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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Angular Tuning Properties of Low Threshold Mechanoreceptors in Isolated Rat Whisker Hair Follicles

Akihiro Yamada, Hidemasa Furue and Jianguo G. Gu
eNeuro 14 November 2022, 9 (6) ENEURO.0175-22.2022; https://doi.org/10.1523/ENEURO.0175-22.2022
Akihiro Yamada
1Department of Anesthesiology and Perioperative Medicine, University of Alabama at Birmingham, Birmingham, AL 35294
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Hidemasa Furue
2Department of Neurophysiology, Hyogo Medical University, Nishinomiya 663-8501, Japan
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Jianguo G. Gu
1Department of Anesthesiology and Perioperative Medicine, University of Alabama at Birmingham, Birmingham, AL 35294
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    Figure 1.

    Angular responses of RA LTMRs in whisker hair follicles of rats. A1–A3, Positions of a left and a right whisker hair (orange), their follicles (red) and afferent roots (blue) in head axes viewed from top of the head (A1), left side (A2, top) and right side (A3, top). In the diagrams, only one hair follicle with its afferent root on each side is shown for clarity. For either the left (A2, top panel) or the right (A3, top panel) whisker hair follicle, its afferent root tilts ∼45° toward dorsal-caudal direction. The positions described here are applicable for the whisker hair follicles located at the central region of whisker pads. A2, bottom, A3, bottom, In vitro recording of afferent impulses while whisker hair is angularly deflected. In experiments, for either a left-side or a right-side hair follicle, the first hair deflection was always applied in the same direction as its afferent root’s direction (solid black arrow indicated, 45° dorsal-caudal direction). Whisker hair deflections were subsequently applied clockwise in a 15° increment. B, Sample trace (top panel) shows RA LTMR impulses in response to ramp-and-hold whisker hair deflection in 24 angular directions each at the amplitude of 200 μm. The recording was from a left C2 whisker hair follicle. The scale bar to the right indicates the angle size of whisker hair deflection. The 24 directions of whisker hair deflection started with 1st deflection in afferent root direction. Bottom three traces are impulses at the expanded time scale from arrow-indicated angles in the top panel, one angle induced responses only in the ramp-up phase (left), another angle induced impulses in both the ramp-up and ramp-down phases (middle), and the third angle induced impulses only in the ramp-down phase (right). In all 24 directions, no impulses were evoked during the static phase. C, Summary data (n = 21) of the sizes of the angles showing impulses only in the ramp-up phase, impulses in both the ramp-up and ramp-down phases, impulses only in the ramp-down phase, and the sizes of angles showing no response (null angle). D, E, Summary data (n = 21) of RA LTMR impulse frequency (D) and number (E) in the ramp-up (circles) and ramp-down (squares) phases at the most sensitive angles. Data represent mean ± SEM, ***p < 0.001.

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    Figure 2.

    Angular tuning parameters and amplitude encoding of RA LTMRs. A, Polar plot shows an example of angular responses of an RA LTMR. Solid and dashed black lines indicate angular responses in the ramp-up and ramp-down phases, respectively. Solid black arrow and dashed black arrow indicate vectors of the ramp-up response and ramp-down response, respectively. Concentric circles and numbers indicate impulse numbers. B, Bar graph shows numbers of RA LTMRs displaying angular tuning in the caudal (caudal ±45°), ventral (ventral ±45°), rostral (rostral ±45°), and dorsal (dorsal ±45°) directions. Black bars, ramp-up responses; gray bars, ramp-down responses. Inset, Tuning direction of each RA LTMR (n = 21). C, Histogram shows the number of RA LTMRs with the angle sizes of high sensitivity. The angle size of high sensitivity was defined as the angle size at which responses were ≥80% of maximal impulses. The bin is 30°. Black bars, ramp-up responses; gray bars, ramp-down responses. D, Histogram shows the number of RA LTMRs with different tuning indexes. The bin of tuning index is 0.1. Black bars, ramp-up responses; gray bars, ramp-down responses. E, Sample traces of RA LTMR impulses induced by a 50-μm (top) and a 200-μm (bottom) ramp-and-hold deflection of a whisker hair in the most sensitive direction. F, RA impulse numbers induced by whisker hair deflection at the most sensitive angle at the amplitudes of 10, 20, 50, 100, 200, 300, 400, and 500 μm (n = 5 for 10–200 μm, 4 for 300–400 μm, and 3 for 500 μm). Dotted line is the curve fitting the experimental data. Data represent mean ± SEM.

  • Figure 3.
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    Figure 3.

    Angular responses of SA1 LTMRs in whisker hair follicles. A, Sample trace (top panel) shows SA1 LTMR impulses in response to ramp-and-hold whisker hair deflection in 24 angular directions each at the amplitude of 200 μm. Whisker hair deflection at each angle is indicated under the sample trace. Bottom three traces are impulses at the expanded time scale from arrow-indicated angles in the top panel, one was the most sensitive angle (−30° to the caudal direction) at which maximal numbers of impulses were evoked in both the dynamic and static phase (left panel), another was the angle at which impulses were evoked only in the ramp-up dynamic phase (middle panel), and the third was the angle at which impulses were evoked in both ramp-up and ramp-down dynamic phases (right panel). The sample traces were recorded from a left C3 whisker hair follicle. B, A different SA1 displaying impulses during the ramp-down dynamic phase (top panel) or impulses during and after ramp-down dynamic phase (bottom trace, postramp). The sample traces were recorded from a left C3 whisker hair follicle. C, Summary data (n = 19) of the sizes of the angles showing impulses in both dynamic and static phase (SA1), during and after ramp-down phase (postramp), only during dynamic phase (RA-like), and the sizes of the angles showing no response (null angle). D, Summary data (n = 19) of the angle sizes of RA-like subclasses with impulses only during ramp-up phase, impulses in both the ramp-up and ramp-down phases, impulses only during the ramp-down phase. E, Instantaneous frequency of impulses at the most sensitive angle shown in A. F, Summary data (n = 19 recordings) of coefficient of variance of interevent intervals of impulses at the most sensitive angles exemplified in A. G, Summary data (n = 19) of impulse frequency of SA1 LTMRs in the dynamic phase (234 ms) and static phase (4.75 s) at most sensitive angles exemplified in A. Data represent mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significantly different.

  • Figure 4.
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    Figure 4.

    Angular tuning parameters and amplitude encoding of SA1 LTMRs. A, Polar plot shows an example of angular response of an SA1 LTMR. Arrow in the plot indicates the vector of the angular response. Concentric circles and numbers indicate impulse numbers. B, Bar graph shows the number of SA1 LTMRs displaying angular tuning to the caudal (caudal ±45°), ventral (ventral ±45°), rostral (rostral ±45°), and dorsal (dorsal ±45°) directions. Inset, Tuning directions of each SA1 LTMR recorded (n = 19). C, Histogram shows distribution of SA1 LTMRs with the angle sizes of high sensitivity. The bin is 30°. D, Histogram shows distribution of SA1 LTMRs with different tuning indexes. The bin of tuning index is 0.1. E, Sample traces show SA1 impulses induced by a 50-μm (top) and a 500-μm (bottom) ramp-and-hold deflection of a whisker hair in the most sensitive direction. F, SA1 impulse numbers induced by whisker deflection at the amplitudes of 10, 20, 50, 100, 200, 300, 400, and 500 μm (n = 4). Dotted line is the curve fitting the experimental data. Data represent mean ± SEM.

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    Figure 5.

    Angular responses of SA2 LTMRs in whisker hair follicles. A, Sample trace (top panel) shows SA2 LTMR impulses in response to ramp-and-hold whisker hair deflection in 24 angular directions each at the amplitude of 200 μm. Whisker hair deflection at each angle is indicated under the sample trace. Bottom three traces are impulses at the expanded time scale from arrow-indicated angles in the top panel, one was the angle at which impulses were evoked only in the ramp-up dynamic phase (left panel), another was the most sensitive angle at which maximal numbers of impulses were evoked in both the dynamic and static phase (middle panel), and the third was the angle at which impulses were evoked in both the ramp-up and ramp-down dynamic phases (right panel). The sample traces were recorded from a right D3 whisker hair follicle. B, A different SA2 displaying impulses during the ramp-down dynamic phase (top panel) or impulses during and after ramp-down dynamic phase (bottom trace, postramp). The sample traces were recorded from a right D3 whisker hair follicle. C, Summary data (n = 23) of the sizes of the angles showing impulses in both dynamic and static phase (SA2), during and after ramp-down phase (postramp), only during dynamic phase (RA-like), and the sizes of the angles showing no response (null angle). D, Summary data (n = 23) of the angle sizes of RA-like subclasses with impulses only during ramp-up phase, impulses in both the ramp-up and ramp-down phases, impulses only in the ramp-down phase. E, Instantaneous frequency of impulses at the most sensitive angle shown in A. F, Summary data (n = 23) of coefficient of variance of interevent intervals of impulses at the most sensitive angles exemplified in A. G, Summary data (n = 23) of impulse frequency of SA2 LTMRs in the dynamic phase (234 ms) and static phase (4.75 s) at most sensitive angles exemplified in A. Data represent mean ± SEM, *p < 0.05, ***p < 0.001, ns, not significantly different.

  • Figure 6.
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    Figure 6.

    Angular tuning parameters and amplitude encoding of SA2 LTMRs. A, Polar plot shows an example of angular response of an SA2 LTMR. Solid arrow indicates the vector of angular responses. Concentric circles and numbers indicate impulse numbers. B, Bar graph shows numbers of SA2 LTMRs that display angular tuning in the caudal (caudal ±45°), ventral (ventral ±45°), rostral (rostral ±45°), and dorsal (dorsal ±45°) directions. Inset is the tuning direction of each SA2 LTMR recorded (n = 23). C, Histogram shows distribution of SA2 LTMRs with the angle sizes of high sensitivity. The bin is 30°. D, Histogram shows distribution of SA2 LTMRs with different tuning index. The bin of tuning index is 0.1. E, Sample traces of SA2 impulses induced by a 50-μm (top) and a 500-μm (bottom) ramp-and-hold deflection of a whisker hair in the most sensitive direction. F, SA2 impulse numbers induced by whisker hair deflection at the amplitudes of 10, 20, 50, 100, 200, 300, 400, and 500 μm (n = 6). Dotted line is the curve fitting the experimental data. Data represent mean ± SEM.

  • Figure 7.
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    Figure 7.

    Comparison of angular tuning and amplitude encoding among RA, SA1, and SA2 LTMRs. A, Comparison of tuning index among SA1 (n = 19), SA2 (n = 23), and RA (n = 21). B, Comparison of the angle sizes of high sensitivity among SA1 (n = 19), SA2 (n = 23), and RA (n = 21). C, Comparison of angle sizes of null responses among SA1 (n = 19), SA2 (n = 23), and RA (n = 21). D, Comparison of impulse frequencies at the dynamic phase among SA1 (n = 19), SA2 (n = 23), and RA (n = 21). E, Comparison of the impulse frequencies at the static phase among SA1 (n = 19), SA2 (n = 23), and RA (n = 21). From A–E, impulses were elicited by whisker hair deflection at the amplitude of 200 μm in testing directions. Data represent mean ± SEM, *p < 0.05, **p < 0.01, ***p < 0.001, ns, not significantly different.

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Angular Tuning Properties of Low Threshold Mechanoreceptors in Isolated Rat Whisker Hair Follicles
Akihiro Yamada, Hidemasa Furue, Jianguo G. Gu
eNeuro 14 November 2022, 9 (6) ENEURO.0175-22.2022; DOI: 10.1523/ENEURO.0175-22.2022

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Angular Tuning Properties of Low Threshold Mechanoreceptors in Isolated Rat Whisker Hair Follicles
Akihiro Yamada, Hidemasa Furue, Jianguo G. Gu
eNeuro 14 November 2022, 9 (6) ENEURO.0175-22.2022; DOI: 10.1523/ENEURO.0175-22.2022
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Keywords

  • angular tuning
  • directional selectivity
  • low threshold mechanoreceptors
  • sensory encoding
  • tactile
  • whisker hair follicle

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