Octopus vulgaris Exhibits Interindividual Differences in Behavioural and Problem-Solving Performance.

By presenting individual Octopus vulgaris with an extractive foraging problem with a puzzle box, we examined the possible correlation between behavioural performances (e.g., ease of adaptation to captive conditions, prevalence of neophobic and neophilic behaviours, and propensity to learn individually or by observing conspecifics), biotic (body and brain size, age, sex) and abiotic (seasonality and place of origin) factors. We found more neophilic animals showing shorter latencies to approach the puzzle box and higher probability of solving the task; also, shorter times to solve the task were correlated with better performance on the individual learning task. However, the most neophilic octopuses that approached the puzzle box more quickly did not reach the solution earlier than other individuals, suggesting that strong neophilic tendency may lead to suboptimal performance at some stages of the problem-solving process. In addition, seasonal and environmental characteristics of location of origin appear to influence the rate of expression of individual traits central to problem solving. Overall, our analysis provides new insights into the traits associated with problem solving in invertebrates and highlights the presence of adaptive mechanisms that promote population-level changes in octopuses' behavioural traits.

Unlocking the symmetric transfer of irrelevant information: gene-environment interplay and enhanced interhemispheric cross-talk.

Hemispheric specialization influences stimulus processing and behavioural control, affecting responses to relevant stimuli. However, most sensory input is irrelevant and must be filtered out to prevent interference with task-relevant behaviour, a process known as habituation. Despite habituation's vital role, little is known about hemispheric specialization for this brain function. We conducted an experiment with domestic chicks, an elite animal model to study lateralization. They were exposed to distracting visual stimuli while feeding when using binocular or monocular vision. Switching the viewing eye after habituation, we examined if habituation was confined to the stimulated hemisphere or shared across hemispheres. We found that both hemispheres learned equally to ignore distracting stimuli. However, embryonic light stimulation, influencing hemispheric specialization, revealed an asymmetry in interhemispheric transfer of the irrelevant information discarded via habituation. Unstimulated chicks exhibited a directional bias, with the right hemisphere failing to transfer distracting stimulus information to the left hemisphere, while transfer from left to right was possible. Nevertheless, embryonic light stimulation counteracted this asymmetry, enhancing communication from the right to the left hemisphere and reducing the pre-existing imbalance. This sharing extends beyond hemisphere-specific functions and encompasses a broader representation of irrelevant events.

Individual differences in habituation: Innate covariation between habituation, exploration, and body size in naïve chicks (Gallus gallus).

Habituation to novel stimuli has been associated with behavioural differences among individuals in numerous animal species. Because the habituation mechanisms depend on previous experiences with a stimulus, one would expect individuals to develop their habituation capacity based on the life experiences that also shape their behavioural traits. And indeed, in adult lizards, exploratory behaviour and body size correlates with habituation. However, here we show that the same factors correlate with habituation of domestic chicks reared under controlled laboratory conditions and tested in the first 3 days after hatching. This result indicates that the covariation between habituation, exploration, and body size does not necessarily depend on experience. Rather, it represents an innate association between exploratory behaviour and risk assessment, which may provide an immediate survival advantage to new-borns of this precocial avian species.

Young domestic chicks spontaneously represent the absence of objects.

Absence is a notion that is usually captured by language-related concepts like zero or negation. Whether nonlinguistic creatures encode similar thoughts is an open question, as everyday behavior marked by absence (of food, of social partners) can be explained solely by expecting presence somewhere else. We investigated 8-day-old chicks' looking behavior in response to events violating expectations about the presence or absence of an object. We found different behavioral responses to violations of presence and absence, suggesting distinct underlying mechanisms. Importantly, chicks displayed an avian signature of novelty detection to violations of absence, namely a sex-dependent left-eye-bias. Follow-up experiments excluded accounts that would explain this bias by perceptual mismatch or by representing the object at different locations. These results suggest that the ability to spontaneously form representations about the absence of objects likely belongs to the initial cognitive repertoire of vertebrate species.

Context-Specific Habituation: A Review.

Habituation consists of the progressive response decrement to a repeated stimulation, a response decline that is not accounted for by sensory or motor fatigue. Together with sensitization, habituation has been traditionally considered to be a prototypical example of non-associative learning, being affected only by the features of the stimulation, as for instance its intensity or frequency. However, despite this widespread belief, evidence exists showing that habituation can be specific to the context of the stimulation, thus suggesting that habituation can have an associative nature. Such an unexpected characteristic of habituation was in fact predicted by a theoretical model of associative learning proposed by Wagner in a series of works that appeared in the late 1970s. Here, we critically review the experimental data that since then have been accumulated in support of this hypothesis. What emerges from the literature is that context-specific habituation is common to several animal species and that the ability to form an association between the habituating stimulus and its context is independent of the complexity of the animal's nervous system. Finally, context-specific habituation is observed for a variety of organism's responses, ranging from visceral to motor and mental activities.

Medium-term feasibility of the management of the invasive crayfish Procambarus clarkii with the sterile males release technique.

BACKGROUND: The sterile male release technique (SMRT) is a useful method applied for controlling invasive and pest species. However, the use of X-rays can lead to negative effects on the survival and health conditions of sterilized males. RESULTS: This study was set up to evaluate the functional integrity of physiological, morphological and behavioural responses in males of the red swamp crayfish, Procambarus clarkii (Girard, 1852), exposed to a dose of 40 Gy of ionizing radiation. Concerning physiological responses, the results showed that the irradiation dose, tested at 5, 12, 28, 35, 65, 99, 132 and 193 days after treatment, has no effects on glycaemic and plasmatic total protein levels measured as biomarkers for general stress indexes. Nevertheless, the significant reduction of circulating haemocytes and the basal levels of phenoloxidase (PO) activities recorded in 40-Gy irradiated crayfishes indicate that the exposure shrinks their capability to mount a rapid nonspecific response, and higher levels of plasmatic total PO activity indicate the ability to compensate and maintain an inducible response. Histological analyses performed at the end of the experiment showed no morphological damage in the testicular acini of irradiated males. Moreover, behavioural responses to two different water stimuli (vaporization and jet), measured at 15 and 45 days after the irradiation, were not modified in exposed crayfishes compared to the control group. CONCLUSIONS: These results confirm the validity of SMRT on young males when the breeding season is less than 4 months but exposure to X-ray should be repeated at mid-breeding season when temperatures allow a longer breeding season. © 2021 Society of Chemical Industry.

Cephalopod Behavior: From Neural Plasticity to Consciousness.

It is only in recent decades that subjective experience - or consciousness - has become a legitimate object of scientific inquiry. As such, it represents perhaps the greatest challenge facing neuroscience today. Subsumed within this challenge is the study of subjective experience in non-human animals: a particularly difficult endeavor that becomes even more so, as one crosses the great evolutionary divide between vertebrate and invertebrate phyla. Here, we explore the possibility of consciousness in one group of invertebrates: cephalopod molluscs. We believe such a review is timely, particularly considering cephalopods' impressive learning and memory abilities, rich behavioral repertoire, and the relative complexity of their nervous systems and sensory capabilities. Indeed, in some cephalopods, these abilities are so sophisticated that they are comparable to those of some higher vertebrates. Following the criteria and framework outlined for the identification of hallmarks of consciousness in non-mammalian species, here we propose that cephalopods - particularly the octopus - provide a unique test case among invertebrates for examining the properties and conditions that, at the very least, afford a basal faculty of consciousness. These include, among others: (i) discriminatory and anticipatory behaviors indicating a strong link between perception and memory recall; (ii) the presence of neural substrates representing functional analogs of thalamus and cortex; (iii) the neurophysiological dynamics resembling the functional signatures of conscious states in mammals. We highlight the current lack of evidence as well as potentially informative areas that warrant further investigation to support the view expressed here. Finally, we identify future research directions for the study of consciousness in these tantalizing animals.

Long-lasting generalization triggered by a single trial event in the invasive crayfish Procambarus clarkii.

Behavioural flexibility allows adaptation to environmental changes, a situation that invasive species have often to face when colonizing new territories. Such flexibility arises from a set of cognitive mechanisms among which generalization plays a key role, as it allows the transfer of past solutions to solve similar new problems. By means of a habituation paradigm, we studied generalization in the invasive crayfish Procambarus clarkii Once crayfish had habituated their defensive response to a specific water jet, we tested whether habituation transferred to a new type of water jet. Although habituation did not generalize when the new stimulus was initially presented, it surprisingly emerged 15 and 45 days later. Hence, remarkably, in Pclarkii, a single presentation of a new event was sufficient to trigger a long-lasting form of learning generalization from previous similar stimuli, a cognitive ability that may concur in providing adaptive advantages to this invasive species.

A standardized battery of tests to measure Octopus vulgaris' behavioural performance.

Here we introduce a series of behavioural tasks to assess inter-individual variability in behaviours exhibited by the cephalopod mollusc Octopus vulgaris. We propose that, by using octopus' predatory behavioural response, it is possible to measure: (1) the ability to adapt to the captive condition (acclimatization), (2) the response towards novel stimuli (neophobia), (3) the capability of social learning, (4) the ability of solving problems (problem solving), and (5) the response to artificial stimuli (preferences, individual learning). To assure comparability and reproducibility of results, this battery of tests is here applied to a large sample of individuals in standardized experimental conditions. Such battery of tests serves as an in vivo screening that should be adopted not only to investigate cognitive abilities in specific behavioural domains, but also to monitor the welfare status of animals under captivity, thus to check sensory functions as well as motor abilities in other investigations within the fields of biology and neuroscience. Our aim was to provide a reliable tool to exploit this animal species for research in different fields.

Context learning before birth: evidence from the chick embryo.

Learning contextual information to form associative memories with stimuli of interest is an important brain function in both human and non-human animals. Intuitively, one would expect that such a sophisticated cognitive skill develops postnatally, as the organism starts exploring the surrounding environment to search for significant contingencies among stimuli. Here we show, instead, that even before hatching, domestic chicks are capable of forming associative memories between discrete alerting sounds and the surrounding context, as attested by the fact that habituation of the freezing response to the sounds is affected by the context of stimulation. This finding indicates that, while in the egg, chicks recognize and learn the context in which they are stimulated. Hence, context learning in chicks is an innate brain function already active before birth, which can provide an immediate survival advantage to the newborns of this precocial avian species.

Distinct effect of early and late embryonic light-stimulation on chicks' lateralization.

Embryonic light exposure affects similarly functional lateralization in fish and birds. While the light acts on an asymmetric habenular system during the first post fertilization hours in zebrafish, in the domestic chicks it shapes the thalamofugal visual pathway affecting the right retinal photoreceptors in the last stages before hatching. However, recent evidence has shown that also in chicks a precocial embryonic time window seems open to light action. Here we addressed the issue of whether the light effect is comparable in the early and late sensitive periods of chicks' embryonic development by testing birds coming from early (EL) and late (LL) light stimulated eggs compared to dark maintained eggs (DK) under different conditions of vision in a gravel-grain task. The perseveration of pecks directed to irrelevant elements revealed that in all chicks the right hemisphere was heavily attracted by the novel elements when tested with the left eye. When using the right eye, instead, only DK chicks attended repeatedly to distractors whereas LL and EL chicks showed a left hemisphere advantage for fine discrimination and sustained attention; conversely, when tested binocularly, LL chicks perseverated significantly more than both DK and EL chicks, likely compensating the distraction with the analysis carried out by both hemispheres. For the first time, we unveiled a fine graded difference between the light modulation exerted during the two time windows, adding evidence to the idea that genes and environmental factors interplay in several separate routes to the modulation of the neurodevelopment of cerebral lateralization in vertebrates.

Naïve 3-day-old domestic chicks (Gallus gallus) are attracted to discrete acoustic patterns characterizing natural vocalizations.

Nonsongbirds can produce rhythmical sounds that, at times, have been shown to be meaningful in their communication. This raises the possibility that rhythm is a separate ability that might have evolved earlier than song. We asked whether nearly completely naïve domestic chicks perceive rhythm and respond in specific ways to different rhythmic patterns. To do so, specific constituent parameters of rhythmicity were used based on the sound of a natural mother hen's cluck. The sound samples created ranged from a continuous sound to articulated rhythmic patterns of alternating strong and weak events. Chicks' reactivity to the patterns was tested over a series of sound exposure experiments by their propensity to operate a running wheel toward the acoustic source, a paradigm simulating chicks' natural affiliative response to the hen's call. Results showed that motor activity increased markedly when acoustic events were discrete (compared with continuous), and significantly when accent structure was faster (compared with slower rates). Similar to human infants, chicks showed a significant preference for pulsed over continuous patterns. Chicks also ran harder toward calls with fast strong pulsating events, suggesting that different arrangements of events in time can be differently arousing, but independently of whether the events were presented in a regular or nonregular fashion. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Short-term memory in habituation and dishabituation of newborn chicks' freezing response.

Cognitive models of habituation and dishabituation postulate that the latter is attributable to the perturbation of the model of the repeated stimulation stored in short-term memory (STM) by the occurrence of a new stimulus, called dishabituator. However, although both behavioral phenomena depend on STM, previous studies in Aplysia have found that dishabituation seems to require further steps of development of the STM system to emerge. Here, we addressed whether this is a universal condition for the appearance of the 2 forms of learning, namely whether dishabituation must necessarily follow habituation. To this aim, we studied habituation and dishabituation of the freezing response to a sudden acoustic stimulation in newly hatched chicks (1 day old vs. 3 days old). The results showed that in chicks, dishabituation was fully present a few hours after hatching, a pattern of results indicating that, in this precocial avian species, habituation and dishabituation share the same developmental trajectory and the underlying STM mechanisms are simultaneously operative soon after birth. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Rapid plasticity attenuation soon after birth revealed by habituation in newborn chicks.

Habituation reflects a form of experience-dependent plasticity whereby the organism progressively learns to ignore the irrelevant information repeatedly encountered. Here, we measured the freezing response to a repeated loud noise in three groups of newborn chicks (Gallus gallus) of different ages (1-2 Day old, 2-3 Day old, and 3-4 Day old) to investigate the ontogeny of habituation in this avian species. Habituation was already present 1 Day after hatching, revealing that the neural mechanisms underlying this form of plasticity are immediately active. Unexpectedly, however, we also found that in the second Day of stimulation the amount of learning was significantly attenuated in chicks of 3-4 days of age as compared to the younger animals, thus showing that 24-48 hr of maturation were sufficient to reduce plasticity. While previous findings in other animal species have proved the existence of a precocious critical period of plasticity in early cortical areas by means of sensory deprivation, our results demonstrate that during the initial development of an intact avian brain also the degree of plasticity underlying a learning process like habituation is maximal soon after birth, and then is subject to a rapid attenuation.

Context-specific habituation of the freezing response in newborn chicks.

Previous studies have found that in mature animals habituation is context-specific in some species but not in others. Given the mixed evidence present in the literature, we decided to explore whether habituation is context-specific in newborn chicks. The results showed that 3 days after hatching, chicks were capable of using global contextual information to rapidly habituate their freezing response to a series of sudden acoustic stimuli. Our study is the 1st to show context-specific habituation in this avian species, a result in agreement with those of previous findings in adult male zebra finches (Taeniopygia guttata). Furthermore, although our study does not intend to provide a systematic investigation of the ontogeny of habituation in this species, our findings show that a few days after hatching, juvenile chicks are capable of a sophisticated associative learning process that takes into account complex environmental information. (PsycINFO Database Record

Inexperienced newborn chicks use geometry to spontaneously reorient to an artificial social partner.

A fundamental process underlying navigation behaviour, shown to occur in every species tested, uses geometric properties of the environment for location memory and orientation. Here we employ a new method to ask whether this basic geometric orientation ability is innately predisposed in the brain or depends on specific experiences navigating in a geometrically rich environment. Using the newborn domestic chick as a model system, we present a working memory task testing reorientation towards a filial imprinting object under rigorous controlled rearing conditions. In the absence of any previous exposure to a geometrically rich environment, newly hatched chicks spontaneously recovered their bearings by making use of distances and directional relations to reorient themselves to an artificial social partner. These findings provide evidence for an innate capacity to navigate by the geometric structure of the environment.

Visual hierarchical processing and lateralization of cognitive functions through domestic chicks' eyes.

Hierarchical stimuli have proven effective for investigating principles of visual organization in humans. A large body of evidence suggests that the analysis of the global forms precedes the analysis of the local forms in our species. Studies on lateralization also indicate that analytic and holistic encoding strategies are separated between the two hemispheres of the brain. This raises the question of whether precedence effects may reflect the activation of lateralized functions within the brain. Non-human animals have perceptual organization and functional lateralization that are comparable to that of humans. Here we trained the domestic chick in a concurrent discrimination task involving hierarchical stimuli. Then, we evaluated the animals for analytic and holistic encoding strategies in a series of transformational tests by relying on a monocular occlusion technique. A local precedence emerged in both the left and the right hemisphere, adding further evidence in favour of analytic processing in non-human animals.