Nidopallium Caudolaterale Research Articles

Functional MRI of imprinting memory in awake newborn domestic chicks

Filial imprinting, a crucial ethological paradigm, provides insights into the neurobiology of early learning and its long-term impact on behaviour. To date, invasive techniques like autoradiography or lesions have been used to study it, limiting the exploration of whole brain networks. Recent advances in fMRI for avian brains now open new windows to explore bird’s brain functions at the network level. We developed an fMRI technique for awake, newly hatched chicks, capturing BOLD signal changes during imprinting experiments. While early memory acquisition phases are understood, long-term storage and retrieval remain unclear. Our findings identified potential long-term storage of imprinting memories across a neural network, including the hippocampal formation, the medial striatum, the arcopallium, and the prefrontal-like nidopallium caudolaterale. This paradigm opens up new avenues for exploring the broader landscape of learning and memory in neonatal vertebrates, enhancing our understanding of behaviour and brain networks.

Innate responses to numerousness reveal neural activation in different brain regions in newly-hatched visually naïve chicks

Whether non-symbolic encoding of quantity is predisposed at birth with dedicated hard-wired neural circuits is debated. Here we presented newly-hatched visually naive chicks with stimuli (flashing dots) of either identical or different numerousness (with a ratio 1:3) with their continuous physical appearance (size, contour length, density, convex hull) randomly changing. Chicks spontaneously tell apart the stimuli on the basis of the number of elements. Upon presentation of either fixed or changing numerousness chicks showed different expression of early gene c-fos in the visual Wulst, the hippocampal formation, the intermediate medial mesopallium, and the caudal part of the nidopallium caudolaterale. The results support the hypothesis that the ability to discriminate quantities does not require any specific instructive experience and involves a neural network with several populations of number-selective neurons. Evidence for innateness of non-symbolic numerical cognition have implications for both neurobiology and philosophy of mathematics.

Input and Output Connections of the Crow Nidopallium Caudolaterale.

The avian telencephalic structure nidopallium caudolaterale (NCL) functions as an analog to the mammalian prefrontal cortex. In crows, corvid songbirds, it plays a crucial role in higher cognitive and executive functions. These functions rely on the NCL's extensive telencephalic connections. However, systematic investigations into the brain-wide connectivity of the NCL in crows or other songbirds are lacking. Here, we studied its input and output connections by injecting retrograde and anterograde tracers into the carrion crow NCL. Our results, mapped onto a published carrion crow brain atlas, confirm NCL multisensory connections and extend prior pigeon findings by identifying a novel input from the hippocampal formation. Furthermore, we analyze crow NCL efferent projections to the arcopallium and report newly identified arcopallial neurons projecting bilaterally to the NCL. These findings help to clarify the role of the NCL as central executive hub in the corvid songbird brain.

Parallel executive pallio-motor loops in the pigeon brain.

A core component of the avian pallial cognitive network is the multimodal nidopallium caudolaterale (NCL) that is considered to be analogous to the mammalian prefrontal cortex (PFC). The NCL plays a key role in a multitude of executive tasks such as working memory, decision-making during navigation, and extinction learning in complex learning environments. Like the PFC, the NCL is positioned at the transition from ascending sensory to descending motor systems. For the latter, it sends descending premotor projections to the intermediate arcopallium (AI) and the medial striatum (MSt). To gain detailed insight into the organization of these projections, we conducted several retrograde and anterograde tracing experiments. First, we tested whether NCL neurons projecting to AI (NCLarco neurons) and MSt (NCLMSt neurons) are constituted by a single neuronal population with bifurcating neurons, or whether they form two distinct populations. Here, we found two distinct projection patterns to both target areas that were associated with different morphologies. Second, we revealed a weak topographic projection toward the medial and lateral striatum and a strong topographic projection toward AI with clearly distinguishable sensory termination fields. Third, we investigated the relationship between the descending NCL pathways to the arcopallium with those from the hyperpallium apicale, which harbors a second major descending pathway of the avian pallium. We embed our findings within a system of parallel pallio-motor loops that carry information from separate sensory modalities to different subpallial systems. Our results also provide insights into the evolution of the avian motor system from which, possibly, the song system has emerged.

Enhanced Hippocampus–Nidopallium Caudolaterale Interaction in Visual–Spatial Associative Learning of Pigeons

Enhanced Hippocampus–Nidopallium Caudolaterale Interaction in Visual–Spatial Associative Learning of Pigeons

Conscious Experience of Stimulus Presence and Absence Is Actively Encoded by Neurons in the Crow Brain.

The emergence of consciousness from brain activity constitutes one of the great riddles in biology. It is commonly assumed that only the conscious perception of the presence of a stimulus elicits neuronal activation to signify a "neural correlate of consciousness," whereas the subjective experience of the absence of a stimulus is associated with a neuronal resting state. Here, we demonstrate that the two subjective states "stimulus present" and "stimulus absent" are represented by two specialized neuron populations in crows, corvid birds. We recorded single-neuron activity from the nidopallium caudolaterale of crows trained to report the presence or absence of images presented near the visual threshold. Because of the task design, neuronal activity tracking the conscious "present" versus "absent" percept was dissociated from that involved in planning a motor response. Distinct neuron populations signaled the subjective percepts of "present" and "absent" by increases in activation. The response selectivity of these two neuron populations was similar in strength and time course. This suggests a balanced code for subjective "presence" versus "absence" experiences, which might be beneficial when both conscious states need to be maintained active in the service of goal-directed behavior.

Convergent Circuit Computation for Categorization in the Brains of Primates and Songbirds.

Categorization is crucial for behavioral flexibility because it enables animals to group stimuli into meaningful classes that can easily be generalized to new circumstances. A most abstract quantitative category is set size, the number of elements in a set. This review explores how categorical number representations are realized by the operations of excitatory and inhibitory neurons in associative telencephalic microcircuits in primates and songbirds. Despite the independent evolution of the primate prefrontal cortex and the avian nidopallium caudolaterale, the neuronal computations of these associative pallial circuits show surprising correspondence. Comparing cellular functions in distantly related taxa can inform about the evolutionary principles of circuit computations for cognition in distinctly but convergently realized brain structures.

Working memory performance is tied to stimulus complexity

Working memory is the cognitive capability to maintain and process information over short periods. Behavioral and computational studies have shown that visual information is associated with working memory performance. However, the underlying neural correlates remain unknown. To identify how visual information affects working memory performance, we conducted behavioral experiments in pigeons (Columba livia) and single unit recordings in the avian prefrontal analog, the nidopallium caudolaterale (NCL). Complex pictures featuring luminance, spatial and color information, were associated with higher working memory performance compared to uniform gray pictures in conjunction with distinct neural coding patterns. For complex pictures, we found a multiplexed neuronal code displaying visual and value-related features that switched to a representation of the upcoming choice during a delay period. When processing gray stimuli, NCL neurons did not multiplex and exclusively represented the choice already during stimulus presentation and throughout the delay period. The prolonged representation possibly resulted in a decay of the memory trace ultimately leading to a decrease in performance. In conclusion, we found that high stimulus complexity is associated with neuronal multiplexing of the working memory representation possibly allowing a facilitated read-out of the neural code resulting in enhancement of working memory performance.

Association neurons in the crow telencephalon link visual signs to numerical values.

Many animals can associate signs with numerical values and use these signs in a goal-directed way during task performance. However, the neuronal basis of this semantic association has only rarely been investigated, and so far only in primates. How mechanisms of number associations are implemented in the distinctly evolved brains of other animal taxa such as birds is currently unknown. Here, we explored this semantic number-sign mapping by recording single-neuron activity in the crows' nidopallium caudolaterale (NCL), a brain structure critically involved in avian numerical cognition. Crows were trained to associate visual shapes with varying numbers of items in a number production task. The responses of many NCL neurons during stimulus presentation reflected the numerical values associated with visual shapes in a behaviorally relevant way. Consistent with the crow's better behavioral performance with signs, neuronal representations of numerical values extracted from shapes were more selective compared to those from dot arrays. The existence of number association neurons in crows points to a phylogenetic preadaptation of the brains of cognitively advanced vertebrates to link visual shapes with numerical meaning.

Glucocorticoid receptor expression in blood, but not across brain regions, reveals long-term effects of early life adversity in zebra finches

Early-life environment can affect organisms for life on many levels. The glucocorticoid receptor (GR) gene has a pivotal role mediating organismal physiological and behavioral responses to environmental change, and is sensitive to early-life environmental conditions and epigenetic programming. Longitudinal studies require non-lethal sampling of peripheral tissues (e.g. blood), but this approach is dependent on the extent to which GR expression in peripheral tissues covaries with GR expression in central tissues. To test for the long-term effects of early life adversity on GR expression across brain and peripheral tissues, we manipulated developmental conditions of captive zebra finches (n = 45), rearing them in either benign or harsh conditions through manipulation of parental foraging costs. We measured relative GR mRNA expression in blood and five brain regions in adulthood: hippocampus, hypothalamus, amygdala, ventral striatum, and the nidopallium caudolaterale (analogous to the mammalian prefrontal cortex), using qPCR. We further tested whether GR expression was modulated by natal brood size (which affected growth), age at sampling, and sex. GR expression correlations among tissues varied widely in magnitude and direction, ranging from -0.27 to +0.80, indicating that our understanding of developmental effects on GR expression and associated phenotypes needs to be region specific rather than organism wide. A more consistent pattern was that GR expression increased with age in blood, ventral striatum and hippocampus; GR expression was independent of age in other tissues. Developmental treatment did not affect GR expression in any of the tissues measured directly, but in blood and ventral striatum of adult females we found a positive correlation between nestling mass and GR expression. Thus, GR expression in blood was affected by early life conditions as reflected in growth in adult females, a pattern also found in one brain tissue, but not ubiquitous across brain regions. These results point at sex-dependent physiological constraints during development, shaping early life effects on GR expression in females only. Further study is required to investigate whether these tissue-dependent effects more generally reflect tissue-dependent long-term effects of early life adversity. This, together with investigating the physiological consequences of GR expression levels on individual performance and coping abilities, will be fundamental towards understanding the mechanisms mediating long-term impacts of early life, and the extent to which these can be quantified through non-lethal sampling.

Performance Baseline of Phase Transfer Entropy Methods for Detecting Animal Brain Area Interactions.

Objective: Phase transfer entropy (TEθ) methods perform well in animal sensory-spatial associative learning. However, their advantages and disadvantages remain unclear, constraining their usage. Method: This paper proposes the performance baseline of the TEθ methods. Specifically, four TEθ methods are applied to the simulated signals generated by a neural mass model and the actual neural data from ferrets with known interaction properties to investigate the accuracy, stability, and computational complexity of the TEθ methods in identifying the directional coupling. Then, the most suitable method is selected based on the performance baseline and used on the local field potential recorded from pigeons to detect the interaction between the hippocampus (Hp) and nidopallium caudolaterale (NCL) in visual-spatial associative learning. Results: (1) This paper obtains a performance baseline table that contains the most suitable method for different scenarios. (2) The TEθ method identifies an information flow preferentially from Hp to NCL of pigeons at the θ band (4-12 Hz) in visual-spatial associative learning. Significance: These outcomes provide a reference for the TEθ methods in detecting the interactions between brain areas.

Artificial night illumination disrupts sleep, and attenuates mood and learning in diurnal animals: evidence from behavior and gene expression studies in zebra finches.

This study investigated the effects of an illuminated night on sleep, mood, and cognitive performance in non-seasonal diurnal zebra finches that were exposed for 6weeks to an ecologically relevant dimly lit night (12L:12dLAN; 150lx: 5lx) with controls on the dark night (12L:12D; 150lx: < 0.01lx). Food and water were provided ad libitum. Under dLAN (dim light at night), birds showed disrupted nocturnal (frequent awakenings) and overall decreased sleep duration. They also exhibited a compromised novel object exploration, a marker of the bird's mood state, and committed more errors, took significantly longer duration to learn with low retrieval performance of the learned task when tested for a color-discrimination (learning) task under the dLAN. Further, compared to controls, there was reduced mRNA expression level of genes involved in the neurogenesis, neural plasticity (bdnf, dcx and egr1) and motivation (th, drd2, taar1 and htr2c; dopamine synthesis and signaling genes) in the brain (hippocampus (HP), nidopallium caudolaterale (NCL), and midbrain) of birds under dLAN. These results show concurrent negative behavioral and molecular neural effects of the dimly illuminated nights, and provide insights into the possible impact on sleep and mental health in diurnal species inhabiting an increasingly urbanized ecosystem.

Categorising: Inside the crow’s brain

Crows can learn to categorise line lengths into experimenter-defined categories. The crow's brain codes and recodes line lengths in individual neurons in the nidopallium caudolaterale, part of the telencephalon.

Categorical representation of abstract spatial magnitudes in the executive telencephalon of crows

The ability to group abstract continuous magnitudes into meaningful categories is cognitively demanding but key to intelligent behavior. To explore its neuronal mechanisms, we trained carrion crows to categorize lines of variable lengths into arbitrary "short" and "long" categories. Single-neuron activity in the nidopallium caudolaterale (NCL) of behaving crows reflected the learned length categories of visual stimuli. The length categories could be reliably decoded from neuronal population activity to predict the crows' conceptual decisions. NCL activity changed with learning when a crow was retrained with the same stimuli assigned to more categories with new boundaries ("short", "medium," and "long"). Categorical neuronal representations emerged dynamically so that sensory length information at the beginning of the trial was transformed into behaviorally relevant categorical representations shortly before the crows' decision making. Our data show malleable categorization capabilities for abstract spatial magnitudes mediated by the flexible networks of the crow NCL.

Executive Control of Sequence Behavior in Pigeons Involves Two Distinct Brain Regions.

Executive functions arise from multiple regions of the brain acting in concert. To facilitate such cross-regional computations, the brain is organized into distinct executive networks, like the frontoparietal network. Despite similar cognitive abilities across many domains, little is known about such executive networks in birds. Recent advances in avian fMRI have shown a possible subset of regions, including the nidopallium caudolaterale (NCL) and the lateral part of medial intermediate nidopallium (NIML), that may contribute to complex cognition, forming an action control system of pigeons. We investigated the neuronal activity of NCL and NIML. Single-cell recordings were obtained during the execution of a complex sequential motor task that required executive control to stop executing one behavior and continue with a different one. We compared the neuronal activity of NIML to NCL and found that both regions fully processed the ongoing sequential execution of the task. Differences arose from how behavioral outcome was processed. Our results indicate that NCL takes on a role in evaluating outcome, while NIML is more tightly associated with ongoing sequential steps. Importantly, both regions seem to contribute to overall behavioral output as parts of a possible avian executive network, crucial for behavioral flexibility and decision-making.

Neural correlates of cognitively controlled vocalizations in a corvid songbird

The neuronal basis of the songbird's song system is well understood. However, little is known about the neuronal correlates of the executive control of songbird vocalizations. Here, we record single-unit activity from the pallial endbrain region "nidopallium caudolaterale" (NCL) of crows that vocalize to the presentation of a visual go-cue but refrain from vocalizing during trials without a go-cue. We find that the preparatory activity of single vocalization-correlated neurons, but also of the entire population of NCL neurons, before vocal onset predicts whether or not the crows will produce an instructed vocalization. Fluctuations in baseline neuronal activity prior to the go-cue influence the premotor activity of such vocalization-correlated neurons and seemingly bias the crows' decision to vocalize. Neuronal response modulation significantly differs between volitional and task-unrelated vocalizations. This suggests that the NCL can take control over the vocal motor network during the production of volitional vocalizations in a corvid songbird.

Goal given moment modulates the time period of gamma oscillations in nidopallium caudolaterale during the goal-directed behavior of pigeon

The cognitive processes of goal-directed navigation are believed to be organized around and serve the identification and selection of goals. Differences in LFP signals in avian nidopallium caudolaterale (NCL) under different goal location/distance information in the goal-directed behavior have been studied. However, for goals that are multifarious constructs that include various information, the modulation of goal time information on the LFP of NCL during goal-directed behavior remains unclear. In this study, we recorded the LFP activity from the NCL of eight pigeons as they performed two goal-directed decision-making tasks in a plus-maze. During the two tasks with different goal time information, spectral analysis revealed significant LFP power selectively enhanced in the slow gamma band (40–60 Hz), while the slow gamma band of LFP which could effectively decode the behavioral goal of the pigeons existed in different time periods. These findings suggest that the LFP activity in the gamma band correlates with the goal-time information, and help to shed light on the contribution of the gamma rhythm recorded from the NCL in goal-directed behavior.

Morphology of the “prefrontal” nidopallium caudolaterale in the long-distance night-migratory Eurasian blackcap (Sylvia atricapilla)

Migrating birds have developed remarkable navigational capabilities to successfully master biannual journeys between their breeding and wintering grounds. To reach their intended destination, they need to calculate navigational goals from a large variety of natural directional and positional cues to set a meaningful motor output command. One brain area, which has been associated with such executive functions, is the nidopallium caudolaterale (NCL), which, due to its striking similarities in terms of neurochemistry, connectivity and function, is considered analogous to the mammalian prefrontal cortex. To establish a baseline for further analyses elucidating the neuronal correlates underlying avian navigation, we performed quantitative and qualitative analyses of dopaminergic fibres in the brains of long-distance night-migratory Eurasian blackcaps (Sylvia atricapilla). We identified four regions in the caudal telencephalon, each of which was characterized by its specific dopaminergic innervation pattern. At least three of them presumably constitute subareas of the NCL in Eurasian blackcaps and could thus be involved in integrating navigational input from different sensory systems. The observed heterogeneity and parcellation of the NCL subcompartments in this migratory species could be a consequence of the special demands related to navigation.

Night melatonin levels affect cognition in diurnal animals: Molecular insights from a corvid exposed to an illuminated night environment

This study investigated the role of nocturnal melatonin secretion in the cognitive performance of diurnal animals. An initial experiment measured the cognitive performance in Indian house crows treated for 11 days with 12 h light at 1.426 W/m2 (∼150 lux) coupled with 12 h of 0.058 W/m2 (∼6-lux) dim light at night (dLAN) or with absolute darkness (0 lux dark night, LD). dLAN treatment significantly decreased midnight melatonin levels and negatively impacted cognitive performance. Subsequently, the role of exogenous melatonin (50 μg; administered intraperitoneally half an hour before the night began) was assessed on the regulation of cognitive performance in two separate experimental cohorts of crows kept under dLAN; LD controls received vehicle. Exogenous melatonin restored its mid-night levels under dLAN at par with those under LD controls, and improved the cognitive performance, as measured in the innovative problem-solving, and spatial and pattern learning-memory efficiency tests in dLAN-treated crows. There were concurrent molecular changes in the cognition-associated brain areas, namely the hippocampus, nidopallium caudolaterale and midbrain. In particular, the expression levels of genes involved in neurogenesis and synaptic plasticity (bdnf, dcx, egr1, creb), and dopamine synthesis and signalling (th, drd1, drd2, darpp32, taar1) were restored to LD control levels in crows treated with illuminated nights and received melatonin. These results demonstrate that the maintenance of nocturnal melatonin levels is crucial for an optimal higher-order brain function in diurnal animals in the face of an environmental threat, such as light pollution.

Behavioral Training Related Neurotransmitter Receptor Expression Dynamics in the Nidopallium Caudolaterale and the Hippocampal Formation of Pigeons.

Learning and memory are linked to dynamic changes at the level of synapses in brain areas that are involved in cognitive tasks. For example, changes in neurotransmitter receptors are prerequisite for tuning signals along local circuits and long-range networks. However, it is still unclear how a series of learning events promotes plasticity within the system of neurotransmitter receptors and their subunits to shape information processing at the neuronal level. Therefore, we investigated the expression of different glutamatergic NMDA (GRIN) and AMPA (GRIA) receptor subunits, the GABAergic GABARG2 subunit, dopaminergic DRD1, serotonergic 5HTR1A and noradrenergic ADRA1A receptors in the pigeon’s brain. We studied the nidopallium caudolaterale, the avian analogue of the prefrontal cortex, and the hippocampal formation, after training the birds in a rewarded stimulus-response association (SR) task and in a simultaneous-matching-to-sample (SMTS) task. The results show that receptor expression changed differentially after behavioral training compared to an untrained control group. In the nidopallium caudolaterale, GRIN2B, GRIA3, GRIA4, DRD1D, and ADRA1A receptor expression was altered after SR training and remained constantly decreased after the SMTS training protocol, while GRIA2 and DRD1A decreased only under the SR condition. In the hippocampal formation, GRIN2B decreased and GABARG2 receptor expression increased after SR training. After SMTS sessions, GRIN2B remained decreased, GABARG2 remained increased if compared to the control group. None of the investigated receptors differed directly between both conditions, although differentially altered. The changes in both regions mostly occur in favor of the stimulus response task. Thus, the present data provide evidence that neurotransmitter receptor expression dynamics play a role in the avian prefrontal cortex and the hippocampal formation for behavioral training and is uniquely, regionally and functionally associated to cognitive processes including learning and memory.