Abstract
Understanding when learning begins is critical for identifying the factors that shape both the developmental course and the function of information acquisition. Until recently, sufficient development of the neural substrates for any sort of vocal learning to begin in songbirds was thought to be reached well after hatching. New research shows that embryonic gene activation and the outcome of vocal learning can be modulated by sound exposure in ovo. We tested whether avian embryos across lineages differ in their auditory response strength and sound learning in ovo, which we studied in vocal learning (Maluridae, Geospizidae) and vocal non-learning (Phasianidae, Spheniscidae) taxa. While measuring heart rate in ovo, we exposed embryos to (i) conspecific or heterospecific vocalizations, to determine their response strength, and (ii) conspecific vocalizations repeatedly, to quantify cardiac habituation, a form of non-associative learning. Response strength towards conspecific vocalizations was greater in two species with vocal production learning compared to two species without. Response patterns consistent with non-associative auditory learning occurred in all species. Our results demonstrate a capacity to perceive and learn to recognize sounds in ovo, as evidenced by habituation, even in species that were previously assumed to have little, if any, vocal production learning.This article is part of the theme issue ‘Vocal learning in animals and humans’.
Highlights
Vocal learning [1] is generally defined as the capacity to produce vocalizations based on the imitation of external sounds, but can extend to the capacity to associate a vocalization with an outcome or to produce an existing vocalization in a novel context
Vocal production learning is only believed to occur in approximately eight lineages of birds and mammals, including humans
With a better understanding of the ontogeny of response strength to sound, we can test predictions about the potential for early-life experience to influence neural pathways associated with vocal learning
Summary
Vocal learning [1] is generally defined as the capacity to produce vocalizations based on the imitation of external sounds (vocal production learning), but can extend to the capacity to associate a vocalization with an outcome (comprehension learning) or to produce an existing vocalization in a novel context (vocal usage learning) (reviewed in [2]). Species-specific vocalizations vary significantly across species; recognizing and producing the right vocalization can be critical to interact with conspecifics [5] Such vocalizations elicit a stronger neural and behavioural response than non-specific sounds ([5], reviewed in [6]), even in acoustically naïve birds, and in the absence of prior conspecific stimulation [7,8]. We measured response strength and non-associative learning (habituation) of vocalizations in avian embryos with different characteristics (e.g. vocal learners versus non-learners; altricial and semi-altricial versus precocial; ancient versus recent lineages). We predicted that the precocial embryos (Phasianidae; classified here as a vocal non-learner) would exhibit larger physiological effects in both experiments because they are physiologically and morphologically more developed at the same comparative age in ovo than the semialtricial (Spheniscidae; classified here as vocal non-learners) and altricial embryos (oscine Maluridae and Geospizidae; both classified here as vocal learners)
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