Original Paper Audiology Neurotology
Audiol Neurotol 2009;14:39–53 DOI: 10.1159/000153434
Received: August 22, 2007 Accepted after revision: June 11, 2008 Published online: September 10, 2008
Cortical Neural Activity Underlying Speech Perception in Postlingual Adult Cochlear Implant Recipients Yael Henkin a, b Simona Tetin-Schneider a, b Minka Hildesheimer a, b Liat Kishon-Rabin a a b
Department of Communication Disorders, Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, and Speech and Hearing Center, Sheba Medical Center, Tel Hashomer, Israel
Key Words Auditory event-related potentials ⴢ P3 potential ⴢ Cochlear implant ⴢ Postlingual adults ⴢ Speech perception ⴢ Phonetic processing
Abstract Auditory event-related potentials (AERPs) and the simultaneously obtained behavioral measures (performance accuracy and reaction time) were used to study speech perception in postlingual adult cochlear implant (CI) recipients and in normal-hearing (NH) controls. AERPs were recorded while subjects were performing oddball discrimination tasks with increasing acoustic-phonetic demand. The tasks consisted of pairs of natural syllables that differed by one of the following phonetic contrasts: vowel place, voicing, vowel height, and place of articulation. Results indicated that the P3 potential was comparable in CI recipients and NH controls when the acoustic cues to the perception of the phonetic contrast were accessible. With the reduction in accessibility to the essential temporal and/or spectral cues, CI recipients exhibited delayed (prolonged P3 latency) and less synchronous (reduced amplitude) central speech-sound processing compared to NH controls. Among the phonetic contrasts used in the present study the place of articulation contrast yielded (1) the most prominent differences between CI recipients and NH controls across all measures, and (2) signifi-
© 2008 S. Karger AG, Basel 1420–3030/09/0141–0039$26.00/0 Fax +41 61 306 12 34 E-Mail
[email protected] www.karger.com
Accessible online at: www.karger.com/aud
cant correlations between the neurophysiologic manifestation of speech discrimination (i.e. P3 latency), and conscious integration of perceptual information (i.e. performance accuracy and reaction time). Thus, P3 exposed the difficulties imposed on the impaired auditory system of CI recipients especially when elicited by speech contrasts that required processing of brief temporal-spectral cues. These findings support the P3 potential as a sensitive neural index of cortical processing that may provide information regarding accessibility and neural encoding of distinct acoustic-phonetic cues in CI recipients. Copyright © 2008 S. Karger AG, Basel
Introduction
Auditory event-related potentials (AERPs) are measures of central auditory function that trace events in time that reflect different stages of neural processing [Hillyard and Kutas, 1983; Kutas and Dale, 1997; Polich and Herbst, 2000; Stapells, 2002]. As such, they may tap into neural encoding of acoustic properties in the central auditory system. These attributes are of great value for the study of speech perception, as the latency of AERP components provide information regarding the timing of the stimulus evaluation process, and the amplitude is thought to reflect the degree of neural synchronization Yael Henkin, PhD Department of Communication Disorders Sheba Medical Center Tel Hashomer, Ramat Gan, 52621 (Israel) Tel. +972 3 534 9817, ext. 101, Fax +972 3 535 2868, E-Mail
[email protected]
evoked by the stimulus [Polich and Herbst, 2000; for review, see Polich, 2007]. AERPs may therefore contribute significantly to the understanding of how the brain uses limited acoustic information provided by a cochlear implant (CI) for processing speech. Several studies attempted to investigate speech perception in CI recipients by means of AERPs. For example, Kraus et al. [1993] and Micco et al. [1995] showed that the mismatch negativity and P3 potentials of ‘good’ CI recipients were remarkably similar to those of normalhearing (NH) controls. The potentials were elicited by pairs of stimuli, that differed by a vowel contrast (/da/ vs. /di/) [Micco et al., 1995] or by a consonant contrast (/da/ vs. /ta/) [Kraus et al., 1993]. Groenen et al. [2001] and Beynon et al. [2005] recorded the P3 potential in adult CI recipients and showed that while a vowel discrimination task (/i/ vs. /a/) elicited P3 potentials similar to those of NH subjects, consonant discrimination tasks (/ba/ vs. /pa/, /ba/ vs. /da/) yielded a smaller, prolonged, or absent P3. The fact that P3 of CI recipients was similar to that recorded from NH subjects in the easier vowel discrimination task suggests that these stimuli may not be sensitive to the differences in central auditory processing between the two groups. On the other hand, the prolonged or absent P3 in the consonant discrimination tasks may reflect auditory processing difficulties of CI recipients in general and of ‘poor’ CI recipients in particular [Kutas et al., 1977; Kraus et al., 1995; Maiste et al., 1995; Henkin et al., 2002; Roman et al., 2004; Kelly et al., 2005]. The identification of speech stimuli that will be sensitive to differences in auditory processing between CI recipients and NH controls requires administering a hierarchical set of speech tasks with different acoustic-phonetic demands. We have recently shown in prelingually deafened children with CI that the P3 potential was sensitive to the hierarchy and complexity of the temporalspectral characteristics of natural speech stimuli. Specifically, P3 elicited by vowel place discrimination was the shortest (mean latency 543 ms) and was prolonged by 101, 147, and 175 ms for voicing, vowel height, and place of articulation discrimination, respectively [Henkin et al., 2008]. Thus, these results provided insight into the accessibility (i.e. ability of the CI device to provide the necessary acoustic cues) and processing of speech stimuli of varying degrees of difficulty. To our knowledge, in adult CI recipients, only Groenen et al. [2001] and Beynon et al. [2005] recorded AERPs to stimuli with different syllable structure and phonetic complexity [vowel (/i/ vs. /a/) and consonant contrasts (e.g. /ba/ vs. /pa/). However, they utilized short synthetic speech stimuli limiting accurate in40
Audiol Neurotol 2009;14:39–53
ferences regarding the processing of natural speech stimuli. The main goal of the present study was, therefore, to characterize the P3 potential elicited by a hierarchical set of oddball discrimination tasks that consisted of natural phonetic contrasts and differed by the salience of their acoustic cues (i.e. temporal or spectral) [Kishon-Rabin et al., 2002; Henkin et al., 2008] in a group of postlingual CI recipients and a group of NH controls. Two additional goals were: (1) To examine the relationship between P3 (latency and amplitude) and the behavioral measures (performance accuracy and reaction time) in an attempt to elucidate to what degree can neurophysiologic measures predict behavior. In general, there is inconsistency regarding this relationship, presumably due to the different levels of processing that are involved during each measure. Specifically, in CI recipients, some studies reported significant correlations between speech perception and discriminative AERPs (e.g. P3) [Kileny et al., 1997] whereas others did not [mismatch negativity, Wable et al., 2000; N1-P2, Firszt et al., 2002; P3, Henkin et al., 2008]. (2) To discuss the resulting data from postlingually deafened adult CI recipients in comparison to data from prelingually deafened children with CI using the same methodology [Henkin et al., 2008].
Methods Subjects Fifteen postlingually deafened adults (10 females) using a unilateral CI participated in the study. All had bilateral profound hearing loss prior to implantation and were tested at a mean age of 51 years (range 30–68 years). Six used the Nucleus 22 with the SPEAK speech-processing strategy; 5 used the Nucleus 24C with the ACE speech-processing strategy, and 4 used the MED-EL Combi 40+ with the CIS+ speech-processing strategy. Table 1 provides individual background information including: gender, age at the time of testing, etiology of deafness, duration of deafness before implantation, CI side, duration of CI use, type of device, speech-processing strategy, pure-tone average at 0.5, 1, 2 kHz with CI, and performance scores in the Hebrew AB one-syllable word test [Boothroyd, 1968; Taitelbaum-Swead et al., 2005]. AB scores were obtained prior to the AERP recording session in all but 2 patients in which scores were obtained 2–4 weeks prior to the recording session. A control group of 12 subjects (8 females) were tested at a mean age of 49.4 years (range 33–57 years). All subjects exhibited normal hearing for octave frequencies between 250 and 8000 Hz. Past medical history was unremarkable. All but 1 CI recipient exhibited well-defined right-handedness based on the Edinburgh Inventory for Handedness [Oldfield, 1971]. A left-handed NH subject was matched to the left CI recipient.
Henkin /Tetin-Schneider /Hildesheimer / Kishon-Rabin
Table 1. Patient background information Patient Male/ female
Age
Etiology
Profound CI use deafness years years
Device
Strategy
CI side
Average thresholds AB word at 0.5, 1, 2 kHz scores, % with CI, dB HL
1a 2a 3 4 5 6a 7a 8 9a 10 11a 12a 13a 14a 15a
56.2 68 57 47.5 56.2 54.5 33.5 44.2 44 57 38 30 63 64.5 56.6
chronic ear infection progressive SNHL polio viral infection ototoxicity unknown hereditary SNHL ototoxicity chronic ear infection trauma viral infection unknown Ménière progressive SNHL progressive SNHL
4 4 3 10 13 3 7 5 11 9 1.5 1.5 2 9 7
Nucleus 22 Nucleus 22 Nucleus 22 Nucleus 22 Nucleus 22 Nucleus 22 MED-EL MED-EL MED-EL MED-EL Nucleus 24C Nucleus 24C Nucleus 24C Nucleus 24C Nucleus 24C
SPEAK SPEAK SPEAK SPEAK SPEAK SPEAK CIS+ CIS+ CIS+ CIS+ ACE ACE ACE ACE ACE
left left right left right right right right right right right right right right left
26.6 28.3 35 33.3 33.3 25 21.6 20 26.6 20 30 26.6 30 26.6 31.66
F F F M M F F M M F F F F M F a b
12.2 10.4 6.5 13 13.5 6.2 2.7 1 1.2 2.3 4.8
