The evolution of brain architectures for predictive coding and active inference

This article considers the evolution of brain architectures for predictive processing. We argue that brain mechanisms for predictive perception and action are not late evolutionary additions of advanced creatures like us. Rather, they emerged gradually from simpler predictive loops (e.g. autonomic and motor reflexes) that were a legacy from our earlier evolutionary ancestors—and were key to solving their fundamental problems of adaptive regulation. We characterize simpler-to-more-complex brains formally, in terms of generative models that include predictive loops of increasing hierarchical breadth and depth. These may start from a simple homeostatic motif and be elaborated during evolution in four main ways: these include the multimodal expansion of predictive control into an allostatic loop; its duplication to form multiple sensorimotor loops that expand an animal's behavioural repertoire; and the gradual endowment of generative models with hierarchical depth (to deal with aspects of the world that unfold at different spatial scales) and temporal depth (to select plans in a future-oriented manner). In turn, these elaborations underwrite the solution to biological regulation problems faced by increasingly sophisticated animals. Our proposal aligns neuroscientific theorising—about predictive processing—with evolutionary and comparative data on brain architectures in different animal species. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Evolution of behavioural control from chordates to primates

This article outlines a hypothetical sequence of evolutionary innovations, along the lineage that produced humans, which extended behavioural control from simple feedback loops to sophisticated control of diverse species-typical actions. I begin with basic feedback mechanisms of ancient mobile animals and follow the major niche transitions from aquatic to terrestrial life, the retreat into nocturnality in early mammals, the transition to arboreal life and the return to diurnality. Along the way, I propose a sequence of elaboration and diversification of the behavioural repertoire and associated neuroanatomical substrates. This includes midbrain control of approach versus escape actions, telencephalic control of local versus long-range foraging, detection of affordances by the dorsal pallium, diversified control of nocturnal foraging in the mammalian neocortex and expansion of primate frontal, temporal and parietal cortex to support a wide variety of primate-specific behavioural strategies. The result is a proposed functional architecture consisting of parallel control systems, each dedicated to specifying the affordances for guiding particular species-typical actions, which compete against each other through a hierarchy of selection mechanisms. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Evaluating Environmental Enrichment Methods in Three Zoo-Housed Varanidae Lizard Species

Environmental enrichment has been shown to enhance the behavioural repertoire and reduce the occurrence of abnormal behaviours, particularly in zoo-housed mammals. However, evidence of its effectiveness in reptiles is lacking. Previously, it was believed that reptiles lacked the cognitive sophistication to benefit from enrichment provision, but studies have demonstrated instances of improved longevity, physical condition and problem-solving behaviour as a result of enhancing husbandry routines. In this study, we evaluate the effectiveness of food- and scent-based enrichment for three varanid species (Komodo dragon, emerald tree monitor lizard and crocodile monitor). Scent piles, scent trails and hanging feeders resulted in a significant increase in exploratory behaviour, with engagement diminishing ≤330 min post provision. The provision of food- versus scent-based enrichment did not result in differences in enrichment engagement across the three species, suggesting that scent is just as effective in increasing natural behaviours. Enhancing the environment in which zoo animals reside is important for their health and wellbeing and also provides visitors with the opportunity to observe naturalistic behaviours. For little known and understudied species such as varanids, evidence of successful (and even unsuccessful) husbandry and management practice is vital for advancing best practice in the zoo industry.

From the Point of View of the Chickens: What Difference Does a Window Make?

We aimed to investigate what broiler chickens prefer when given free choice between a barn side with artificial lighting only as opposed to the other barn side with natural light through glass windows and artificial light. Eighty-five 1 day-old male Cobb 500 broiler chickens were divided into 10 pens; half of each pen area was provided with only artificial light (OAL) and the other half with natural and artificial light (NAL), and birds were free to move across sides. Environmental indicators and external conditions such as temperature, relative humidity, air velocity, ammonia and illuminance were monitored inside and outside the barn. Chickens’ preference was registered each three days, divided in categories: I (at 9, 12, and 15 days), II (at 18, 21, 24, and 27 days), and III (at 30, 33 and 36 days). The effect of the interaction between environmental indicators and week was statistically different only for illuminance. Chickens preferred NAL to OAL from 18 days onwards (II p < 0.001; III p = 0.016). Drinking (p = 0.034) and exploration or locomotion (p = 0.042) behaviours were more frequent, and “not visible” behaviours (p < 0.001) were less frequent, in NAL. Foraging was the only behaviour with an interaction effect between age category and light treatment, as birds during period II expressed this behaviour more frequently in NAL than OAL (p = 0.003). For our experimental conditions, the chickens preferred NAL from 18 days of age onwards, when the confounding effect of the heating light was removed, and their behavioural repertoire was also different according to each side of the barn and to their ages.

Ectoedemia argyropeza (Zeller, 1839) sur Peuplier Tremble : traits de comportement inférés à partir de la distribution des traces d’activités subsistant sur les feuilles-hôtes (Lepidoptera, Nepticulidae)

Ectoedemia argyropeza on Aspen leaves: deciphering retrospectively some behavioural traits from the distribution of traces of the insect activities subsisting on host-leaves (Lepidoptera, Nepticulidae). Despite their usually small size, endotrophic insects —especially those whose larvae are mining into their host-leaves— exhibit patterns of behaviour that are often more elaborate than what is usually seen in many ectotrophic herbivorous insects. However, since it is generally difficult to capture properly these behaviours in the field, precisely due to the small size of these insects, it turns out to be more convenient attempting to uncover retrospectively some of these behaviours on the basis of their resulting traces which subsist on the host-leaves. In order to be able to infer reliable information from this retrospective approach, the examination of a substantial number of host leaves and the support of appropriate statistical tests are required. The present study concerns a species of microlepidoptera, Ectoedemia argyropeza, whose caterpillars are exclusively mining the leaves of Aspen (Populus tremula) and which is still further distinguished, in a remarkable manner, by the induction of a preliminary galling (“cecidian”) development stage. This unusual combination of life traits contributes to enrich the insect’s behavioural repertoire and therefore offers a more promising field of investigation. For this species, I more particularly focus on the way the artefacts resulting from the insect activities are distributed spatially, on (or in) the host leaf, namely: (i) the spatial distribution of eggs deposited on the host-leaf petiole, (ii) the hierarchy of preferential positioning of the caterpillar corridor in the section of the petiole, hypertrophied by the cecidogenic reaction, (iii) the hierarchy of preferential locations of mines in the host-leaf blade. Were also tested, on the one hand, the existence (or not) of paired relationships between each of the three categories of distributions mentioned above and, on the other hand, the degree of conformation of each of these different distributions to the bilateral symmetry of the leaf support. The behavioural aspects that can be tentatively inferred from the above information are subsequently discussed.

Marmosets: a promising model for probing the neural mechanisms underlying complex visual networks such as the frontal–parietal network

The technology, methodology and models used by visual neuroscientists have provided great insights into the structure and function of individual brain areas. However, complex cognitive functions arise in the brain due to networks comprising multiple interacting cortical areas that are wired together with precise anatomical connections. A prime example of this phenomenon is the frontal–parietal network and two key regions within it: the frontal eye fields (FEF) and lateral intraparietal area (area LIP). Activity in these cortical areas has independently been tied to oculomotor control, motor preparation, visual attention and decision-making. Strong, bidirectional anatomical connections have also been traced between FEF and area LIP, suggesting that the aforementioned visual functions depend on these inter-area interactions. However, advancements in our knowledge about the interactions between area LIP and FEF are limited with the main animal model, the rhesus macaque, because these key regions are buried in the sulci of the brain. In this review, we propose that the common marmoset is the ideal model for investigating how anatomical connections give rise to functionally-complex cognitive visual behaviours, such as those modulated by the frontal–parietal network, because of the homology of their cortical networks with humans and macaques, amenability to transgenic technology, and rich behavioural repertoire. Furthermore, the lissencephalic structure of the marmoset brain enables application of powerful techniques, such as array-based electrophysiology and optogenetics, which are critical to bridge the gaps in our knowledge about structure and function in the brain.

Behaviour of cranes (family Gruidae) mirrors their phylogenetic relationships

Background The behavioural repertoire of every species evolved over time and its evolution can be traced through the phylogenetic relationships in distinct groups. Cranes (family Gruidae) represent a small, old, monophyletic group with well-corroborated phylogenetic relationships on the species level, and at the same time they exhibit a complex and well-described behavioural repertoire. Methods We therefore investigated the evolution of behavioural traits of cranes in a phylogenetic context using several phylogenetic approaches and two types of trait scoring. The cranes exhibit more than a hundred behavioural displays, almost one third of which may be phylogenetically informative. Results More than half of the analysed traits carry a significant phylogenetic signal. The ancestor of cranes already exhibited a quite complex behavioural repertoire, which remained unchanged in Balearicinae but altered greatly in Gruinae, specifically by the shedding of traits rather than their creation. Trait scoring has an influence on results within the Gruinae, primarily in genera Bugeranus and Anthropoides. Conclusions Albeit the behavioural traits alone cannot be used for resolving species-level relationships within the Gruidae, when optimized on molecular tree, they can help us to detect interesting evolutionary transformations of behaviour repertoire within Gruiformes. The Limpkin (Aramus guarauna) seems to be the most enigmatic species and should be studied in detail for its behavioural repertoire, which may include some precursors of crane behavioural traits.

Synergy between behavioural research on beluga whales (Delphinapterus leucas) conducted in zoological and wild settings

Behavioural observations of captive beluga whales have complemented and extended much of what has been learnt about this species in the wild. Aquarium-based research has provided finer-scale specificity for many topics, including the seasonal breeding pattern that is characteristic of this species, as well as socio-sexual behaviour that appears to be an important part of the behavioural repertoire of this species. One example is a strong propensity for male–male social interactions that begin to develop at an early age. In addition, detailed behavioural milestones in calves have been documented in ways that extend that which have been collected from wild populations. These include swim positions with mother, separations/reunions with mother, and other social interactions, and play. Characteristics of beluga maternal care have also been studied more often in captive settings than in the wild, particularly with respect to details pertaining to nursing behaviour, individual differences in maternal style and allomaternal care. Other topics that have received scientific scrutiny in zoological settings include individual differences and behavioural laterality. Thus, a greater understanding of beluga behavioural biology has the potential to emerge as a consequence of synergy between research conducted in the two settings.

The voices of an alleged mute: sound emissions in a Tropidurus lizard

Although the major Squamata lineages are primarily oriented by chemical or visual sensory systems, many lizards are able to use acoustic information and several species produce sounds. However, while gekkotans are renowned by their complex vocal repertoires, sounds of other lizards are much less known. Herein we characterize the sounds emitted by individuals of Tropidurus catalanensis (Tropiduridae) from southeastern Brazil in response to threat stimuli. Our results revealed that the acoustic display was consistently emitted by adult individuals. The typical sound emission consisted of a single click, very short in duration, and without frequency modulation. This is the first report of sound emission by Tropidurus lizards, expanding the knowledge on the behavioural repertoire of the genus, and contributing to understanding the extension of sound emission in lizards.

Biomechanical demands of percussive techniques in the context of early stone toolmaking

Recent discoveries in archaeology and palaeoanthropology highlight that stone tool knapping could have emerged first within the genera Australopithecus or Kenyanthropus rather than Homo . To explore the implications of this hypothesis determining the physical demands and motor control needed for performing the percussive movements during the oldest stone toolmaking technology (i.e. Lomekwian) would help. We analysed the joint angle patterns and muscle activity of a knapping expert using three stone tool replication techniques: unipolar flaking on the passive hammer (PH), bipolar (BP) flaking on the anvil, and multidirectional and multifacial flaking with free hand (FH). PH presents high levels of activity for Biceps brachii and wrist extensors and flexors. By contrast, BP and FH are characterized by high solicitation of forearm pronation. The synergy analyses depict a high muscular and kinematic coordination. Whereas the muscle pattern is very close between the techniques, the kinematic pattern is more variable, especially for PH. FH displays better muscle coordination and conversely lesser joint angle coordination. These observations suggest that the transition from anvil and hammer to freehand knapping techniques in early hominins would have been made possible by the acquisition of a behavioural repertoire producing an evolutionary advantage that gradually would have been beneficial for stone tool production.