1. SCC Afferents Kim McArthur Vestibular Classics November 3, 2006

2. Overview Review: SCC Mechanics Afferent Peripheral Morphology Afferent Physiology Proposed Mechanisms

3. Review: SCC Mechanics G. Melvill Jones (1972) Initial Position Q = head/canal displacement P = endolymph displacement CW moment: IPaccel  like ma CCW moments: B(Qvel-Pvel)  viscosity of endolymph (damping) K(Q–P)  elasticity of cupula (spring)

4. Review: SCC Transfer Function Q-P (s) = ___αT 1 T 2 s____ Qvel (T 1 s+1)(T 2 s+1) T 1 >>T 2 T 1 = B/K ; T 2 = I/B ; T 1 T 2 = I/K

5. Review: SCC Transfer Function HF range (ω>1/T 2 )  responsive to angular position (dominated by inertia) MF range (1/T 1 <ω<1/T 2 )  responsive to angular velocity (dominated by endolymph viscosity) LF range (ω<1/T 1 )  responsive to angular acceleration (both dominated by cupular elasticity) 1/T 1 G. Melvill Jones (1972) 1/T 2

6. Peripheral Morphology Dickman in Fundamental Neuroscience, 2 nd ed. (2002)

7. Peripheral Morphology Baird et al 1988 Dimorphic/HC/R Dimorphic/HC/Intermed Bouton/AC/R Calyx/HC/I Dimorphic/AC/I

8. Peripheral Morphology Haque, Huss & Dickman (2006)

9. Physiology Spontaneous discharge Spatial tuning Discharge regularity Sensitivity to galvanic stimulation Adaptation to constant velocity Dynamics (transfer function)

10. Physiology: Spontaneous Discharge Goldberg & Fernandez 1971

11. Physiology: Sinusoidal Response Goldberg & Fernandez 1971

12. Physiology: Sinusoidal Response Goldberg & Fernandez 1971

13. Physiology: Spatial Tuning Haque, Angelaki & Dickman 2004

14. Physiology: Spatial Tuning Haque, Angelaki & Dickman 2004

15. Physiology: Discharge Regularity Goldberg & Fernandez 1971

16. Physiology: Discharge Regularity Goldberg & Fernandez 1971 Baird et al 1988

17. Physiology: CV & Galvanic Sensitivity Baird et al 1988

18. Physiology: CV & Gain/Phase Baird et al 1988 Haque, Angelaki & Dickman 2004

19. Physiology: Adaptation Goldberg & Fernandez 1971

20. Physiology: Dynamics Goldberg & Fernandez 1971

21. Physiology: Dynamics Goldberg & Fernandez 1971

22. Physiology: Dynamics Baird et al 1988 Haque, Angelaki & Dickman 2004

23. To re-cap … Morphology: Type I hair cells – calyx (& dimorphic) afferent terminals in the central zone Type II hair cells – bouton (& dimorphic) afferent terminals in the peripheral zone

24. To re-cap … Physiology: Cosine tuning to canal planes Discharge regularity (CV) varies across the population Dynamics may differ from prediction based on torsion-pendulum model of SCC mechanics Adaptation  low-frequency phase lead Cupular velocity sensitivity  high-frequency phase lead and gain enhancement

25. Mechanisms: Co-variation of Properties Irregular afferents: Calyx/dimorphic terminals in the central zone Phasic-tonic response dynamics (adaptation + cupular velocity sensitivity) Large responses to efferent fiber stimulation Large, low threshold responses to galvanic stimulation Regular afferents: Bouton/dimorphic terminals in the peripheral zone Tonic response dynamics (resemble expectation from canal dynamics) Small responses to efferent fiber stimulation Small, high threshold responses to galvanic stimulation

26. Mechanisms: Discharge Regularity Compartmental cable calculations indicate that electronic distance has only a small effect on discharge regularity Dimorphic units with similar terminal branching patterns may be regular or irregular  Terminal branching pattern is not causally related to discharge regularity (may be causally related to location of the terminal within the neuroepithelium) Baird et al 1988

27. Mechanisms: Discharge Regularity General Model: Variability in the SD of ISI due to: Synaptic noise Slope of the recovery function Galvanic sensitivity will be tied to the recovery function, but will be independent of synaptic noise Goldberg, Smith & Fernandez 1984

28. Mechanisms: Discharge Regularity Prediction: If the shape of the recovery function is an important contributing factor in discharge regularity, then CV should correlate with galvanic sensitivity.  Irregular afferents will have higher sensitivity to galvanic stimulation Goldberg, Smith & Fernandez 1984

29. Mechanisms: Discharge Regularity Goldberg, Smith & Fernandez 1984  Afferent irregularity is causally related to its post-spike voltage recovery function (Irregular afferents have faster recovery, due to a smaller, more rapidly decaying K+ AHP)

30. Therefore … K+ AHP Slowly decaying  Slow recovery function Regular discharge (low CV) Low galvanic sensitivity Occurs more in peripheral zone Rapidly decaying  Rapid recovery function Irregular discharge (high CV) High galvanic sensitivity Occurs more in central zone

31. Mechanisms: Response Dynamics Dynamics in response to galvanic currents are similar for regular and irregular afferents (Goldberg, Fernandez & Smith 1982) Dynamics in response to natural stimulation differ (as previously shown)  Dynamics do not arise from the same mechanism as discharge regularity  Dynamics arise from transduction prior to the afferent spike encoder (probably during hair cell transduction)

32. Mechanisms: Synaptic Gain Synaptic gain = system gain / encoder gain (galvanic sensitivity) Bouton and dimorphic afferents have higher synaptic gains than calyx units, possibly due to the low input impedance of type I hair cells  Synaptic gain is causally linked to hair cell innervation (calyx units innervate type I hair cells – lower gain)

33. Therefore … Hair cell innervation Calyx units - Type I only  Low input impedance Smaller synaptic gains Bouton/Dimorphic units – also Type II  Higher input impedance Larger synaptic gains

34. SUMMARY Afferent discharge regularity and galvanic sensitivity are determined by the slope of the recovery function (K+ AHP), which may be determined by location within the crista Peripheral zone – slow recovery – regular Central zone – fast recovery – irregular Synaptic gains are determined by hair cell innervation Type I HC (calyx) – low synaptic gains Type II HC (bouton) – higher synaptic gains Response dynamics are probably determined by hair cell transduction (either intrinsic to the HC or characteristic of the synapse) Regular afferents tend to have more canal-like dynamics Irregular afferents exhibit more adaptation (low-frequency phase lead) and more cupular velocity sensitivity (high-frequency phase lead and gain enhancement) HOWEVER … dynamics are not determined by the recovery function, but by some correlated property prior to the spike encoder

35. Some Notes on Function Most secondary neurons receive mixed regular and irregular input VOR: Driven by regular afferents, modified by irregular afferents (?) VCR: Driven by irregular afferents (?)