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.

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.

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.

Categorical Auditory Working Memory in Crows.

The ability to group sensory data into behaviorally meaningful classes and to maintain these perceptual categories active in working memory is key to intelligent behavior. Here, we show that carrion crows, highly vocal and cognitively advanced corvid songbirds, possess categorical auditory working memory. The crows were trained in a delayed match-to-category task that required them to flexibly match remembered sounds based on the upward or downward shift of the sounds' frequency modulation. After training, the crows instantaneously classified novel sounds into the correct auditory categories. The crows showed sharp category boundaries as a function of the relative frequency interval of the modulation. In addition, the crows generalized frequency-modulated sounds within a category and correctly classified novel sounds kept in working memory irrespective of other acoustic features of the sound. This suggests that crows can form and actively memorize auditory perceptual categories in the service of cognitive control of their goal-directed behaviors.

A neural correlate of sensory consciousness in a corvid bird.

Subjective experiences that can be consciously accessed and reported are associated with the cerebral cortex. Whether sensory consciousness can also arise from differently organized brains that lack a layered cerebral cortex, such as the bird brain, remains unknown. We show that single-neuron responses in the pallial endbrain of crows performing a visual detection task correlate with the birds' perception about stimulus presence or absence and argue that this is an empirical marker of avian consciousness. Neuronal activity follows a temporal two-stage process in which the first activity component mainly reflects physical stimulus intensity, whereas the later component predicts the crows' perceptual reports. These results suggest that the neural foundations that allow sensory consciousness arose either before the emergence of mammals or independently in at least the avian lineage and do not necessarily require a cerebral cortex.

Neurons in the Endbrain of Numerically Naive Crows Spontaneously Encode Visual Numerosity.

Endowed with an elaborate cerebral cortex, humans and other primates can assess the number of items in a set, or numerosity, from birth on [1] and without being trained [2]. Whether spontaneous numerosity extraction is a unique feat of the mammalian cerebral cortex [3-7] or rather an adaptive property that can be found in differently designed and independently evolved neural substrates, such as the avian enbrain [8], is unknown. To address this question, we recorded single-cell activity from the nidopallium caudolaterale (NCL), a high-level avian association brain area [9-11], of numerically naive crows. We found that a proportion of NCL neurons were spontaneously responsive to numerosity and tuned to the number of items, even though the crows were never trained to assess numerical quantity. Our data show that numerosity-selective neuronal responses are spontaneously present in the distinct endbrains of diverge vertebrate taxa. This seemingly hard-wired property of the avian endbrain to extract numerical quantity explains how birds in the wild, or right after hatching, can exploit numerical cues when making foraging or social decisions. It suggests that endbrain circuitries that evolved based on convergent evolution, such as the avian endbrain, give rise to the same numerosity code.

Comparing the face inversion effect in crows and humans.

Humans show impaired recognition of faces that are presented upside down, a phenomenon termed face inversion effect, which is thought to reflect the special relevance of faces for humans. Here, we investigated whether a phylogenetically distantly related avian species, the carrion crow, with similar socio-cognitive abilities to human and non-human primates, exhibits a face inversion effect. In a delayed matching-to-sample task, two crows had to differentiate profiles of crow faces as well as matched controls, presented both upright and inverted. Because crows can discriminate humans based on their faces, we also assessed the face inversion effect using human faces. Both crows performed better with crow faces than with human faces and performed worse when responding to inverted pictures in general compared to upright pictures. However, neither of the crows showed a face inversion effect. For comparative reasons, the tests were repeated with human subjects. As expected, humans showed a face-specific inversion effect. Therefore, we did not find any evidence that crows-like humans-process faces as a special visual stimulus. Instead, individual recognition in crows may be based on cues other than a conspecific's facial profile, such as their body, or on processing of local features rather than holistic processing.

Encoding of global visual motion in the nidopallium caudolaterale of behaving crows.

Songbirds possess acute vision. How higher brain centres represent basic and parameterised visual stimuli to process sensory signals according to their behavioural importance has not been studied in a systematic way. We therefore examined how carrion crows (Corvus corone) and their nidopallial visual neurons process global visual motion information in dynamic random-dot displays during a delayed match-to-sample (DMS) task. The behavioural data show that moderately fast motion speeds (16° of visual angle/s) result in superior direction discrimination performance. To characterise how neurons encode and maintain task-relevant visual motion information, we recorded the single-unit activity in the telencephalic association area 'nidopallium caudolaterale' (NCL) of behaving crows. The NCL is considered to be the avian analogue of the mammalian prefrontal cortex. Almost a third (28%) of randomly selected NCL neurons responded selectively to the motion direction of the sample stimulus, mostly to downward motions. Only few NCL neurons (7.5%) responded consistently to specific motion directions during the delay period. In error trials, when the crows chose the wrong motion direction, the encoding of motion direction was significantly reduced. This indicates that sensory representations of NCL neurons are relevant to the birds' behaviour. These data suggest that the corvid NCL, even though operating at the apex of the telencephalic processing hierarchy, constitutes a telencephalic site for global motion integration.