Fifty-six right-handed males and 68 females (aged 17-22 years) participated in the experiment. During interference between global and local aspects of stimuli the mean reaction times for correct global responses was quicker than local responses, and the right hemisphere has been dominated during global selective processing independently from the sex. Sex differences in perception of visual hierarchical stimuli were more pronounced than in comparison condition: men prefer mostly the right-hemispheric global strategy of information processing, but women--the left-hemispheric local one. Dominance of global strategy in men and local strategy in women during visual hierarchical stimuli perception together with no sex differences in correct responses indicates possibility of similar results in cognitive activity by different ways.     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

A non‐lethal method for estimation of gonad and pyloric caecum indices in sea stars

Abstract. Gonad and pyloric caecum indices are widely used indicators of reproductive effort and nutritional condition in asteroids. Current methods of quantification generally require sacrificing multiple animals and the resulting reduction in local sea star density could have an unintended impact on benthic communities. Using the intertidal sea star Pisaster ochraceus, we developed and tested a method for estimating organ indices through the non‐lethal sampling of single arms. Indices estimated via dissections of single arms accurately predicted the values obtained by sacrificing whole animals. In laboratory and field trials, we compared two methods of sampling single arms: (1) arm removal, and (2) organ extraction through an incision (without arm removal). Two years after these treatments, organs had regenerated in the affected arms of most sea stars, but were small relative to those in unmanipulated arms. The extent of organ recovery did not differ between the two treatments, but sea stars in the arm removal group were relocated in the field more frequently than those in the arm incision group. Our results suggest that sampling via the removal of single arms can be an effective, non‐lethal method for estimating gonad and pyloric caecum indices in asteroids.     

Perceptual learning and sensomotor flexibility: cortical plasticity under attentional control?

Recent research reveals long-lasting cortical plasticity of early sensory cortices even in adults. Sensory signals could be modified under top-down control if necessary quite early in order to optimize their signal-to-noise ratio, leading to 'low level' or 'early' perceptual learning (PL). For easy tasks, such elaborate top-down influences are usually not required, and learning is restricted to late selection of the appropriate signals on higher cortical levels, which seems easier and faster to achieve. But to reach the absolute limits of sensory performance, PL seems to optimize the entire chain of sensory processing. Hence, improvement for these extreme perceptual abilities is quite specific for a number of stimulus parameters, such as the position in the visual field and sometimes even the trained eye, reflecting the specificity of receptive fields in early sensory cortices. Early PL may be just one example--even if a very extensive one--of the mechanisms of neuronal plasticity and sensomotor flexibility that are constantly updating our sensomotor representations as a result of experience. As an illustration, this review contains some new experimental results on PL and sensory flexibility in the context of adaptation to multifocal intraocular lenses.     

Interval timing in children: effects of auditory and visual pacing stimuli and relationships with reading and attention variables

Motor timing tasks have been employed in studies of neurodevelopmental disorders such as developmental dyslexia and ADHD, where they provide an index of temporal processing ability. Investigations of these disorders have used different stimulus parameters within the motor timing tasks that are likely to affect performance measures. Here we assessed the effect of auditory and visual pacing stimuli on synchronised motor timing performance and its relationship with cognitive and behavioural predictors that are commonly used in the diagnosis of these highly prevalent developmental disorders. Twenty-one children (mean age 9.6 years) completed a finger tapping task in two stimulus conditions, together with additional psychometric measures. As anticipated, synchronisation to the beat (ISI 329 ms) was less accurate in the visually paced condition. Decomposition of timing variance indicated that this effect resulted from differences in the way that visual and auditory paced tasks are processed by central timekeeping and associated peripheral implementation systems. The ability to utilise an efficient processing strategy on the visual task correlated with both reading and sustained attention skills. Dissociations between these patterns of relationship across task modality suggest that not all timing tasks are equivalent.