TY - JOUR
T1 - Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl
AU - Schneider, Eve R.
AU - Mastrotto, Marco
AU - Laursen, Willem J.
AU - Schulz, Vincent P.
AU - Goodman, Jena B.
AU - Funk, Owen H.
AU - Gallagher, Patrick G.
AU - Gracheva, Elena O.
AU - Bagriantsev, Sviatoslav N.
N1 - Publisher Copyright:
© 2014, National Academy of Sciences. All rights reserved.
PY - 2014/10/14
Y1 - 2014/10/14
N2 - Relying almost exclusively on their acute sense of touch, tactile-foraging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactile-foraging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.
AB - Relying almost exclusively on their acute sense of touch, tactile-foraging birds can feed in murky water, but the cellular mechanism is unknown. Mechanical stimuli activate specialized cutaneous end organs in the bill, innervated by trigeminal afferents. We report that trigeminal ganglia (TG) of domestic and wild tactile-foraging ducks exhibit numerical expansion of large-diameter mechanoreceptive neurons expressing the mechano-gated ion channel Piezo2. These features are not found in visually foraging birds. Moreover, in the duck, the expansion of mechanoreceptors occurs at the expense of thermosensors. Direct mechanical stimulation of duck TG neurons evokes high-amplitude depolarizing current with a low threshold of activation, high signal amplification gain, and slow kinetics of inactivation. Together, these factors contribute to efficient conversion of light mechanical stimuli into neuronal excitation. Our results reveal an evolutionary strategy to hone tactile perception in vertebrates at the level of primary afferents.
KW - Mechanotransduction
KW - Piezo2
KW - TRPM8
KW - TRPV1
UR - http://www.scopus.com/inward/record.url?scp=84907888286&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=84907888286&partnerID=8YFLogxK
U2 - 10.1073/pnas.1413656111
DO - 10.1073/pnas.1413656111
M3 - Article
C2 - 25246547
AN - SCOPUS:84907888286
SN - 0027-8424
VL - 111
SP - 14941
EP - 14946
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 41
ER -