Crows "count" the number of self-generated vocalizations.

Producing a specific number of vocalizations with purpose requires a sophisticated combination of numerical abilities and vocal control. Whether this capacity exists in animals other than humans is yet unknown. We show that crows can flexibly produce variable numbers of one to four vocalizations in response to arbitrary cues associated with numerical values. The acoustic features of the first vocalization of a sequence were predictive of the total number of vocalizations, indicating a planning process. Moreover, the acoustic features of vocal units predicted their order in the sequence and could be used to read out counting errors during vocal production.

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.

Sequential neuronal processing of number values, abstract decision, and action in the primate prefrontal cortex.

Decision-making requires processing of sensory information, comparing the gathered evidence to make a judgment, and performing the action to communicate it. How neuronal representations transform during this cascade of representations remains a matter of debate. Here, we studied the succession of neuronal representations in the primate prefrontal cortex (PFC). We trained monkeys to judge whether a pair of sequentially presented displays had the same number of items. We used a combination of single neuron and population-level analyses and discovered a sequential transformation of represented information with trial progression. While numerical values were initially represented with high precision and in conjunction with detailed information such as order, the decision was encoded in a low-dimensional subspace of neural activity. This decision encoding was invariant to both retrospective numerical values and prospective motor plans, representing only the binary judgment of "same number" versus "different number," thus facilitating the generalization of decisions to novel number pairs. We conclude that this transformation of neuronal codes within the prefrontal cortex supports cognitive flexibility and generalizability of decisions to new conditions.

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.

The neuronal implementation of representational geometry in primate prefrontal cortex.

Modern neuroscience has seen the rise of a population-doctrine that represents cognitive variables using geometrical structures in activity space. Representational geometry does not, however, account for how individual neurons implement these representations. Leveraging the principle of sparse coding, we present a framework to dissect representational geometry into biologically interpretable components that retain links to single neurons. Applied to extracellular recordings from the primate prefrontal cortex in a working memory task with interference, the identified components revealed disentangled and sequential memory representations including the recovery of memory content after distraction, signals hidden to conventional analyses. Each component was contributed by small subpopulations of neurons with distinct spiking properties and response dynamics. Modeling showed that such sparse implementations are supported by recurrently connected circuits as in prefrontal cortex. The perspective of neuronal implementation links representational geometries to their cellular constituents, providing mechanistic insights into how neural systems encode and process information.

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.

Dopamine receptor activation regulates reward expectancy signals during cognitive control in primate prefrontal neurons.

Dopamine neurons respond to reward-predicting cues but also modulate information processing in the prefrontal cortex essential for cognitive control. Whether dopamine controls reward expectation signals in prefrontal cortex that motivate cognitive control is unknown. We trained two male macaques on a working memory task while varying the reward size earned for successful task completion. We recorded neurons in lateral prefrontal cortex while simultaneously stimulating dopamine D1 receptor (D1R) or D2 receptor (D2R) families using micro-iontophoresis. We show that many neurons predict reward size throughout the trial. D1R stimulation showed mixed effects following reward cues but decreased reward expectancy coding during the memory delay. By contrast, D2R stimulation increased reward expectancy coding in multiple task periods, including cueing and memory periods. Stimulation of either dopamine receptors increased the neurons' selective responses to reward size upon reward delivery. The differential modulation of reward expectancy by dopamine receptors suggests that dopamine regulates reward expectancy necessary for successful cognitive control.

Numerical Representation for Action in Crows Obeys the Weber-Fechner Law.

The psychophysical laws governing the judgment of perceived numbers of objects or events, called the number sense, have been studied in detail. However, the behavioral principles of equally important numerical representations for action are largely unexplored in both humans and animals. We trained two male carrion crows (Corvus corone) to judge numerical values of instruction stimuli from one to five and to flexibly perform a matching number of pecks. Our quantitative analysis of the crows' number production performance shows the same behavioral regularities that have previously been demonstrated for the judgment of sensory numerosity, such as the numerical distance effect, the numerical magnitude effect, and the logarithmical compression of the number line. The presence of these psychophysical phenomena in crows producing number of pecks suggests a unified sensorimotor number representation system underlying the judgment of the number of external stimuli and internally generated actions.

Distinct neuronal representation of small and large numbers in the human medial temporal lobe.

Whether small numerical quantities are represented by a special subitizing system that is distinct from a large-number estimation system has been debated for over a century. Here we show that two separate neural mechanisms underlie the representation of small and large numbers. We performed single neuron recordings in the medial temporal lobe of neurosurgical patients judging numbers. We found a boundary in neuronal coding around number 4 that correlates with the behavioural transition from subitizing to estimation. In the subitizing range, neurons showed superior tuning selectivity accompanied by suppression effects suggestive of surround inhibition as a selectivity-increasing mechanism. In contrast, tuning selectivity decreased with increasing numbers beyond 4, characterizing a ratio-dependent number estimation system. The two systems with the coding boundary separating them were also indicated using decoding and clustering analyses. The identified small-number subitizing system could be linked to attention and working memory that show comparable capacity limitations.

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.

Costs and benefits of voluntary attention in crows.

Behavioural signatures of voluntary, endogenous selective attention have been found in both mammals and birds, but the relationship between performance benefits at attended and costs at unattended locations remains unclear. We trained two carrion crows (Corvus corone) on a Posner-like spatial cueing task with dissociated cue and target locations, using both highly predictive and neutral central cues to compare reaction time (RT) and detection accuracy for validly, invalidly and neutrally cued targets. We found robust RT effects of predictive cueing at varying stimulus-onset asynchronies (SOA) that resulted from both advantages at cued locations and costs at un-cued locations. Both crows showed cueing effects around 15-25 ms with an early onset at 100 ms SOA, comparable to macaques. Our results provide a direct assessment of costs and benefits of voluntary attention in a bird species. They show that crows are able to guide spatial attention using associative cues, and that the processing advantage at attended locations impairs performance at unattended locations.

Neuroscience of cognitive control in crows.

Crows, a group of corvid songbird species, show superb behavioral flexibility largely stemming from their advanced cognitive control functions. These functions mainly originate from the associative avian pallium that evolved independently from the mammalian cerebral cortex. This article presents a brief overview of cognitive control functions and their neuronal foundation in crows.

Crows flexibly apply statistical inferences based on previous experience.

Statistical inference, the ability to use limited information to draw conclusions about the likelihood of an event, is critical for decision-making during uncertainty. The ability to make statistical inferences was thought to be a uniquely human skill requiring verbal instruction and mathematical reasoning.1 However, basic inferences have been demonstrated in both preliterate and pre-numerate individuals,2,3,4,5,6,7 as well as non-human primates.8 More recently, the ability to make statistical inferences has been extended to members outside of the primate lineage in birds.9,10 True statistical inference requires subjects use relative rather than absolute frequency of previously experienced events. Here, we show that crows can relate memorized reward probabilities to infer reward-maximizing decisions. Two crows were trained to associate multiple reward probabilities ranging from 10% to 90% to arbitrary stimuli. When later faced with the choice between various stimulus combinations, crows retrieved the reward probabilities associated with individual stimuli from memory and used them to gain maximum reward. The crows showed behavioral distance and size effects when judging reward values, indicating that the crows represented probabilities as abstract magnitudes. When controlling for absolute reward frequency, crows still made reward-maximizing choices, which is the signature of true statistical inference. Our study provides compelling evidence of decision-making by relative reward frequency in a statistical inference task.

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.

Resolving the prefrontal mechanisms of adaptive cognitive behaviors: A cross-species perspective.

The prefrontal cortex (PFC) enables a staggering variety of complex behaviors, such as planning actions, solving problems, and adapting to new situations according to external information and internal states. These higher-order abilities, collectively defined as adaptive cognitive behavior, require cellular ensembles that coordinate the tradeoff between the stability and flexibility of neural representations. While the mechanisms underlying the function of cellular ensembles are still unclear, recent experimental and theoretical studies suggest that temporal coordination dynamically binds prefrontal neurons into functional ensembles. A so far largely separate stream of research has investigated the prefrontal efferent and afferent connectivity. These two research streams have recently converged on the hypothesis that prefrontal connectivity patterns influence ensemble formation and the function of neurons within ensembles. Here, we propose a unitary concept that, leveraging a cross-species definition of prefrontal regions, explains how prefrontal ensembles adaptively regulate and efficiently coordinate multiple processes in distinct cognitive behaviors.

Crows protect visual working memory against interference.

Working memory, the ability to actively maintain and manipulate information across time, is key to intelligent behavior. Because of the limited capacity of working memory, relevant information needs to be protected against distracting representations. Whether birds can resist distractors and safeguard memorized relevant information is unclear. We trained carrion crows in a delayed match-to-sample task to memorize an image while resisting other, interfering stimuli. We found that the repetition of the sample stimulus during the memory delay improved performance accuracy and accelerated reaction time relative to a reference condition with a neutral interfering stimulus. In contrast, the presentation of the image that constituted the subsequent non-match test stimulus mildly weakened performance. However, the crows' robust performance in this most demanding distractor condition indicates that sample information was actively protected from being overwritten by the distractor. These data show that crows can cognitively control and safeguard behaviorally relevant working memory contents.

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.

Recursive sequence generation in crows.

Recursion, the process of embedding structures within similar structures, is often considered a foundation of symbolic competence and a uniquely human capability. To understand its evolution, we can study the recursive aptitudes of nonhuman animals. We adopted the behavioral protocol of a recent study demonstrating that humans and nonhuman primates grasp recursion. We presented sequences of bracket pair stimuli (e.g., [ ] and { }) to crows who were instructed to peck at training lists. They were then tested on their ability to transfer center-embedded structure to never-before-seen pairings of brackets. We reveal that crows have recursive capacities; they perform on par with children and even outperform macaques. The crows continued to produce recursive sequences after extending to longer and thus deeper embeddings. These results demonstrate that recursive capabilities are not limited to the primate genealogy and may have occurred separately from or before human symbolic competence in different animal taxa.

Number selective sensorimotor neurons in the crow translate perceived numerosity into number of actions.

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.

Oscillations without cortex: Working memory modulates brainwaves in the endbrain of crows.

Complex cognition requires coordinated neuronal activity at the network level. In mammals, this coordination results in distinct dynamics of local field potentials (LFP) central to many models of higher cognition. These models often implicitly assume a cortical organization. Higher associative regions of the brains of birds do not have cortical layering, yet single-cell correlates of higher cognition are very similar to those found in mammals. We recorded LFP in the avian equivalent of prefrontal cortex while crows performed a highly controlled and cognitively demanding working memory task. We found signatures in local field potentials, modulated by working memory. Frequencies of a narrow gamma and the beta band contained information about the location of target items and were modulated by working memory load. This indicates a critical involvement of these bands in ongoing cognitive processing. We also observed bursts in the beta and gamma frequencies, similar to those that play a vital part in 'activity silent' models of working memory. Thus, despite the lack of a cortical organization the avian associative pallium can create LFP signatures reminiscent of those observed in primates. This points towards a critical cognitive function of oscillatory dynamics evolved through convergence in species capable of complex cognition.