Noncortical coding of biological motion in newborn chicks' brain.

Biological motion, the typical movement of vertebrates, is perceptually salient for many animal species. Newly hatched domestic chicks and human newborns show a spontaneous preference for simple biological motion stimuli (point-light displays) at birth prior to any visual learning. Despite evidence of such preference at birth, neural studies performed so far have focused on a specialized neural network involving primarily cortical areas. Here, we presented newly hatched visually naïve domestic chicks to either biological or rigid motion stimuli and measured for the first time their brain activation. Immediate Early Gene (c-Fos) expression revealed selective activation in the preoptic area of the hypothalamus and the nucleus taeniae of the amygdala. These results suggest that subpallial/subcortical regions play a crucial role in biological motion perception at hatching, paving the way for future studies on adult animals, including humans.

Number neurons in the nidopallium of young domestic chicks.

Numerical cognition is ubiquitous in the animal kingdom. Domestic chicks are a widely used developmental model for studying numerical cognition. Soon after hatching, chicks can perform sophisticated numerical tasks. Nevertheless, the neural basis of their numerical abilities has remained unknown. Here, we describe number neurons in the caudal nidopallium (functionally equivalent to the mammalian prefrontal cortex) of young domestic chicks. Number neurons that we found in young chicks showed remarkable similarities to those in the prefrontal cortex and caudal nidopallium of adult animals. Thus, our results suggest that numerosity perception based on number neurons might be an inborn feature of the vertebrate brain.

Hierarchical processing of feature, egocentric and relational information for spatial orientation in domestic chicks.

Animals can use different types of information for navigation. Domestic chicks (Gallus gallus) prefer to use local features as a beacon over spatial relational information. However, the role of egocentric navigation strategies is less understood. Here, we tested domestic chicks' egocentric and allocentric orientation abilities in a large circular arena. In experiment 1, we investigated whether domestic chicks possess a side bias during viewpoint-dependent egocentric orientation, revealing facilitation for targets on the chicks' left side. Experiment 2 showed that local features are preferred over viewpoint-dependent egocentric information when the two conflict. Lastly, in experiment 3, we found that in a situation where there is a choice between egocentric and allocentric spatial relational information provided by free-standing objects, chicks preferentially rely on egocentric information. We conclude that chicks orient according to a hierarchy of cues, in which the use of the visual appearance of an object is the dominant strategy, followed by viewpoint-dependent egocentric information and finally by spatial relational information.

Looks like home: numerosity, but not spatial frequency guides preference in zebrafish larvae (Danio rerio).

Despite their young age, zebrafish larvae have a well-developed visual system and can distinguish between different visual stimuli. First, we investigated if the first visual surroundings the larvae experience during the first days after hatching shape their habitat preference. Indeed, these animals seem to "imprint" on the first surroundings they see and select visual stimuli accordingly at 7 days post fertilization (dpf). In particular, if zebrafish larvae experience a bar background just after hatching, they later on prefer bars over white stimuli, and vice versa. We then used this acquired preference for bars to investigate innate numerical abilities. We wanted to specifically test if the zebrafish larvae show real numerical abilities or if they rely on a lower-level mechanism-i.e. spatial frequency-to discriminate between two different numerosities. When we matched the spatial frequency in stimuli with different numbers of bars, the larvae reliably selected the higher numerosity. A previous study has ruled out that 7 dpf zebrafish larvae use convex hull, cumulative surface area and density to choose between two numerosities. Therefore, our results indicate that zebrafish larvae rely on real numerical abilities rather than other cues, including spatial frequency, when spontaneously comparing two sets with different numbers of bars.

Dlk1 dosage regulates hippocampal neurogenesis and cognition.

Neurogenesis in the adult brain gives rise to functional neurons, which integrate into neuronal circuits and modulate neural plasticity. Sustained neurogenesis throughout life occurs in the subgranular zone (SGZ) of the dentate gyrus in the hippocampus and is hypothesized to be involved in behavioral/cognitive processes such as memory and in diseases. Genomic imprinting is of critical importance to brain development and normal behavior, and exemplifies how epigenetic states regulate genome function and gene dosage. While most genes are expressed from both alleles, imprinted genes are usually expressed from either the maternally or the paternally inherited chromosome. Here, we show that in contrast to its canonical imprinting in nonneurogenic regions, Delta-like homolog 1 (Dlk1) is expressed biallelically in the SGZ, and both parental alleles are required for stem cell behavior and normal adult neurogenesis in the hippocampus. To evaluate the effects of maternally, paternally, and biallelically inherited mutations within the Dlk1 gene in specific behavioral domains, we subjected Dlk1-mutant mice to a battery of tests that dissociate and evaluate the effects of Dlk1 dosage on spatial learning ability and on anxiety traits. Importantly, reduction in Dlk1 levels triggers specific cognitive abnormalities that affect aspects of discriminating differences in environmental stimuli, emphasizing the importance of selective absence of imprinting in this neurogenic niche.

Core knowledge as a neuro-ethologist views it.

Innateness of core knowledge mechanisms (in the form of "cognitive priors") can be revealed by proper comparisons of altricial and precocial species. Cognitive priors and sensitive periods in their expression may also provide clues for the development of plausible artificial intelligence systems.

Life is in motion (through a chick's eye).

Cognitive scientists, social psychologists, computer scientists, neuroscientists, ethologists and many others have all wondered how brains detect and interpret the motion of living organisms. It appears that specific cues, incorporated into our brains by natural selection, serve to signal the presence of living organisms. A simple geometric figure such as a triangle put in motion with specific kinematic rules can look alive, and it can even seem to have intentions and goals. In this article, we survey decades of parallel investigations on the motion cues that drive animacy perception-the sensation that something is alive-in non-human animals, especially in precocial species, such as the domestic chick, to identify inborn biological predispositions. At the same time, we highlight the relevance of these studies for an understanding of human typical and atypical cognitive development.

Naïve chicks do not prefer objects with stable body orientation, though they may prefer behavioural variability.

Domestic chicks (Gallus gallus domesticus) have been widely used as a model to study the motion cues that allow visually naïve organisms to detect animate agents shortly after hatching/birth. Our previous work has shown that chicks prefer to approach agents whose main body axis and motion direction are aligned (a feature typical of creatures whose motion is constrained by a bilaterally symmetric body plan). However, it has never been investigated whether chicks are also sensitive to the fact that an agent maintains a stable front-back body orientation in motion (i.e. consistency in which end is leading and which trailing). This is another feature typical of bilateria, which is also associated with the detection of animate agents in humans. The aim of the present study was to fill this gap. Contrary to our initial expectations, after testing 300 chicks across 3 experimental conditions, we found a recurrent preference for the agent which did not maintain a stable front-back body orientation. Since this preference was limited to female chicks, the results are discussed also in relation to sex differences in the social behaviour of this model. Overall, we show for the first time that chicks can discriminate agents based on the stability of their front-back orientation. The unexpected direction of the effect could reflect a preference for agents' whose behaviour is less predictable. Chicks may prefer agents with greater behavioural variability, a trait which has been associated with animate agents, or have a tendency to explore agents performing "odd behaviours".

Neurons in the Dorso-Central Division of Zebrafish Pallium Respond to Change in Visual Numerosity.

We found a region of the zebrafish pallium that shows selective activation upon change in the numerosity of visual stimuli. Zebrafish were habituated to sets of small dots that changed in individual size, position, and density, while maintaining their numerousness and overall surface. During dishabituation tests, zebrafish faced a change in number (with the same overall surface), in shape (with the same overall surface and number), or in size (with the same shape and number) of the dots, whereas, in a control group, zebrafish faced the same stimuli as during the habituation. Modulation of the expression of the immediate early genes c-fos and egr-1 and in situ hybridization revealed a selective activation of the caudal part of the dorso-central division of the zebrafish pallium upon change in numerosity. These findings support the existence of an evolutionarily conserved mechanism for approximate magnitude and provide an avenue for understanding its underlying molecular correlates.

Spontaneous preference for unpredictability in the temporal contingencies between agents' motion in naive domestic chicks.

The ability to recognize animate agents based on their motion has been investigated in humans and animals alike. When the movements of multiple objects are interdependent, humans perceive the presence of social interactions and goal-directed behaviours. Here, we investigated how visually naive domestic chicks respond to agents whose motion was reciprocally contingent in space and time (i.e. the time and direction of motion of one object can be predicted from the time and direction of motion of another object). We presented a 'social aggregation' stimulus, in which three smaller discs repeatedly converged towards a bigger disc, moving in a manner resembling a mother hen and chicks (versus a control stimulus lacking such interactions). Remarkably, chicks preferred stimuli in which the timing of the motion of one object could not be predicted by that of other objects. This is the first demonstration of a sensitivity to the temporal relationships between the motion of different objects in naive animals, a trait that could be at the basis of the development of the perception of social interaction and goal-directed behaviours.

Characterizing ontogeny of quantity discrimination in zebrafish.

A sense of non-symbolic numerical magnitudes is widespread in the animal kingdom and has been documented in adult zebrafish. Here, we investigated the ontogeny of this ability using a group size preference (GSP) task in juvenile zebrafish. Fish showed GSP from 21 days post-fertilization and reliably chose the larger group when presented with discriminations of between 1 versus 3, 2 versus 5 and 2 versus 3 conspecifics but not 2 versus 4 conspecifics. When the ratio between the number of conspecifics in each group was maintained at 1 : 2, fish could discriminate between 1 versus 2 individuals and 3 versus 6, but again, not when given a choice between 2 versus 4 individuals. These findings are in agreement with studies in other species, suggesting the systems involved in quantity representation do not operate separately from other cognitive mechanisms. Rather they suggest quantity processing in fishes may be the result of an interplay between attentional, cognitive and memory-related mechanisms as in humans and other animals. Our results emphasize the potential of the use of zebrafish to explore the genetic and neural processes underlying the ontogeny and function of number cognition.

Inexperienced preys know when to flee or to freeze in front of a threat.

Using appropriate antipredatory responses is crucial for survival. While slowing down reduces the chances of being detected from distant predators, fleeing away is advantageous in front of an approaching predator. Whether appropriate responses depend on experience with moving objects is still an open question. To clarify whether adopting appropriate fleeing or freezing responses requires previous experience, we investigated responses of chicks naive to movement. When exposed to the moving cues mimicking an approaching predator (a rapidly expanding, looming stimulus), chicks displayed a fast escape response. In contrast, when presented with a distal threat (a small stimulus sweeping overhead) they decreased their speed, a maneuver useful to avoid detection. The fast expansion of the stimulus toward the subject, rather than its size per se or change in luminance, triggered the escape response. These results show that young animals, in the absence of previous experience, can use motion cues to select the appropriate responses to different threats. The adaptive needs of young preys are thus matched by spontaneous defensive mechanisms that do not require learning.

Cortical route for facelike pattern processing in human newborns.

Humans are endowed with an exceptional ability for detecting faces, a competence that, in adults, is supported by a set of face-specific cortical patches. Human newborns, already shortly after birth, preferentially orient to faces, even when they are presented in the form of highly schematic geometrical patterns vs. perceptually equivalent nonfacelike stimuli. The neural substrates underlying this early preference are still largely unexplored. Is the adult face-specific cortical circuit already active at birth, or does its specialization develop slowly as a function of experience and/or maturation? We measured EEG responses in 1- to 4-day-old awake, attentive human newborns to schematic facelike patterns and nonfacelike control stimuli, visually presented with slow oscillatory "peekaboo" dynamics (0.8 Hz) in a frequency-tagging design. Despite the limited duration of newborns' attention, reliable frequency-tagged responses could be estimated for each stimulus from the peak of the EEG power spectrum at the stimulation frequency. Upright facelike stimuli elicited a significantly stronger frequency-tagged response than inverted facelike controls in a large set of electrodes. Source reconstruction of the underlying cortical activity revealed the recruitment of a partially right-lateralized network comprising lateral occipitotemporal and medial parietal areas overlapping with the adult face-processing circuit. This result suggests that the cortical route specialized in face processing is already functional at birth.

Efficient Low-Frequency SSVEP Detection with Wearable EEG Using Normalized Canonical Correlation Analysis.

Recent studies show that the integrity of core perceptual and cognitive functions may be tested in a short time with Steady-State Visual Evoked Potentials (SSVEP) with low stimulation frequencies, between 1 and 10 Hz. Wearable EEG systems provide unique opportunities to test these brain functions on diverse populations in out-of-the-lab conditions. However, they also pose significant challenges as the number of EEG channels is typically limited, and the recording conditions might induce high noise levels, particularly for low frequencies. Here we tested the performance of Normalized Canonical Correlation Analysis (NCCA), a frequency-normalized version of CCA, to quantify SSVEP from wearable EEG data with stimulation frequencies ranging from 1 to 10 Hz. We validated NCCA on data collected with an 8-channel wearable wireless EEG system based on BioWolf, a compact, ultra-light, ultra-low-power recording platform. The results show that NCCA correctly and rapidly detects SSVEP at the stimulation frequency within a few cycles of stimulation, even at the lowest frequency (4 s recordings are sufficient for a stimulation frequency of 1 Hz), outperforming a state-of-the-art normalized power spectral measure. Importantly, no preliminary artifact correction or channel selection was required. Potential applications of these results to research and clinical studies are discussed.

Towards a standardization of non-symbolic numerical experiments: GeNEsIS, a flexible and user-friendly tool to generate controlled stimuli.

Several studies have suggested that vertebrate and invertebrate species may possess a number sense, i.e. an ability to process in a non-symbolic and non-verbal way the numerousness of a set of items. However, this hypothesis has been challenged by the presence of other non-numerical continuous physical variables, which vary along with numerosity (i.e., any change in the number of visual physical elements in a set naturally involves a related change in visual features such as area, density, contour length and convex hull of the stimulus). It is therefore necessary to control and manipulate the continuous physical information when investigating the ability of humans and other animals to perceive numerousness. During decades of research, different methods have been implemented in order to address this issue, which has implications for experiment replicability and inter-species comparisons, since no general standardized procedure is currently being used. Here we present the 'Generation of Numerical Elements Images Software' (GeNEsIS) for the creation of non-symbolic numerical arrays in a standardized and user-friendly environment. The main aim of this tool is to provide researchers in the field of numerical cognition a manageable and precise instrument to produce visual numerical arrays controlled for all the continuous variables. Additionally, we implemented the ability to actively guide stimuli presentation during habituation/dishabituation and dual-choice comparison tasks used in human and comparative research.

Asymmetric distribution of pallial-expressed genes in zebrafish (Danio rerio).

The left and right distribution of a set of twenty-six genes in the zebrafish pallium was examined by RT-qPCR experiments. The analysis comprised four general pallial markers (eomesa, emx2, emx3 and prox1); eight genes, dapper1, htr3a, htr3b, htr4, id2, ndr2, pkcß and lmo4, that have been described as asymmetric distributed in the brain of mammals (human and mouse); six genes, arrb2, auts2, baiap2, fez1, gap43 and robo1, asymmetrically distributed in the mammalian cortex, that have been associated with autism in humans; and, eight genes, baz1b, fzd9, limk1, tubgcp5, cyfip1, grik1a, nipa1 and nipa2, which have been associated with developmental dyscalculia, a brain disability linked to brain laterality in humans. We found a leftward bias in the expression of 10 genes (dapper1, htr3a, htr3b, htr4, id2, ndr2, pkcß, auts2, baiap2 and grik1a) and a rightward bias for 5 genes (lmo4, arrb2, fez1, gap43, robo1) in agreement with the data reported in mammals. We also found a rightward lateralization for nipa1 and nipa2, whereas the remaining genes (eomesa, emx2, emx3, prox1, baz1b, cyfip1, fzd9, limk1 and tubgpc5) were bilaterally distributed. These findings suggest a basic homology in the asymmetric expression of several pallial vertebrate genes.

The rose and the fly. A conjecture on the origin of consciousness.

The Scottish philosopher Thomas Reid and more recently the evolutionary psychologist Nicholas Humphrey argued for a basic distinction between sensation (what is happening to me) and perception (what is happening out there) with the former, but not the latter, being associated with consciousness. Conscious experiences in this view would emerge from changes in the state of the body, i.e. as bodily actions, and would maintain such a primal characteristic nowadays. I argue that the evolutionary reason for the sensation/perception distinction can be traced back to organisms' movement, and to the consequent need to tell apart two varieties of an otherwise identical local stimulation: namely, either as the outcome of external stimuli passively impinging on body surface or as the outcome of an organism movement giving rise to encountering with external stimuli. The Erich von Holst Reafferenzprinzip effectively modelled such a distinction by postulating that an efference copy is generated in association with the motor command thus nullifying any sensory signal that arises as a by-product of an organism movement. I argue that if sensation originally equates to a bodily action (or its internalized representation), then it could be that an efference copy of local (or internalized) bodily action is generated under stimulation and compared to that associated with active motor command. This way the result would be leaving sensation (what is happening to me) or nullifying it and leaving only perception (what is happening out there) depending on whether or not a motor command has occurred. Implications of this hypothesis for the presence of consciousness in animals or other organisms such as plants are briefly discussed.

A sense of number in invertebrates.

Non-symbolic numerical abilities are widespread among vertebrates due to their important adaptive value. Moreover, these abilities were considered peculiar of vertebrate species as numerical competence is regarded as cognitively sophisticated. However, recent evidence convincingly showed that this is not the case: invertebrates, with their limited number of neurons, proved able to successfully discriminate different quantities (e.g., of prey), to use the ordinal property of numbers, to solve arithmetic operations as addition and subtraction and even to master the concept of zero numerosity. To date, though, the debate is still open on the presence and the nature of a «sense of number¼ in invertebrates. Whether this is peculiar for discrete countable quantities (numerosities) or whether this is part of a more general magnitude system dealing with both discrete and continuous quantities, as hypothesized for humans and other vertebrates. Here we reviewed the main studies on numerical abilities of invertebrates, discussing in particular the recent findings supporting the hypothesis of a general mechanism that allows for processing of both discrete (i.e., number) and continuous dimensions (e.g., space).

Steps towards a computational ethology: an automatized, interactive setup to investigate filial imprinting and biological predispositions.

Soon after hatching, the young of precocial species, such as domestic chicks or ducklings, learn to recognize their social partner by simply being exposed to it (imprinting process). Even artificial objects or stimuli displayed on monitor screens can effectively trigger filial imprinting, though learning is canalized by spontaneous preferences for animacy signals, such as certain kinds of motion or a face-like appearance. Imprinting is used as a behavioural paradigm for studies on memory formation, early learning and predispositions, as well as number and space cognition, and brain asymmetries. Here, we present an automatized setup to expose and/or test animals for a variety of imprinting experiments. The setup consists of a cage with two high-frequency screens at the opposite ends where stimuli are shown. Provided with a camera covering the whole space of the cage, the behaviour of the animal is recorded continuously. A graphic user interface implemented in Matlab allows a custom configuration of the experimental protocol, that together with Psychtoolbox drives the presentation of images on the screens, with accurate time scheduling and a highly precise framerate. The setup can be implemented into a complete workflow to analyse behaviour in a fully automatized way by combining Matlab (and Psychtoolbox) to control the monitor screens and stimuli, DeepLabCut to track animals' behaviour, Python (and R) to extract data and perform statistical analyses. The automated setup allows neuro-behavioural scientists to perform standardized protocols during their experiments, with faster data collection and analyses, and reproducible results.

Response of male and female domestic chicks to change in the number (quantity) of imprinting objects.

When facing two sets of imprinting objects of different numerousness, domestic chicks prefer to approach the larger one. Given that choice for familiar and novel stimuli in imprinting situations is known to be affected by the sex of the animals, we investigated how male and female domestic chicks divide the time spent in the proximity of a familiar versus an unfamiliar number of objects, and how animals interact (by pecking) with these objects. We confirmed that chicks discriminate among the different numerousnesses, but we also showed that females and males behave differently, depending on the degree of familiarity of the objects. When objects in the testing sets were all familiar, females equally explored both sets and pecked at all objects individually. Males instead selectively approached the familiar numerousness and pecked more at it. When both testing sets comprised familiar as well as novel objects, both males and females approached the larger numerousness of familiar objects. However, chicks directed all their pecks toward the novel object within the set. Differences in the behavior of males and females can be accounted for in terms of sex difference in the motivation to reinstate social contact with the familiar objects and to explore novel ones, likely associated with the ecology and the social structure of the species before domestication.