Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.lateral magnocellular nucleus of the anterior nidopallium | Hebbian learning | mirror neuron
A wealth of research in infants and animals demonstrates discrimination of quantities, in some cases nonverbal numerical perception, and even elementary calculation capacities. We investigated the ability of three African grey parrots (Psittacus erithacus) to select the largest amount of food between two sets, either discrete food items (experiment 1) or as volume of a food substance (experiment 2). The two amounts were presented simultaneously and were visible at the time of choice. Parrots were tested several times for all possible combinations between 1 and 5 seeds or 0.2 and 1 ml of food substance. In both conditions, subjects performed above chance for almost all combinations. Accuracy was negatively correlated with the ratio, that is performance improved with greater differences between amounts. Therefore, these results with both individual items and volume discrimination suggest that parrots use an analogue of magnitude, rather than object-file mechanisms to quantify items and substances.
One advantage of living in a social group is the opportunity to use information provided by other individuals. Social information can be based on cues provided by a conspecific or even by a heterospecific individual (e.g., gaze direction, vocalizations, pointing gestures). Although the use of human gaze and gestures has been extensively studied in primates, and is increasingly studied in other mammals, there is no documentation of birds using these cues in a cooperative context. In this study, we tested the ability of three African gray parrots to use different human cues (pointing and/or gazing) in an object-choice task. We found that one subject spontaneously used the most salient pointing gesture (looking and steady pointing with hand at about 20 cm from the baited box). The two others were also able to use this cue after 15 trials. None of the parrots spontaneously used the steady gaze cues (combined head and eye orientation), but one learned to do so effectively after only 15 trials when the distance between the head and the baited box was about 1 m. However, none of the parrots were able to use the momentary pointing nor the distal pointing and gazing cues. These results are discussed in terms of sensitivity to joint attention as a prerequisite to understand pointing gestures as it is to the referential use of labels.
Sensitivity to the sequential structure of communication sounds is fundamental not only for language comprehension in humans but also for song recognition in songbirds. By quantifying single-unit responses, we first assessed whether the sequential order of song elements, called syllables, in conspecific songs is encoded in a secondary auditory cortex-like region of the zebra finch brain. Based on a habituation/ dishabituation paradigm, we show that, after multiple repetitions of the same conspecific song, rearranging syllable order reinstated strong responses. A large proportion of neurons showed sensitivity to song context in which syllables occurred providing support for the nonlinear processing of syllable sequences. Sensitivity to the temporal order of items within a sequence should enable learning its underlying structure, an ability considered a core mechanism of the human language faculty. We show that repetitions of songs that were ordered according to a specific grammatical structure (i.e., ABAB or AABB structures; A and B denoting song syllables) led to different responses in both anesthetized and awake birds. Once responses were decreased due to song repetitions, the transition from one structure to the other could affect the firing rates and/or the spike patterns. Our results suggest that detection was based on local differences rather than encoding of the global song structure as a whole. Our study demonstrates that a high-level auditory region provides neuronal mechanisms to help discriminate stimuli that differ in their sequential structure.Sequence processing has been proposed as a potential precursor of language syntax. As a sequencing operation, the encoding of the temporal order of items within a sequence may help in recognition of relationships between adjacent items and in learning the underlying structure. Taking advantage of the stimulus-specific adaptation phenomenon observed in a high-level auditory region of the zebra finch brain, we addressed this question at the neuronal level. Reordering elements within conspecific songs reinstated robust responses. Neurons also detected changes in the structure of artificial songs, and this detection depended on local transitions between adjacent or nonadjacent syllables. These findings establish the songbird as a model system for deciphering the mechanisms underlying sequence processing at the single-cell level.
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