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.

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.

Behavioral and Neuronal Representation of Numerosity Zero in the Crow.

Different species of animals can discriminate numerosity, the countable number of objects in a set. The representations of countable numerosities have been deciphered down to the level of single neurons. However, despite its importance for human number theory, a special numerical quantity, the empty set (numerosity zero), has remained largely unexplored. We explored the behavioral and neuronal representation of the empty set in carrion crows. Crows were trained to discriminate small numerosities including the empty set. Performance data showed a numerical distance effect for the empty set in one crow, suggesting that the empty set and countable numerosities are represented along the crows' "mental number line." Single-cell recordings in the endbrain region nidopallium caudolaterale (NCL) showed a considerable proportion of NCL neurons tuned to the preferred numerosity zero. As evidenced by neuronal distance and size effects, NCL neurons integrated the empty set in the neural number line. A subsequent neuronal population analysis using a statistical classifier approach showed that the neuronal numerical representations were predictive of the crows' success in the task. These behavioral and neuronal data suggests that the conception of the empty set as a cognitive precursor of a zero-like number concept is not an exclusive property of the cerebral cortex of primates. Zero as a quantitative category cannot only be implemented in the layered neocortex of primates, but also in the anatomically distinct endbrain circuitries of birds that evolved based on convergent evolution.SIGNIFICANCE STATEMENT The conception of "nothing" as number "zero" is celebrated as one of the greatest achievements in mathematics. To explore whether precursors of zero-like concepts can be found in vertebrates with a cerebrum that anatomically differs starkly from our primate brain, we investigated this in carrion crows. We show that crows can grasp the empty set as a null numerical quantity that is mentally represented next to number one. Moreover, we show that single neurons in an associative avian cerebral region specifically respond to the empty set and show the same physiological characteristics as for countable quantities. This suggests that zero as a quantitative category can also be implemented in the anatomically distinct endbrain circuitries of birds that evolved based on convergent evolution.

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.

Neuronal Correlates of Spatial Working Memory in the Endbrain of Crows.

Birds are renowned for their excellent spatial cognition. Corvid songbirds, in particular, rely on explicit representation of spatial cues in memory when caching food and retrieving caches for later consumption. However, the neuronal correlates of flexible spatial memory abilities are largely unknown in birds. We therefore trained carrion crows (Corvus corone) on a spatial delayed-response task in which they had to maintain the variable location of a visual item for a few seconds in working memory. After the crows performed this task with high precision, we recorded single-cell activity from the associative endbrain area Nidopallium caudolaterale (NCL) in the behaving crows. A large fraction of NCL neurons were tuned to individual preferred locations and selectively maintained the spatial location of items in working memory. A comparison of firing rates with reaction times suggested that the majority of delay-selective neurons represented stored location information rather than motor preparation. Almost 30% of all recorded neurons were tuned during both visual presentation and memory delay, and their spatial tuning was significantly correlated. The population of recorded neurons stably maintained spatial information over the course of the working memory period. Importantly, the neural responses of spatially tuned neurons were relevant for the crows' choices and allowed a statistical classifier to predict the subsequently chosen target location in free-choice trials. Our findings demonstrate the pivotal role of the avian NCL in spatial working memory that is reminiscent of the function of the convergently evolved primate prefrontal cortex in spatial working memory.

Spatial memory for vertical locations.

Most studies on spatial memory refer to the horizontal plane, leaving an open question as to whether findings generalize to vertical spaces where gravity and the visual upright of our surrounding space are salient orientation cues. In three experiments, we examined which reference frame is used to organize memory for vertical locations: the one based on the body vertical, the visual-room vertical, or the direction of gravity. Participants judged interobject spatial relationships learned from a vertical layout in a virtual room. During learning and testing, we varied the orientation of the participant's body (upright vs. lying sideways) and the visually presented room relative to gravity (e.g., rotated by 90° along the frontal plane). Across all experiments, participants made quicker or more accurate judgments when the room was oriented in the same way as during learning with respect to their body, irrespective of their orientations relative to gravity. This suggests that participants employed an egocentric body-based reference frame for representing vertical object locations. Our study also revealed an effect of body-gravity alignment during testing. Participants recalled spatial relations more accurately when upright, regardless of the body and visual-room orientation during learning. This finding is consistent with a hypothesis of selection conflict between different reference frames. Overall, our results suggest that a body-based reference frame is preferred over salient allocentric reference frames in memory for vertical locations perceived from a single view. Further, memory of vertical space seems to be tuned to work best in the default upright body orientation. (PsycINFO Database Record (c) 2019 APA, all rights reserved).