Environmental enrichment promotes neural plasticity and cognitive ability in fish

Different kinds of experience during early life can play a significant role in the development of an animal''s behavioural phenotype. In natural contexts, this influences behaviours from anti-predator responses to navigation abilities. By contrast, for animals reared in captive environments, the homogeneous nature of their experience tends to reduce behavioural flexibility. Studies with cage-reared rodents indicate that captivity often compromises neural development and neural plasticity. Such neural and behavioural deficits can be problematic if captive-bred animals are being reared with the intention of releasing them as part of a conservation strategy. Over the last decade, there has been growing interest in the use of environmental enrichment to promote behavioural flexibility in animals that are bred for release. Here, we describe the positive effects of environmental enrichment on neural plasticity and cognition in juvenile Atlantic salmon (Salmo salar). Exposing fish to enriched conditions upregulated the forebrain expression of NeuroD1 mRNA and improved learning ability assessed in a spatial task. The addition of enrichment to the captive environment thus promotes neural and behavioural changes that are likely to promote behavioural flexibility and improve post-release survival.     

Dynamic visual cues induce jaw opening and closing by tiger beetles during pursuit of prey

In dynamic locomotory contexts, visual cues often trigger adaptive behaviour by the viewer, yet studies investigating how animals determine impending collisions typically employ either stationary viewers or objects. Here, we describe a dynamic situation of visually guided prey pursuit in which both impending prey contact and escape elicit observable adaptive behaviours in the pursuer, a predatory beetle. We investigated which visual cues may independently control opening and closing of the beetle''s jaws during chases of prey dummies. Jaw opening and closing typically occur when prey is within the 60° binocular field, but not at specific distances, angular sizes or time-to-collision. We show that a sign change in the expansion rate of the target image precedes jaw opening (16 ms) and closing (35 ms), signalling to the beetle that it is gaining on the target or that the target is getting away. We discuss the ‘sloppiness'' of such variation in the lag of the behavioural response, especially jaw closing, as an adaptation to uncertainty about target position due to degradation of the target image by motion blur from the fast-running beetle.     

Insect–machine hybrid system for understanding and evaluating sensory-motor control by sex pheromone in Bombyx mori

To elucidate the dynamic information processing in a brain underlying adaptive behavior, it is necessary to understand the behavior and corresponding neural activities. This requires animals which have clear relationships between behavior and corresponding neural activities. Insects are precisely such animals and one of the adaptive behaviors of insects is high-accuracy odor source orientation. The most direct way to know the relationships between neural activity and behavior is by recording neural activities in a brain from freely behaving insects. There is also a method to give stimuli mimicking the natural environment to tethered insects allowing insects to walk or fly at the same position. In addition to these methods an ‘insect–machine hybrid system’ is proposed, which is another experimental system meeting the conditions necessary for approaching the dynamic processing in the brain of insects for generating adaptive behavior. This insect–machine hybrid system is an experimental system which has a mobile robot as its body. The robot is controlled by the insect through its behavior or the neural activities recorded from the brain. As we can arbitrarily control the motor output of the robot, we can intervene at the relationship between the insect and the environmental conditions.     

Visuomotor Response to Object Expansion in Free-Flying Bumble Bees

The flight control systems of flying insects enable many kinds of sophisticated maneuvers, including avoidance of midair collisions. Visuomotor response to an approaching object, received as image expansion on insects’ retina, is a complex event in a dynamic environment where both animals and objects are moving. There are intensive free flight studies on the landing response in which insects receive image expansion by their own movement. However, few studies have been conducted regarding how freely flying insects respond to approaching objects. Here, using common laboratory insects for behavioral research, the bumblebee Bombus ignitus, we examined their visual response to an approaching object in the free-flying condition. While the insect was slowly flying in a free-flight arena, an expanding stripe was projected laterally from one side of the arena with a high-speed digital mirror device projector. Rather than turning away reported before, the bumble bees performed complex flight maneuvers. We synchronized flight trajectories, orientations and wing stroke frequencies with projection parameters of temporal resolution in 0.5 ms, and analyzed the instantaneous relationship between visual input and behavioral output. In their complex behavioral responses, we identified the following two visuomotor behaviors: increasing stroke frequency when the bumble bees confront the stripe expansion, and turning towards (not away) the stripe expansion when it is located laterally to the bee. Our results suggested that the response to object expansion is not a simple and reflexive escape but includes object fixation, presumably for subsequent behavioral choice.     

Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom‐up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top‐down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) ‘kinetic null modelling’ of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature‐insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.     

Choosing the greater of two goods: neural currencies for valuation and decision making

To make adaptive decisions, animals must evaluate the costs and benefits of available options. The nascent field of neuroeconomics has set itself the ambitious goal of understanding the brain mechanisms that are responsible for these evaluative processes. A series of recent neurophysiological studies in monkeys has begun to address this challenge using novel methods to manipulate and measure an animal's internal valuation of competing alternatives. By emphasizing the behavioural mechanisms and neural signals that mediate decision making under conditions of uncertainty, these studies might lay the foundation for an emerging neurobiology of choice behaviour.     

Physiological Adaptations of Crayfish to the Hypoxic Environment

SYNOPSIS. Crayfish routinely encounter waters of reduced oxygentension, resulting in a broad array of behavioral and physiologicalresponses. Many animals when faced with this stress will simplyremove themselves from the irritating environment through voluntarymigration. When an animal, either by choice or through physicalconstraints remains in a hypoxic environment it must compensatefor the reduction in O₂ availability. Many crayfish have theability to maintain oxygen consumption independent of waterPo₂ down to some critical level; below this the animal can nolonger maintain normoxic levels of aerobic metabolism. Regulationof oxygen uptake is thought to be due to a hypoxia-induced hyperventilationalong with an increase in hemocyanin O₂ affinity and an improvementin the ability of the respiratory surfaces to transfer O₂. Crayfishexposed to a reduction in water oxygen also show a strong bradycardia,which is compensated for by an increase in stroke volume, resultingin a maintenance of cardiac output. The adaptive advantage ofthis response is uncertain. As water Po₂ drops crayfish havebeen shown to redistribute cardiac output, presumably throughthe action of the cardioarterial valves. Hemolymph is shuntedto the anterior end of the animal, resulting in a greater perfusionof nervous tissue. The animals' ability to detect changes inwater Po₂ appear to result from O₂ sensitive receptors locatedon the gills or in the branchiocardiac veins. The integratedphysiological response toward environmental hypoxia allows thecrayfish to not only deal with the stress but to maintain activity.     

Frogs flee from the sound of fire

Fire has an important role in the sensory ecology of many animals. Using acoustic cues to detect approaching fires may give slow-moving animals a head start when fleeing from fires. We report that aestivating juvenile reed frogs (Hyperolius nitidulus) respond to playbacks of the sound of fire by fleeing in the direction of protective cover, where they are safe. This is a novel response to fire not known to occur in other animals. Moreover, we identify the rapid rise-time of the crackling sound of fire as the probable cue used. These results suggest that amphibian hearing not only has evolved through sexual selection, but also must be viewed in a broader context.     

Retirement investment theory explains patterns in songbird nest-site choice

When opposing evolutionary selection pressures act on a behavioural trait, the result is often stabilizing selection for an intermediate optimal phenotype, with deviations from the predicted optimum attributed to tracking a moving target, development of behavioural syndromes or shifts in riskiness over an individual''s lifetime. We investigated nest-site choice by female golden-winged warblers, and the selection pressures acting on that choice by two fitness components, nest success and fledgling survival. We observed strong and consistent opposing selection pressures on nest-site choice for maximizing these two fitness components, and an abrupt, within-season switch in the fitness component birds prioritize via nest-site choice, dependent on the time remaining for additional nesting attempts. We found that females consistently deviated from the predicted optimal behaviour when choosing nest sites because they can make multiple attempts at one fitness component, nest success, but only one attempt at the subsequent component, fledgling survival. Our results demonstrate a unique natural strategy for balancing opposing selection pressures to maximize total fitness. This time-dependent switch from high to low risk tolerance in nest-site choice maximizes songbird fitness in the same way a well-timed switch in human investor risk tolerance can maximize one''s nest egg at retirement. Our results also provide strong evidence for the adaptive nature of songbird nest-site choice, which we suggest has been elusive primarily due to a lack of consideration for fledgling survival.     

An Analysis of Field Potentials During Different Tailflip Behaviours in Crayfish

Crayfish tailflips have been intensively studied to reveal the decision-making processes and neural organisation underlying a stereotyped escape behaviour. Three behaviours mediated by different neural pathways have been well described: medial giant, lateral giant and non-giant tailflips. It has proved difficult to distinguish between the three without invasive or restrictive experimental manipulation. We report unambiguous differences between the signals generated by the crayfish Cherax destructor during the three types of tailflip when recorded by bath electrodes placed in the holding aquarium. Using our ability to distinguish between the different behaviours in freely moving animals we examined the relationship between the type of tailflip evoked by stimulation to different parts of the body. The transition zone between medial and lateral giant tailflips is the thoracic-abdominal border but it is not absolute and some stimuli produce responses that cannot be unambiguously assigned to either behavioural category. We examined the latency between stimulation at different points down the length of the body and the appearance of the electrical signal accompanying escape for both medial and lateral tailflips. We used two methods to estimate the proportion of the latency accounted for by giant fibre conduction velocity. The results support current views of the differences between the activation sites of the two giant fibre systems and suggest why stimulation in the transition zone results in ambiguous outcomes.     

CB(1) Receptor Autoradiographic Characterization of the Individual Differences in Approach and Avoidance Motivation

Typically, approach behaviour is displayed in the context of moving towards a desired goal, while avoidance behaviour is displayed in the context of moving away from threatening or novel stimuli. In the current research, we detected three sub-populations of C57BL/6J mice that spontaneously responded with avoiding, balancing or approaching behaviours in the presence of the same conflicting stimuli. While the balancing animals reacted with balanced responses between approach and avoidance, the avoiding or approaching animals exhibited inhibitory or advance responses towards one of the conflicting inputs, respectively. Individual differences in approach and avoidance motivation might be modulated by the normal variance in the level of functioning of different systems, such as endocannabinoid system (ECS). The present research was aimed at analysing the ECS involvement on approach and avoidance behavioural processes. To this aim, in the three selected sub-populations of mice that exhibited avoiding or balancing or approaching responses in an approach/avoidance Y-maze we analysed density and functionality of CB(1) receptors as well as enzyme fatty acid amide hydrolase activity in different brain regions, including the networks functionally responsible for emotional and motivational control. The main finding of the present study demonstrates that in both approaching and avoiding animals higher CB(1) receptor density in the amygdaloidal centro-medial nuclei and in the hypothalamic ventro-medial nucleus was found when compared with the CB(1) receptor density exhibited by the balancing animals. The characterization of the individual differences to respond in a motivationally based manner is relevant to clarify how the individual differences in ECS activity are associated with differences in motivational and affective functioning.     

Courtship and genetic quality: asymmetric males show their best side

Fluctuating asymmetry (FA), the small random deviations from perfect morphological symmetry that result during development, is ubiquitous throughout the animal kingdom. In many species, FA seems to play a role in mate choice, perhaps because it signals an individual''s genetic quality and health. However, the relationship between an individual''s FA and behaviour is generally unknown: what do more asymmetric individuals do about their own asymmetry? We now show for the first time that individuals respond behaviourally to their own morphological FA in what appears to be an adaptive manner. During courtship, male guppies exhibiting high FA in ornamental colour, bias their displays towards their more colourful body side, thus potentially increasing their attractiveness by exaggerating the quantity of their orange signal. This appears to be a strictly behavioural male response to cues provided by females, as it does not occur when males court a non-reactive model female. Whether inferior males realize any mating advantage remains uncertain, but our study clearly demonstrates a behavioural response to random morphological asymmetries that appears to be adaptive. We propose that the tendency to show or otherwise use a ‘best side’ is common in nature, with implications for sexual signalling and the evolution of more pronounced asymmetries.     

Are Cape Ground Squirrels (Xerus inauris) Sensitive to Variation in the Pay‐offs from Their Caches?

For food caching to be adaptive, the benefits of recovery must outweigh the costs of storing an item. One of the costs to cachers is the risk of theft, and therefore, it is predicted that individuals may be sensitive to this theft and show various behavioural strategies to minimise it. In this study, we gave wild Cape ground squirrels (Xerus inauris) a choice between two different coloured items of the same food type: one item with a specific colour that was always artificially removed when cached and the other item with a different colour that was not removed when cached. During the choice presentations, subjects reduced the amount they consumed and cached of the food items with the colour that was experimentally removed when cached, despite the two items only differing in caching pay‐off. This avoidance to choose the food with the colour that was removed occurred over time, which suggests that subjects were using information about the item's pay‐off during cache recovery and this then impacted on successive decisions. This study highlights how the sensitivity to a food item's pay‐off can affect an individual's choice towards items that offer the greater overall reward.     

Recording Single Neurons' Action Potentials from Freely Moving Pigeons Across Three Stages of Learning

While the subject of learning has attracted immense interest from both behavioral and neural scientists, only relatively few investigators have observed single-neuron activity while animals are acquiring an operantly conditioned response, or when that response is extinguished. But even in these cases, observation periods usually encompass only a single stage of learning, i.e. acquisition or extinction, but not both (exceptions include protocols employing reversal learning; see Bingman et al.¹ for an example). However, acquisition and extinction entail different learning mechanisms and are therefore expected to be accompanied by different types and/or loci of neural plasticity.Accordingly, we developed a behavioral paradigm which institutes three stages of learning in a single behavioral session and which is well suited for the simultaneous recording of single neurons'' action potentials. Animals are trained on a single-interval forced choice task which requires mapping each of two possible choice responses to the presentation of different novel visual stimuli (acquisition). After having reached a predefined performance criterion, one of the two choice responses is no longer reinforced (extinction). Following a certain decrement in performance level, correct responses are reinforced again (reacquisition). By using a new set of stimuli in every session, animals can undergo the acquisition-extinction-reacquisition process repeatedly. Because all three stages of learning occur in a single behavioral session, the paradigm is ideal for the simultaneous observation of the spiking output of multiple single neurons. We use pigeons as model systems, but the task can easily be adapted to any other species capable of conditioned discrimination learning.     

Differential Neural Activation Patterns in Patients with Parkinson's Disease and Freezing of Gait in Response to Concurrent Cognitive and Motor Load

Freezing of gait is a devastating symptom of Parkinson''s disease (PD) that is exacerbated by the processing of cognitive information whilst walking. To date, no studies have explored the neural correlates associated with increases in cognitive load whilst performing a motor task in patients with freezing. In this experiment, 14 PD patients with and 15 PD patients without freezing of gait underwent 3T fMRI while performing a virtual reality gait task. Directions to walk and stop were presented on the viewing screen as either direct cues or as more cognitively indirect pre-learned cues. Both groups showed a consistent pattern of BOLD response within the Cognitive Control Network during performance of the paradigm. However, a between group comparison revealed that those PD patients with freezing of gait were less able to recruit the bilateral anterior insula, ventral striatum and the pre-supplementary motor area, as well as the left subthalamic nucleus when responding to indirect cognitive cues whilst maintaining a motor output. These results suggest that PD patients with freezing of gait are unable to properly recruit specific cortical and subcortical regions within the Cognitive Control Network during the performance of simultaneous motor and cognitive functions.     

Temperature compensation in the nervous system of the grasshopper

Abstract The wind-sensitive head hair neurones of the grasshopper Schistocerca americana (Drury) are influenced by temperature, increasing the number of spikes fired in response to a given hair deflection as temperature increases. Because these neurones show similar increases in spike output for greater hair deflections, an interneurone which receives their input would not be able to distinguish changes in stimulus strength from changes in temperature, unless the effects of temperature were compensated or independently measured. This study examines the effects of temperature on the output of the tritocerebral commissure giant (TCG), an interneurone that receives wind hair input. Some wind hairs provide excitatory input to the TCG, while others are inhibitory (Bacon & Möhl, 1983). Temperature variations similar to those measured in freely moving animals were applied to the wind hairs and TCG while the interneurone's spike output was recorded. Two manipulations resulted in temperature compensated outputs from the TCG: (1) When both excitatory and inhibitory hair fields were stimulated simultaneously, the temperature sensitivity of the interneurone's spike output was significantly lower than when the excitatory hairs alone were stimulated. (2) The spike output of the TCG showed very little sensitivity to temperature changes which occurred only at its wind hair inputs, the temperature of the interneurone itself remaining constant. It is therefore possible for the output of a neural circuit to be temperature compensated even though the circuit itself may be composed of temperature-sensitive units. Possible mechanisms by which temperature compensation may be produced in the TCG are discussed, and the behavioural relevance of the conditions under which TCG output is temperature compensated is considered.     

Is there a brainstem substrate for action selection?

The search for the neural substrate of vertebrate action selection has focused on structures in the forebrain and midbrain, and particularly on the group of sub-cortical nuclei known as the basal ganglia. Yet, the behavioural repertoire of decerebrate and neonatal animals suggests the existence of a relatively self-contained neural substrate for action selection in the brainstem. We propose that the medial reticular formation (mRF) is the substrate's main component and review evidence showing that the mRF's inputs, outputs and intrinsic organization are consistent with the requirements of an action-selection system. The internal architecture of the mRF is composed of interconnected neuron clusters. We present an anatomical model which suggests that the mRF's intrinsic circuitry constitutes a small-world network and extend this result to show that it may have evolved to reduce axonal wiring. Potential configurations of action representation within the internal circuitry of the mRF are then assessed by computational modelling. We present new results demonstrating that each cluster's output is most likely to represent activation of a component action; thus, coactivation of a set of these clusters would lead to the coordinated behavioural response observed in the animal. Finally, we consider the potential integration of the basal ganglia and mRF substrates for selection and suggest that they may collectively form a layered/hierarchical control system.     

The vulnerability of juvenile signal crayfish to perch and eel predation

1. We conducted laboratory experiments to determine how juvenile signal crayfish (Pacifastacus leniusculus) responded to two predators with different foraging behaviours (European eel Anguilla anguilla and European perch Perca fluviatilis), and whether these responses affected their vulnerability. 2. By accelerating a model predator towards crayfish which had been temporarily blinded, we assessed whether crayfish had to see predators in order to escape. Blind crayfish escaped later than did sighted crayfish attacked in the same manner. 3. Both eels and perch elicited similar evasive behaviour when approaching and attacking sighted crayfish. Crayfish usually escaped these initial attacks but perch chased and caught more crayfish than did eels. 4. In a third experiment, perch preyed more rapidly on a population of crayfish than did eels. By the end of the experiment, however, crayfish survival rates were similar in response to eel and perch predation. 5. Our results show that crayfish are well adapted to evade predatory attacks based on rapid responses to both visual and/or mechanical stimuli. The results also suggest that behaviourally, crayfish are more vulnerable to attacks by perch than by eels. We discuss these findings in relation to other factors that affect the vulnerability of crayfish to these predators.     

Behavioral, morphologic and biochemical correlates of the early effect of a neural transplant into the damaged brain of adult rats

Complex study was carried out of the behavioural, morphological and neurobiochemical parameters of the effect of an embryonal neural transplant of the amygdala in the first weeks after its introduction into the area of the left amygdala of adult rats-recipients. The neural transplant promoted normalization of animals food search, disturbed by operative interference. The amygdalar embryonal tissue lowered the proliferative glia reaction, produced by the brain lesion, and intensified the nervous tissue regeneration. The neural transplant intensified generalized adaptive neurobiochemical processes in the lesioned brain.     

An experimental approach to the formation of diet preferences and individual specialisation in European mink

Individual dietary specialisation can occur within populations even when average diets suggest that the population has a generalist feeding strategy. Individual specialisation may impact fitness and has been related to demographic traits, ecological opportunity, competition, learning and animal personality. However, the causation and formation of individual specialisation are not fully understood. Experiments on animals raised in controlled environments provide an opportunity to examine dietary preferences and learning largely independent from variation in lifetime experiences and ecological opportunity. Here, we use a feeding experiment to examine individual specialisation and learning in captive bred European mink (Mustela lutreola) in an Estonian conservation programme. In a series of cafeteria experiments, animals could choose between one familiar food item (Baltic herring Clupea harengus membras) and two initially novel ones (noble crayfish Astacus astacus and house mouse Mus musculus). In general, mice were rarely eaten whilst crayfish consumption increased over time and fish decreased. At the individual level, there was a mix of generalists and crayfish or fish specialists, and the individuals differed in learning time in relation to novel prey. Our results indicate that individual variation in innate preferences and learning both contributes to individual diet specialisation. The differences in learning indicate individual variation in behavioural plasticity, which in turn can be related to personality. This could be of concern in conservation, as personality has been shown to affect survival in translocations.