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The song control nucleus HVC of songbirds has emerged as a widespread model system to study adult neurogenesis and the factors that modulate the incorporation of new neurons, including seasonal state, sex differences or sex steroid hormone concentrations. However, the specific function of these new neurons born in adulthood remains poorly understood. We implemented a new procedure based on focal X-ray irradiation to deplete neural progenitors in the ventricular zone adjacent to HVC and study the functional consequences. A 23 Gy dose depleted by more than 50 percent the incorporation of BrdU in neural progenitors, a depletion that was confirmed by a significant decrease in doublecortin positive neurons. This depletion of neurogenesis significantly increased the variability of testosterone-induced songs in females and decreased their bandwidth. Expression of the immediate early gene ZENK in secondary auditory areas of the telencephalon that respond to song was also inhibited. These data provide evidence that new neurons in HVC play a role in both song production and perception and that X-ray focal irradiation represents an excellent tool to advance our understanding of adult neurogenesis.

Exposure to predator scents triggers an instinctive fear response in mice, including a surge in blood levels of stress hormones; here, the amygdalo-piriform transition area is identified as provoking these hormonal responses. Neural circuits responsive to predator odours Exposure to volatile predator scents triggers an instinctive fear response in mice, including a surge in the stress hormones corticotrophin-releasing hormone (CRH), adrenocorticotropic hormone (ACTH) and corticosterone. Such stereotyped responses are likely to be mediated by hard-wired neural circuits, but the olfactory areas involved have so far remain unknown. Here Linda Buck and colleagues identify the amygdalo-piriform transition area as the only olfactory area upstream of hypothalamic CRH neurons that is activated by volatile predator odours, and show that this area mediates hormonal but not behavioural fear responses to these odours. Instinctive reactions to danger are critical to the perpetuation of species and are observed throughout the animal kingdom. The scent of predators induces an instinctive fear response in mice that includes behavioural changes, as well as a surge in blood stress hormones that mobilizes multiple body systems to escape impending danger 1 , 2 . How the olfactory system routes predator signals detected in the nose to achieve these effects is unknown. Here we identify a specific area of the olfactory cortex in mice that induces stress hormone responses to volatile predator odours. Using monosynaptic and polysynaptic viral tracers, we found that multiple olfactory cortical areas transmit signals to hypothalamic corticotropin-releasing hormone (CRH) neurons, which control stress hormone levels. However, only one minor cortical area, the amygdalo-piriform transition area (AmPir), contained neurons upstream of CRH neurons that were activated by volatile predator odours. Chemogenetic stimulation of AmPir activated CRH neurons and induced an increase in blood stress hormones, mimicking an instinctive fear response. Moreover, chemogenetic silencing of AmPir markedly reduced the stress hormone response to predator odours without affecting a fear behaviour. These findings suggest that AmPir, a small area comprising <5% of the olfactory cortex, plays a key part in the hormonal component of the instinctive fear response to volatile predator scents.

Spatial learning in teleost fish requires an intact telencephalon 1 , a brain region that contains putative analogues to components of the mammalian limbic system (for example, hippocampus) 2 – 4 . However, cells fundamental to spatial cognition in mammals—for example, place cells (PCs) 5 , 6 —have yet to be established in any fish species. In this study, using tracking microscopy to record brain-wide calcium activity in freely swimming larval zebrafish 7 , we compute the spatial information content 8 of each neuron across the brain. Strikingly, in every recorded animal, cells with the highest spatial specificity were enriched in the zebrafish telencephalon. These PCs form a population code of space from which we can decode the animal’s spatial location across time. By continuous recording of population-level activity, we found that the activity manifold of PCs refines and untangles over time. Through systematic manipulation of allothetic and idiothetic cues, we demonstrate that zebrafish PCs integrate multiple sources of information and can flexibly remap to form distinct spatial maps. Using analysis of neighbourhood distance between PCs across environments, we found evidence for a weakly preconfigured network in the telencephalon. The discovery of zebrafish PCs represents a step forward in our understanding of spatial cognition across species and the functional role of the early vertebrate telencephalon. Using a tracking microscope for freely moving animals, the authors discover a population of place cells in the zebrafish brain and demonstrate that a non-amniote brain is capable of integrating allothetic and idiothetic information to create a neural map of space.

Environmental enrichment is considered as a recommended tool to guarantee or improve the welfare of captive fish. This study demonstrates for the first time that structural environmental enrichment enhances cognition, exploratory behaviour and brain physiological functions of gilthead seabream ( Sparus aurata ). Seabream was reared in groups (n = 15) during 60 days under two different treatments: enriched tanks with plant-fibre ropes (EE) or bare/non-enriched tanks (NE). Fish were then exposed to a purpose-built maze for 1 h every second day in four trials. Analysis of video recordings showed that seabream under EE conditions presented higher overall exploratory behaviour, spatial orientation and learning capability compared to seabream from NE conditions. Results from brain monoamines analyses may suggest increased recent dopaminergic activity in telencephalon, known to be involved in learning processes; and increased serotonergic activity in cerebellum, involved in the coordination of balance, movements and orientation. In addition, EE-reared fish showed increased antioxidant activity in whole brain, with no apparent oxidative damage. Structural EE seemed to induce an hormetic response on juvenile seabream, improving their welfare status during captivity. Application of this kind of physical structure might be feasible at fish farms as a passive and non-invasive tool to improve welfare of intensively cultured seabream.

Interval timing, the ability to perceive and estimate durations between events, is essential for many animal behaviors. In mammals, it is linked to specific cortical and sub-cortical brain regions, but its neural basis in birds remains unclear. We trained two male carrion crows on a time estimation task using visual stimuli, cueing them to wait for a minimum duration of 1500 ms, 3000 ms, or 6000 ms before responding to receive a reward. During the task, we recorded activity from single neurons in the nidopallium caudolaterale (NCL), the avian executive telencephalon. Many neurons showed tuning to specific durations, suggesting that time intervals are encoded as abstract magnitudes along an ordered scale. Population-level decoding revealed that NCL activity predicted the crows’ intended wait time, independent of the sensory properties of the cues. These findings show that abstract time estimation can emerge from neural architectures different from the mammalian neocortex. It is unknown how birds estimate time using brains organized differently from mammals. Here, the authors show that neurons in the crow NCL encode duration categories, supporting abstract, cue-independent representations of time intervals.

Dorsoventral patterning of the telencephalon is established early in forebrain development and underlies many of the regional subdivisions that are critical to the later organization of neural circuits in the cerebral cortex and basal ganglia. Sonic hedgehog (Shh) is involved in the generation of the ventral-most telencephalic cells, but the identity of the extrinsic signal(s) that induce dorsal character in telencephalic cells is not known. Here we show in chick embryos that sequential Wnt and fibroblast growth factor (FGF) signaling specifies cells of dorsal telencephalic character.

The vagus nerve is the primary means of neural communication between the gastrointestinal (GI) tract and the brain. Vagally mediated GI signals activate the hippocampus (HPC), a brain region classically linked with memory function. However, the endogenous relevance of GI-derived vagal HPC communication is unknown. Here we utilize a saporin (SAP)-based lesioning procedure to reveal that selective GI vagal sensory/afferent ablation in rats impairs HPC-dependent episodic and spatial memory, effects associated with reduced HPC neurotrophic and neurogenesis markers. To determine the neural pathways connecting the gut to the HPC, we utilize monosynaptic and multisynaptic virus-based tracing methods to identify the medial septum as a relay connecting the medial nucleus tractus solitarius (where GI vagal afferents synapse) to dorsal HPC glutamatergic neurons. We conclude that endogenous GI-derived vagal sensory signaling promotes HPC-dependent memory function via a multi-order brainstem–septal pathway, thereby identifying a previously unknown role for the gut–brain axis in memory control. Feeding-relevant vagal signaling occurs between the gastrointestinal tract and the brain, but it is unclear if this pathway influences cognitive processes. This study shows that endogenous gastrointestinal derived vagal sensory signaling promotes hippocampal-dependent memory function via a multi-order brainstem–septal pathway.

Brains that are capable of representing numerosity, the number of items in a set, have arisen repeatedly and independently in different animal taxa. This review compares the cognitive and physiological mechanisms found in a nonhuman primate, the rhesus macaque, and a corvid songbird, the carrion crow, in order to elucidate the evolutionary adaptations underlying numerical competence. Monkeys and corvids are known for their advanced cognitive competence, despite them both having independently and distinctly evolved endbrains that resulted from a long history of parallel evolution. In both species, numerosity is represented as an analogue magnitude by an approximate number system that obeys the Weber–Fechner Law. In addition, the activity of numerosity-selective neurons in the fronto-parietal association cortex of monkeys and the telencephalic associative area nidopallium caudolaterale of crows mirrors the animals' performance. In both species' brains, neuronal activity is tuned to a preferred numerosity, encodes the numerical value in an approximate fashion, and is best represented on a logarithmic scale. Collectively, the data show an impressive correspondence of the cognitive and neuronal mechanisms for numerosity representations across monkeys and crows. This suggests that remotely related vertebrates with distinctly developed endbrains adopted similar physiological solutions to common computational problems in numerosity processing. This article is part of a discussion meeting issue ‘The origins of numerical abilities'.

Translating a perceived number into a matching number of self-generated actions is a hallmark of numerical reasoning in humans and animals alike. To explore this sensorimotor transformation, we trained crows to judge numerical values in displays and to flexibly plan and perform a matching number of pecks. We report number selective sensorimotor neurons in the crow telencephalon that signaled the impending number of self-generated actions. Neuronal population activity during the sensorimotor transformation period predicted whether the crows mistakenly planned fewer or more pecks than instructed. During sensorimotor transformation, both a static neuronal code characterized by persistently number-selective neurons and a dynamic code originating from neurons carrying rapidly changing numerical information emerged. The findings indicate there are distinct functions of abstract neuronal codes supporting the sensorimotor number system. Translating a perceived number into a matching number of self-generated actions is key in numerical reasoning. Here, the authors report sensorimotor neurons in the crow telencephalon that signaled the impending number of self-generated actions.

Humans’ symbolic counting skills are built on a primordial ability to approximately estimate the number of items, or numerosity. To date it is debated whether numerosities presented in categorically different formats, that is as temporal sequences versus spatial arrays, are represented abstractly in the brain. To address this issue, we identified the behavioral characteristics and neuronal codes for sequential and simultaneous number formats in crows. We find a format-dependent representation by distinct groups of selective neurons during the sensory encoding stage. However, an abstract and format-independent numerosity code emerges once the encoding phase is completed and numerosities needed to be memorized. These results suggest a successive two-stage code for categorically different number formats and help to reconcile conflicting findings observed in psychophysics and brain imaging. Numbers are processed as abstract categories, despite considerable variations in presentation formats. By recording single-neuron activity in behaving crows, the authors show successive format-dependent and format-independent numerosity codes in the avian endbrain.