Neural Plasticity and Attention in Normal Hearing and in Tinnitus

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1 Neural Plasticity and Attention in Normal Hearing and in Tinnitus Larry E. Roberts Department of Psychology, Neuroscience, and Behaviour McMaster University, Hamilton, Ontario, Canada; Over the Horizon: 8 th International TRI Tinnitus Conference Auckland, New Zealand, March With appreciation to the Neurological Foundation of New Zealand and the New Zealand Tinnitus and Hyperacusis Network TINNITUS RESEARCH INITIATIVE

2 Recanzone et al Frequency tuning Tuning bandwidth Spike rates Response latency Neural plasticity on this scale should be expressed in AEPs and AEFs

Auditory Projection Pathway Frontal/Temporal Cortex Oscillatory activity Nonprimary Auditory Cortex N1, Ta, N1c, P2, N2 Primary Auditory Cortex MLRs, 40-Hz ASSR Subcortical Structures FFRs ABRs

3 Auditory Projection Pathway Frontal/Temporal Cortex Oscillatory activity Nonprimary Auditory Cortex N1, Ta, N1c, P2, N2 Primary Auditory Cortex MLRs, 40-Hz ASSR Subcortical Structures FFRs ABRs Intrinsic alertness network - Dosenbach et al 2006, 2007 Orienting top-down system and the cingulo-opercular task maintenance network - Peterson and Posner 2102 Default mode network Raichle 2001, 2010 Dorsal visual attention system - Corbetta and Schulman 2002

4 Three Topics: (1) What are rules for plasticity and attention in normal hearing subjects? (2) Are these rules changed in tinnitus? (3) Sound therapy for tinnitus

5 P2 and N1c are Neuroplastic, N1 is not Laboratory Training Professional Musicians 2 khz 40-Hz AM tone violin and piano tones Bosnyak, Eaton, & Roberts (2004) Cerebral Cortex 14:1088-l099. Shahin, Bosnyak, Trainor, and Roberts (2003) J. Neuroscience 23,

2000 Hz carrier AM @ 40 Hz Amplitude and

6 40-Hz How We Auditory Study Steady Acoustic State Training Response (ASSR) 2000 Hz carrier 40 Hz Amplitude and phase ASSR sources localize tonotopically to A1

Amplitude of the ASSR is Modulated Attention ASSR Phase by Experience 2000 Hz carrier AM @ 40 Hz Subjects trained to detect targets in a 2-kHz 40-Hz AM sound Alternating active/passive blocks p = 0.

7 Amplitude of the ASSR is Modulated Attention ASSR Phase by Experience 2000 Hz carrier 40 Hz Subjects trained to detect targets in a 2-kHz 40-Hz AM sound Alternating active/passive blocks p = N1 amplitude increased with attention but not with experience p = p = P2 amplitude increased on day 2, in both groups Group E Group C1 Gander, Bosnyak, & Roberts (2010) Hearing Research 269:81-94

9 Results Suggest These Principles for the Normal Hearing Adult Brain: (1) Competitive interactions in A1 constrain cortical representations for trained sounds (ASSR Amplitude does not increase); (2) Cortical representations in nonprimary cortex are more plastic (P2 and N1c amplitudes increase); (3) The temporal response properties of neurons in A1 are modified by experience with sound (ASSR phase changes with sound exposure); (4) Attention increases the neural population engaged during learning (ASSR and N1 amplitude increase); (5) But attention is not required for auditory remodeling; (6) Some neuroplastic effects are developmentally dependent (P2) and others not (ASSR phase); (7) Modulation by attention is not expressed in AEPs until early adolescence.

10 Three Topics: (1) What are rules for plasticity and attention in normal hearing subjects? (2) Are these rules changed in tinnitus? (3) Sound therapy for tinnitus

11 Almost everything changes, when training is given in the Tinnitus Frequency Region: (1) ASSR Amplitude increases with training for a 5 khz 4- Hz AM sound; (2) Changes in ASSR phase are abolished; (3) Modulation of ASSR and N1 Amplitude by attention is abolished or impaired; (4) But P2 amplitude increases normally with training in Tinnitus

12 11 tinnitus subjects 11 control subjects Age and hearing level matched Trained for 7 sessions to detect targets in a 5 khz 40-Hz AM sound in the TFR of the tinnitus subjects Alternating active/passive blocks Roberts, Bosnyak, & Thompson (2012) Front. Syst. Neurosci. 6:40. doi: /fnsys

13 ASSR Phase:

14 ASSR and N1 amplitude: N1 p = 0.03 ASSR p = 0.05 p = way p = way

15 Attention Effects (active minus passive blocks) Probe 5 khz ASSR N1 tinnitus controls Day 1

16 Attention Effects (active minus passive blocks) Probe 500 Hz Probe 5 khz ASSR N1 tinnitus controls Day 1

17 Tinnitus: baseline

18 Tinnitus: detect 5 khz target PFC Attention System Task Requirement (detect 5 khz targets)

19 Tinnitus: detect 500 Hz target PFC Attention System Task Requirement (detect 500 Hz targets)

20 Rules of Plasticity and Attention in tinnitus: (1) Cortical representations can grow in TFR of A1 for trained sounds; (2) Cortical representations in A2 remain plastic (maybe more so); (3) Temporal changes normally expressed in A1 are obstructed, more so if the training sound nears the peak of the tinnitus spectrum; (3) Top-down auditory attention works normally in tinnitus, but modulation of tinnitus-related neural activity in A1 and A2 is obstructed; (4) These effects are consistent with the neural changes seen in tinnitus accompanied by hearing loss: (decreased inhibition and increased spontaneous/synchronous neural activity in the hearing loss regions of auditory cortex)

21 Three Topics: (1) Neural Plasticity in normal hearing (2) Are the rules changed in tinnitus? (3) Sound therapy for tinnitus

22 Does Sound Therapy Work for Tinnitus?

23 Does Sound Therapy Work for Tinnitus? Active training within the TFR Flor, Hoffmann, Struve, Diesch (2004) Appl. Psychophysiol. Biofeedback 29(2): Herriaz, Diges, Cobo, Plaza, Aparicio (2006) Acta Oto-Laryngologica 126:8083. Herriaz, Diges, Cobo, Aparicio (2009) Eur. Arch Otorhinolaryngol. 266:9 16 Noreña, Micheyl, Chéry-Croze, Collet (2002) Audiol. Neurootol. 7: Active training outside the TFR Searchfield, Morrison-Low, Wise (2007) Prog. Brain Res. 166: Baguley, Atlas (2007) Prog. Brain Res. 166: Folmer, Carroll (2006) Otolaryng. Head Neck Surg. 134: Moffat, Adjout, Gallego, Thai-Van, Collet, A Norena (2009) Hearing Res. 254: Passive experience within the TFR Davis, Paki, Hanley (2007) Ear & Hearing 28(2): Davis, Wilde, Steed, Hanley (2008) Ear, Nose and Throat Journal 87: Hanley, Davis, Paki, Quinn, Bellekom (2008) Ann. Otol. Rhinol. Laryngol. 117: Folmer, Carroll (2006) Otolaryng. Head Neck Surg. 134: Henry, Schechter, Zaugg et al (2006) J. Am. Acad. Audiol. 17: Passive experience outside the TFR Okamoto, Stracke, Stoll, Pantev (2010) Proceed. Nat. Acad. Sci. USA Tiesman, Okamoto, and Pantev PLoS One (2011). Tass et al. Restorative Neurology and Neuroscience 30 (2012) studies overall 7 best results (all subjects): VAS % Monitoring alone: -12.0% Effect of Sound Therapy: - 8.4% Roberts and Bosnyak (2010). In A. Moller, et al..(eds) Textbook of Tinnitus Humana Springer Press] (Updated) These results are disappointing

24 Does sound matter at all? Here are some reasons why it should

25 Local field potentials Normal hearing cat exposed to 4-20 khz tone pip ensemble 68 db SPL 6 to 8 weeks Cats sleep a lot 12h/day control 24h/day control exposed exposed 1-3 weeks 8-12 weeks Recovery control exposed Pienkowski M, Eggermont JJ. Ear Hear May-Jun;33(3):

Map Reorganization Noreña & Eggermont, 2005. J. Neurosci.

26 Loudness Growth 23h/day 2 weeks Formby, Sherlock, & Gold (2003) J. Acoust. Soc. Am. 114: Map Reorganization Noreña & Eggermont, J. Neurosci. 25, EAE 6-20 khz High frequency ABR thresholds recovered in these animals

27 Is Cochlear damage a game-changer? (1) Loss of inhibition means that neural representations can increase in Tinnitus Frequency Region; (2) Increased and persistent activity in attention networks; (3) Tinnitus-related neural changes consequent on deafferentation may impede therapeutic remodeling by sound exposure; (Training with a pure tone in the TFR is not a good idea)

28 Roberts, Moffat, Baumann, Ward, and Bosnyak (2008) J. Res. Otolaryngology (JARO) 9: Schaette & McApline Gu & Melcher Hebert & Fournier Kujawa & Liberman

29 Roberts, Moffat, Baumann, Ward, and Bosnyak (2008) J. Res. Otolaryngology (JARO) 9:

remodeling impaired outside of the TFR of tinnitus sufferers? (4) Immersion in sound: sleep?

30 A To-Do List (1) We need better measures of cochlear pathology than the audiogram (2) Animal studies could tell us how suppression of neuron response properties by sound is modulated by different levels of threshold shift: (3) Is neural remodeling impaired outside of the TFR of tinnitus sufferers? (4) Immersion in sound: sleep? (5) Does early intervention with sound improve cochlear function? (6) Hearing restoration technologies (7) Invest in prevention of hearing loss

Dangerous Decibels (William Martin) www.dangerousdecibels.org Roberts, Martin, & Bosnyak (2010).

31 Dangerous Decibels (William Martin) Roberts, Martin, & Bosnyak (2010). The prevention of tinnitus and noise-induced hearing loss. Textbook Of Tinnitus Eds: Møller et. Humana-Springer (pp )

32 Ground-Shaking Noise Rocks N.F.L., and Eardrums Take Big Hit November by Joyce Cohen Arrowhead Stadium, Kansas City, October 13, 2013 World Record db A scale

33 With thanks to: Tinnitus Plasticity Ian Bruce Dan Bosnyak Brandon Paul Antoine Shahin Laurel Trainor Graeme Moffat V ictoria Mosher Taylor Tuff Dave Thompson Phil Gander Scott Baynton The Neurological Foundation of New Zealand and the New Zealand Tinnitus and Hyperacusis Network TINNITUS RESEARCH INITIATIVE

Chapter 72 Auditory Training in Tinnitus

Chapter 72 Auditory Training in Tinnitus Larry E. Roberts and Daniel J. Bosnyak Keypoints 1. We reviewed sensory training studies from the point of view that tinnitus is caused by synchronous neural activity