The problem of temporal coding in cochlear implants

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1 The problem of temporal coding in cochlear implants Ian C. Bruce McMaster University Hamilton, Ontario

2 Outline Why temporal coding for CIs is problematic Analysis of data from Wise et al. (CIAP 2009) and some other published data gives insight into the physiological issues A computational model of auditory nerve fibers helps explain some of the membrane mechanisms 2

3 CI Speech Processor Design (Clark, 1998 ) Neural Response? 3

4 Problems with spatial aspects of response patterns 1. Field interactions non-simultaneous stimulation needed 2. Current spread excitation of broader neural population than desired maybe current steering or higherdensity electrode arrays can help? 4

5 Problems with temporal aspects of response patterns? 1. Restricted dynamic range Problems with coding via spike rate 2. Temporal precision Better than acoustic stimulation 3. Temporal interactions Historically thought to be only very brief refractory effects 5

6 Refractoriness (Miller et al., 2001) 6

7 Refractoriness (Miller et al., 2001) 7

8 Resulting widely held beliefs The real problems for cochlear implants are current spread and dynamic range Temporal coding should be as good or better than acoustic stimulation, and consequently High-rate stimulation strategies should be able to convey more acoustic information Temporal pitch perception should be as good or better than acoustic perception 8

9 Speech Perception vs Pulse Rate (Nie et al., 2006 ) (Weber et al., 2007 ) See Arora et al. (Int. J. Audiol., 2009) for a recent review. 9

10 Rate Pitch Perception (Zeng, 2002) (Kong and Carlyon, 2010) 10

11 What is the physiological basis for these perceptual results? Need to look more closely at the physiological data, including Cat AN fiber data of Wise et al. (CIAP 2009): Neonatal cats (n=9) ototoxically deafened with neomycin and at two months of age were implanted with a seven-channel intracochlear electrode array. Environmentally derived ICES was delivered chronically for six months in 8 of these cats. Age-matched control cats (n=4) were acutely deafened at the time of the electrophysiological experiment. 11

12 Rate entrainment properties (Wise et al., 2009) Why do some fibers have higher maximum entrainment rates than others? What is causing the difference between the chronically stimulated (ICES) and acutely-deafened (Control) cats? 12

13 Possible temporal interactions Refractoriness drop in excitability following a spike Spike-rate adaptation drop in excitability due to ongoing spiking Accommodation drop in excitability due to sub-threshold responses Facilitation increase in excitability due to sub-threshold responses 13

14 Absolute refractory period (Wise et al., 2009) Absolute refractory period (ARP) is slightly longer in control cats However, this cannot directly explain why some fibers cannot entrain to rates much beyond 300 pps 14

15 Relative refractoriness (Miller et al., 2001) (Cartee et al., 2000) 15

16 Relative refractoriness in humans (as per the ECAP) (Cohen, 2009e) (Botros and Psarros, 2010) 16

17 Accommodation/Adaptation (Zhang et al., 2007) 17

18 Accommodation/Adaptation (Sly et al., CIAP 2005) 18

19 Explanation of entrainment from low-rate response properties? Wise et al. did not measure relative refractoriness and adaptation/ accommodation in detail. However, they did measure input/output (I/O) functions for 200-pps pulse trains. Can the maximum entrainment rate behaviour be inferred from the 200-pps burst behaviour? 19

20 First Pulse I/O Functions 20

21 Burst (200pps) I/O Functions 21

22 Burst response variability 22

23 Revisiting max rate results 23

24 Revisiting max rate results 24

25 Revisiting max rate results 25

26 Causes of variability in max rate? Significant (just) but very weak correlations for pooled data However, these two factors are correlated, so very little gained in stepwise regression Probably require better measures of relative refractoriness and accommodation/adaptation 26

27 Cause of abnormally-high max entrainment rates? Facilitation 200 pps!!) 27

$Absolute refractory period Latency (Wise et al.$

28 Other factors to consider (for which we have data) Absolute refractory period Latency (Wise et al., 2009) 28

29 Stochastic Fast-Sodium and Delayed-Rectifier Model (Negm & Bruce, IEEE EMBC 2008; Mino et al., IEEE TBME 2004 ) 29

30 Addition of I KLT and I h Channels (Negm & Bruce, IEEE EMBC 2008; Rothman & Manis, J Neurophysiol 2003) 30

31 Ion Channel Properties Fast-sodium and delayed-rectifier potassium channels of HH model: 1. Closed at resting potential 2. Gating dynamics ~ 1 μs to 1 ms I h and I KLT channels: 1. Partially open at resting potential 2. Gating dynamics ~ 0.1 to 100 ms 31

32 Data 32

33 Model Predictions (Adapted from Negm & Bruce, IEEE EMBC 2008) 33

34 Data (Sly et al., CIAP 2005) 34

35 Model Predictions 35

36 Example membrane potentials 36

37 Data (Miller et al., 2001) 37

38 Model Predictions 38

39 Model I/O Functions 39

40 Model Variance per Pulse 40

41 Model Rate Entrainment 41

42 Model PSTHs for 800 pps 42

43 HCN Channel Location (Yi et al., 2010) 43

44 Conclusions There is substantial heterogeneity in the temporal interactions exhibited by different AN fibers I KLT and I h appear to explain a number of these interactions, except long relative refractoriness Rate entrainment behaviour in single AN fibers is fairly consistent with the psychophysical data 44

45 Future Directions Effects of neurotrophin treatment, etc. on ion channel properties and consequently temporal response properties Other factors contributing to max entrainment behaviour Channel location and density on fiber Improved ion channel models, and additional ion channels to consider 45

46 Acknowledgments Modelling Work: Mohamed Negm Robin Davis & Paul Manis Laurie Cohen, Tony Burkitt & David Grayden Mark White, Leon Heffer, David Sly & Stephen O Leary Auditory Nerve Physiology: Andrew Wise, James Fallon, Stephen O Leary, David Sly & Robert Shepherd Alison Neil, Anne Coco, Jin Xu, Tom Landry & Elisa Borg Funding: The Bionic Ear Institute The University of Melbourne Barber Gennum Chair Endowment NSERC Discovery Grant The NIDCD (HHS-N C) The Garnett Passe and Rodney Williams Memorial Foundation The Marian E. H. Flack Trust 46

47 Thanks! Questions? 47

48 HCN Channel Location (Yi et al., 2010) 48

49 Temporal Precision (Hartmann et al., 1984) 49

50 Temporal Precision (Hartmann et al., 1984) 50

51 Channel Type and Location? (Hossain et al., 2005) 51

52 Channel Type and Location? (Lai and Jan, 2006) 52

53 Effect of Ion Channels on AP 53

54 Activation/Inactivation 54

55 Gating Time Constants 55

56 Activation/Inactivation 56

57 Gating Time Constants 57

58 Inter-pulse Membrane Potential 58

59 Mid-train Single Spike 59

60 Zero Injected Current 60

61 Revisiting max rate results 61

62 Heffer et al. (CIAP 2009) model 62

63 Auditory periphery model (Zilany et al., 2009) 63

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