Coevolution of motor cortex and behavioral specializations associated with flight and echolocation in bats

Halley, Andrew C; Baldwin, Mary K. L.; Cooke, Dylan F.; Englund, Mackenzie; Pineda, Carlos R.; Schmid, Tobias A.; Yartsev, Michael M.; Krubitzer, Leah

doi:10.1016/j.cub.2022.04.094

Cited by 6 publications

(7 citation statements)

References 35 publications

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“…Therefore, to guide our anatomical identification of a vocal area in the bat motor cortex, we first determined whether a direct corticospinal anatomical connection exists in R. aegyptiacus . Guided by cortical mapping experiments ( 41 ), we injected anterograde tracers into part of the motor cortex that has been associated with orofacial motor control (ofM1) and searched for labeled descending cortical fibers in the hindbrain region where the laryngeal motoneurons reside, the nucleus ambiguus (NA) (Fig. 2A, Supp.…”

Section: Main Textmentioning

confidence: 99%

Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Wirthlin

Schmid

Elie

et al. 2022

Preprint

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Vocal learning, the ability to modify vocal behavior based on experience, is a convergently evolved trait in birds and mammals. To identify genomic elements associated with vocal learning, we integrated new experiments conducted in the brain of the Egyptian fruit bat with analyses of the genomes of 222 placental mammals. We first identified an anatomically specialized region of the bat motor cortex containing direct monosynaptic projections to laryngeal motoneurons. Using wireless neural recordings of this brain region in freely vocalizing bats, we verified that single neuron activity in this region relates to vocal production. We profiled the open chromatin of this vocal-motor region, which we used to train machine learning models to identify enhancers associated with vocal learning across mammals. We found 201 proteins and 45 candidate enhancers that display convergent evolution associated with vocal learning, many of which overlapped loci associated with human speech disability. One such locus contains the neurodevelopmental transcription factors TSHZ3 and ZNF536 and multiple candidate vocal learning-associated enhancers, suggesting the co-evolution of protein and regulatory sequences underlying vocal learning.

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Section: Main Textmentioning

confidence: 99%

Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Wirthlin

Schmid

Elie

et al. 2022

Preprint

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“…We first determined whether a direct corticobulbar anatomical connection existed in R. aegyptiacus . Guided by cortical mapping experiments ( 47 ), we injected anterograde tracers into the part of the motor cortex that has been associated with orofacial motor control, the orofacial motor cortex (ofM1), and identified fluorescently labeled descending cortical fibers in the hindbrain region where the laryngeal motoneurons reside, the nucleus ambiguus (NA) (Fig. 2A; fig.…”

Section: Resultsmentioning

confidence: 99%

“…Because gene regulation is often tissue specific, we sought to identify motor regions of the brain involved in vocal production and contrast their epigenomic profiles with that of those not involved in vocal production. We conducted this comparison in the Egyptian fruit bat, R. aegyptiacus, a mammalian species with robust vocal plasticity (16,46) and with data on its motor cortex mapping (47). To identify a candidate region, we were guided by the hypothesis that fine vocal motor control, a key ability in vocal learning, may be associated with the anatomical specialization of the motor cortex (48)(49)(50)(51).…”

Section: Identification Of a Vocal Production Region In Egyptian Frui...mentioning

confidence: 99%

Vocal learning–associated convergent evolution in mammalian proteins and regulatory elements

Wirthlin,

Schmid,

Elie

et al. 2024

Science

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Vocal production learning is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical and neurophysiological data from the Egyptian fruit-bat with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal-motor cortical region in the Egyptian fruit-bat, an emergent vocal learner, and leveraged that knowledge to identify active cis -regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.

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“…The neural circuits for echolocation in bats have been studied intensively, albeit mostly from the perspective of auditory processing (Rubsamen and Schweizer, 1986;Gooler and O'Neill, 1987;Fenzl and Schuller, 2005). Neurons in the anterior cingulate cortex, motor cortex, and pyramidal motor systems project directly, as well as indirectly by intermediate nuclei, to vocal motor neurons in nucleus ambiguus in the brainstem (Huffman and Henson, 1990;Fenzl and Schuller, 2005;Metzner and Schuller, 2010;Halley et al, 2022). Input from the motor cortex serves motor coordination of learned vocal patterns, while input from the anterior cingulate cortex controls the voluntary initiation and suppression of vocalizations (Jürgens, 2002).…”

Section: Neural Pathways and Preadaptations For Vocal Production Lear...mentioning

confidence: 99%

An ecological and neurobiological perspective on the evolution of vocal learning

Brenowitz

Beecher

2023

Front. Ecol. Evol.

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Vocal production learning (VPL) involves the use of auditory experience to guide the production of novel signals or to modify pre-existing signals. It allows animals to develop signals that are more complex and/or more flexible than innately developed signals. It has evolved rarely in vocal animals, widespread only in three avian and four mammalian taxa. The evolution of VPL was accompanied by innovations of the vocal motor neural circuitry. VPL is rare because of its various costs. Ecology, social spacing, and social fluidity can favor the evolution of VPL. It is striking that most taxa with VPL evolved in visually limited habitats, where sound is the only effective channel for communicating over distance from sender to receiver. Selective factors that favor the ability to produce complex and/or flexible signals would act predominantly on acoustic signals, and favor the evolution of VPL. Learning may be the only practical way to develop a signal complex enough to encode different types of information for assessment by receivers in animals that rely on acoustic communication, or to modify signals as local social factors dictate.

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Coevolution of motor cortex and behavioral specializations associated with flight and echolocation in bats

Cited by 6 publications

References 35 publications

Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

Vocal learning–associated convergent evolution in mammalian proteins and regulatory elements

An ecological and neurobiological perspective on the evolution of vocal learning

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