Mechanical responses of rat vibrissae to airflow

Yu, Yan S. W.; Graff, Matthew M.; Hartmann, Mitra J. Z.

doi:10.1242/jeb.126896

Cited by 40 publications

(62 citation statements)

References 61 publications

(87 reference statements)

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“…Previous work has shown that a whisker both bends and vibrates in response to airflow stimulation (Yu et al, 2016a). Vibrissae-responsive neurons would be expected to respond to both of these mechanical components.…”

Section: Introductionmentioning

confidence: 98%

Whisker Vibrations and the Activity of Trigeminal Primary Afferents in Response to Airflow

Bush²,

Hartmann

2019

J. Neurosci.

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Rodents are the most commonly studied model system in neuroscience, but surprisingly few studies investigate the natural sensory stimuli that rodent nervous systems evolved to interpret. Even fewer studies examine neural responses to these natural stimuli. Decades of research have investigated the rat vibrissal (whisker) system in the context of direct touch and tactile stimulation, but recent work has shown that rats also use their whiskers to help detect and localize airflow. The present study investigates the neural basis for this ability as dictated by the mechanical response of whiskers to airflow. Mechanical experiments show that a whisker's vibration magnitude depends on airspeed and the intrinsic shape of the whisker. Surprisingly, the direction of the whisker's vibration changes as a function of airflow speed: vibrations transition from parallel to perpendicular with respect to the airflow as airspeed increases. Recordings from primary sensory trigeminal ganglion neurons show that these neurons exhibit responses consistent with those that would be predicted from direct touch. Trigeminal neuron firing rate increases with airspeed, is modulated by the orientation of the whisker relative to the airflow, and is influenced by the whisker's resonant frequencies. We develop a simple model to describe how a population of neurons could leverage mechanical relationships to decode both airspeed and direction. These results open new avenues for studying vibrissotactile regions of the brain in the context of evolutionarily important airflow-sensing behaviors and olfactory search. Although this study used only female rats, all results are expected to generalize to male rats.The rodent vibrissal (whisker) system has been studied for decades in the context of direct tactile sensation, but recent work has indicated that rats also use whiskers to help localize airflow. Neural circuits in somatosensory regions of the rodent brain thus likely evolved in part to process airflow information. This study investigates the whiskers' mechanical response to airflow and the associated neural response. Airspeed affects the magnitude of whisker vibration and the response magnitude of whisker-sensitive primary sensory neurons in the trigeminal ganglion. Surprisingly, the direction of vibration and the associated directionally dependent neural response changes with airspeed. These findings suggest a population code for airflow speed and direction and open new avenues for studying vibrissotactile regions of the brain.

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Section: Introductionmentioning

confidence: 98%

Whisker Vibrations and the Activity of Trigeminal Primary Afferents in Response to Airflow

Bush²,

Hartmann

2019

J. Neurosci.

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“…Although some sensory hairs and hair-like organs that mediate anemotaxis in multiple species have been identified [8][9][10][11], the neural underpinnings of how information about the wind direction is transformed into directional behavioral responses during anemotaxis in the CNS have been understudied.…”

Section: Introductionmentioning

confidence: 99%

Neural Substrates of Drosophila Larval Anemotaxis

et al. 2019

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Graphical AbstractHighlights d Drosophila larvae perform negative anemotaxis d To anemotax, larvae modulate the turn rate, size, and direction as in other taxis d Chordotonal and multidendritic class III sensory neurons together mediate anemotaxis d The anemotactic circuitry involves both the nerve cord and the brain SUMMARY Animals use sensory information to move toward more favorable conditions. Drosophila larvae can move up or down gradients of odors (chemotax), light (phototax), and temperature (thermotax) by modulating the probability, direction, and size of turns based on sensory input. Whether larvae can anemotax in gradients of mechanosensory cues is unknown. Further, although many of the sensory neurons that mediate taxis have been described, the central circuits are not well understood. Here, we used highthroughput, quantitative behavioral assays to demonstrate Drosophila larvae anemotax in gradients of wind speeds and to characterize the behavioral strategies involved. We found that larvae modulate the probability, direction, and size of turns to move away from higher wind speeds. This suggests that similar central decision-making mechanisms underlie taxis in somatosensory and other sensory modalities. By silencing the activity of single or very few neuron types in a behavioral screen, we found two sensory (chordotonal and multidendritic class III) and six nerve cord neuron types involved in anemotaxis. We reconstructed the identified neurons in an electron microscopy volume that spans the entire larval nervous system and found they received direct input from the mechanosensory neurons or from each other. In this way, we identified local interneurons and firstand second-order subesophageal zone (SEZ) and brain projection neurons. Finally, silencing a dopaminergic brain neuron type impairs anemotaxis. These findings suggest that anemotaxis involves both nerve cord and brain circuits. The candidate neurons and circuitry identified in our study provide a basis for future detailed mechanistic understanding of the circuit principles of anemotaxis. CATMAID https://catmaid.readthedocs.org/ [32] MATLAB http://www.mathworks.com [45, 69] Current Biology 29, 554-566.e1-e4, February 18, 2019 e1

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“…We also measured the resonant vibrational response of crest feathers for several other types of 342 short peacock feathers (three lengths of peacock mantle feathers, the shortest length of train eyespot feather, and four different body contour feathers), and for one or more crest feathers 344 from four other bird species: two additional species from order Galliformes, the Himalayan monal (Lophophorus impejanus) and the golden pheasant (Chrysolophus pictus); the Victoria 346 crowned pigeon (Goura Victoria) from the order Columbiformes, and the yellow-crested cockatoo (Cacatua sulphurea) from the order Psittaciformes; see S1 Table and S1 The resonant response for each of these feathers was measured for driving forces in the out-ofplane direction for n = 3 trials for each feather at each of two frequency sweep rates (2.0 Hz/s, 0 350 to 120 Hz; 1.33 Hz/s, 0 to 80 Hz); the Himalayan monal sample was also studied using a sweep rate of 0.5 Hz/s over 0 to 30 to reproduce this analysis are available with the data repository for this study [70]. The Nyquist frequency, which gives the upper bound on measurable frequencies [79], was 120 Hz (half the 362 frame capture rate) (> 4× typical biological vibration frequencies used during peafowl displays).…”

Section: Vibrational Dynamics Measurementsmentioning

confidence: 99%

“…A large body of research in mammals and arthropods has 108 found that antennae and sensory hairs play important mechanosensory roles in sound detection; this function is also known to be influenced by their vibrational response and mechanical 110 structures [27,28]. For example, in order for a feather crest to sense environmental airflows, it would need to bend sufficiently to activate mechanosensory nerve cells (P1-P4; Box 1), as has 112 been shown for pigeon covert feathers [2], arthropod sensory hairs, pinniped whiskers, bat sensory hairs, fish lateral line organs [29], and rat whiskers [30,30]. Thus, one would expect 114 crest feathers to be compliant enough to deflect when stimulated by salient airflow stimuli.…”

Section: Introductionmentioning

confidence: 99%

“…To do so, we first consider which features we would expect these feathers to have to function 202 effectively as mechanosensors for different stimuli. For example, in order for the crest to sense environmental airflows, it would need to bend sufficiently to activate mechanosensory nerve 204 cells, as has been shown for pigeon covert feathers (Necker, 1985b), arthropod sensory hairs, pinniped whiskers, bat sensory hairs, and fish lateral line organs (Bleckmann et al, 2014) and rat 206 whiskers (Yu et al, 2016;Yu et al, 2016).…”

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confidence: 99%

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Biomechanics of the peafowl’s crest reveals frequencies tuned to social displays

Kane

Beveren

Dakin

2017

Preprint

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Summary statement: Avian crest feathers have mechanical properties that make them suitable 18 for sensing airflows generated during multimodal social displays. 20. CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/197525 doi: bioRxiv preprint first posted online Oct. 2, 2017; 2 ABSTRACT 22Feathers act as vibrotactile sensors that can detect mechanical stimuli during avian flight and tactile navigation, suggesting that they may also function to detect signals during social 24 displays. We explored this novel sensory modality using the crest plumage of Indian peafowl (Pavo cristatus). We first determined whether the airborne stimuli generated by peafowl 26 courtship and social displays couple efficiently via resonance to the vibrational response of feather crests from the heads of peafowl. Peafowl crests were found to have fundamental 28 resonant modes with frequencies that could be driven near-optimally by the shaking frequencies used by peafowl performing train vibrating displays. Crests also were driven to vibrate near 30 resonance when audio recordings of sounds generated by these displays were played back in the acoustic near-field, where such displays are experienced in vivo. When peacock wing-shaking 32 courtship behaviour was simulated in the laboratory, the resulting directional airflow excited measurable vibrations of crest feathers. These results suggest that peafowl crests have properties 34 that make them suitable mechanosensors for airborne stimuli generated during social displays. Such stimuli could complement acoustic perception, thereby enhancing detection and 36 interpretation of social displays. Diverse feather crests are found in many bird species that perform similar displays, suggesting that this proposed sensory modality may be widespread, and 38 possibly derived from flow sensing in other contexts. We suggest behavioral studies to further explore these ideas and their functional implications. 40

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Mechanical responses of rat vibrissae to airflow

Cited by 40 publications

References 61 publications

Whisker Vibrations and the Activity of Trigeminal Primary Afferents in Response to Airflow

Whisker Vibrations and the Activity of Trigeminal Primary Afferents in Response to Airflow

Neural Substrates of Drosophila Larval Anemotaxis

Biomechanics of the peafowl’s crest reveals frequencies tuned to social displays

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