Far-field responses to stimulation of the cochlear nucleus by microsurgically placed penetrating and surface electrodes in the cat

Restricted access

Object. A new generation of penetrating electrodes for auditory brainstem implants is on the verge of being introduced into clinical practice. This study was designed to compare electrically evoked auditory brainstem responses (EABRs) to stimulation of the cochlear nucleus (CN) by microsurgically implanted surface electrodes and insertion electrodes (INSELs) with stimulation areas of identical size.

Methods. Via a lateral suboccipital approach, arrays of surface and penetrating microelectrodes with geometric stimulation areas measuring 4417 µm2 (diameter 75 µm) were placed over and inserted into the CN in 10 adult cats. After recording the auditory brainstem response (ABR) at the mastoid process, the CN, and the level of the inferior colliculus, EABRs to stimulation of the CN were recorded using biphasic, charge-balanced stimuli with phase durations of 80 µsec, 160 µsec, and 240 µsec at a repetition rate of 22.3 Hz. Waveform, threshold, maximum amplitude, and the dynamic range of the responses were compared for surface and penetrating electrodes.

The EABR waveforms that appeared for both types of stimulation resembled each other closely. The mean impedance was slightly lower (30 ± 3.4 kΩ compared with 31.7 ± 4.5 kΩ, at 10 kHz), but the mean EABR threshold was significantly higher (51.8 µA compared with 40.5 µA, t = 3.5, p = 0.002) for surface electrode arrays as opposed to penetrating electrode arrays. Due to lower saturation levels of the INSEL array, dynamic ranges were almost identical between the two types of stimulation. Sectioning of the eighth cranial nerve did not abolish EABRs.

Conclusions. Microsurgical insertion of electrodes into the CN complex may be guided and monitored using techniques similar to those applied for implantation of surface electrodes. Lower thresholds and almost equivalent dynamic ranges indicate that a more direct access to secondary auditory neurons is achieved using penetrating electrodes.

Article Information

Address reprint requests to: Steffen K. Rosahl, M.D., International Neuroscience Institute, Alexis-Carrel-Strasse 4, D-30625 Hannover, Germany. email: rosahl@ini-hannover.de.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Intraoperative photographs. A: Microsurgical approach for placement of a penetrating microelectrode into the CN of the cat. A lateral suboccipital craniotomy is extended to the transverse sinus cranially and to the condyle and foramen magnum caudally, with partial removal of the C-1 arch. After the dura is opened, the flocculus of the cerebellum and the brainstem (bs) are visualized. B: The superior portion of the flocculus was aspirated and the INSEL array was moved forward to the petrous apex at the level of the ventral petrosal sinus (vps). To introduce the electrode anterolaterally into the depth between the seventh and eighth cranial nerves, the sinus must be dissected to allow for gentle medial retraction of the peduncular region. C: With the penetrating electrode in place, a surface electrode is slit in the direction of the tentorial notch so that a recording can be made from the proximal brainstem at the level of the IC.

  • View in gallery

    Traces of brainstem auditory evoked potentials (BAEPs). Upper: Auditory brainstem responses evoked by acoustic click stimulation with alternate polarity recorded from different locations before and after the eighth cranial nerve was sectioned. Note that the potential recorded from the penetrating electrode in the CN is 50 times larger than the far-field ABR measured at the mastoid process. Wave IV of the latter response corresponds to a prominent peak recorded from the vicinity of the IC. Lower: Following dissection of the auditory nerve, all brainstem components of the ABR were abolished and only an injury potential occurring within the time range of Wave I persisted. The vertical line on the left marks the time of stimulus onset. ms = millisecond.

  • View in gallery

    Traces showing responses to electrical stimulation of the CN recorded at the level of the IC and referenced to the vertex. The response persisted following complete sectioning of the eighth cranial nerve (N. VIII; bottom trace).

  • View in gallery

    Traces showing recorded EABRs to stimulation of the CN by surface electrodes (left) and INSELs (right) with increasing current intensities. Threshold and maximum stimulus currents were lower for penetrating stimulation.

  • View in gallery

    Bar graphs demonstrating a comparison between means and standard errors of the mean for independance (left), threshold (center), and dynamic range (right) of EABRs to stimulation of the CN with surface electrodes and INSELs. Despite lower thresholds for the INSEL array, the dynamic range was not significantly wider for stimulation with penetrating electrodes.

References

  • 1.

    Agnew WFMcCreery DBYuen TGet al: Effects of prolonged electrical stimulation of the central nervous system in Agnew WFMcCreery DB (eds): Neural Prostheses: Fundamental Studies. Englewood Cliffs, NJ: Prentice-Hall1990 pp 147168Agnew WF McCreery DB Yuen TG et al: Effects of prolonged electrical stimulation of the central nervous system in Agnew WF McCreery DB (eds): Neural Prostheses: Fundamental Studies. Englewood Cliffs NJ: Prentice-Hall 1990 pp 147–168

  • 2.

    Bourk TRMielcarz JPNorris BE: Tonotopic organization of the anteroventral cochlear nucleus of the cat. Hear Res 4:2152411981Bourk TR Mielcarz JP Norris BE: Tonotopic organization of the anteroventral cochlear nucleus of the cat. Hear Res 4:215–241 1981

  • 3.

    Brackmann DEHitselberger WENelson RAet al: Auditory brainstem implant: I. Issues in surgical implantation. Otolaryngol Head Neck Surg 108:6246331993Brackmann DE Hitselberger WE Nelson RA et al: Auditory brainstem implant: I. Issues in surgical implantation. Otolaryngol Head Neck Surg 108:624–633 1993

  • 4.

    Buchwald JSHuang C: Far-field acoustic response: origins in the cat. Science 189:3823841975Buchwald JS Huang C: Far-field acoustic response: origins in the cat. Science 189:382–384 1975

  • 5.

    Cohen ESBrawer JRMorest DK: Projections of the cochlea to the dorsal cochlear nucleus in the cat. Exp Neurol 35:4704791972Cohen ES Brawer JR Morest DK: Projections of the cochlea to the dorsal cochlear nucleus in the cat. Exp Neurol 35:470–479 1972

  • 6.

    Edell DJToi VVMcNeil VMet al: Factors influencing the biocompatibility of insertable silicon microshafts in cerebral cortex. IEEE Trans Biomed Eng 39:6356431992Edell DJ Toi VV McNeil VM et al: Factors influencing the biocompatibility of insertable silicon microshafts in cerebral cortex. IEEE Trans Biomed Eng 39:635–643 1992

  • 7.

    Edgerton BJHouse WFHitselberger W: Hearing by cochlear nucleus stimulation in humans. Ann Otol Rhinol Laryngol Suppl 91:1171241982Edgerton BJ House WF Hitselberger W: Hearing by cochlear nucleus stimulation in humans. Ann Otol Rhinol Laryngol Suppl 91:117–124 1982

  • 8.

    Eisenberg LSMaltan AAPortillo Fet al: Electrical stimulation of the auditory brain stem structure in deafened adults. J Rehabil Res Dev 24:9221987Eisenberg LS Maltan AA Portillo F et al: Electrical stimulation of the auditory brain stem structure in deafened adults. J Rehabil Res Dev 24:9–22 1987

  • 9.

    El-Kashlan HKNiparko JKAltschuler RAet al: Direct electrical stimulation of the cochlear nucleus: surface vs. penetrating stimulation. Otolaryngol Head Neck Surg 105:5335431991El-Kashlan HK Niparko JK Altschuler RA et al: Direct electrical stimulation of the cochlear nucleus: surface vs. penetrating stimulation. Otolaryngol Head Neck Surg 105:533–543 1991

  • 10.

    Frohne CLesinski AMatthies Cet al: Übersicht über die Ableitung früher auditorischer Potentiale bei elektrischer Stimulation. Audiologische Akustik 36:1681761997Frohne C Lesinski A Matthies C et al: Übersicht über die Ableitung früher auditorischer Potentiale bei elektrischer Stimulation. Audiologische Akustik 36:168–176 1997

  • 11.

    Gerken GMSaunders SSSimhadri-Sumithra Ret al: Behavioral thresholds for electrical stimulation applied to auditory brainstem nuclei in cat are altered by injurious and noninjurious sound. Hear Res 20:2212311985Gerken GM Saunders SS Simhadri-Sumithra R et al: Behavioral thresholds for electrical stimulation applied to auditory brainstem nuclei in cat are altered by injurious and noninjurious sound. Hear Res 20:221–231 1985

  • 12.

    Hitselberger WE: Auditory brain stem implant. Zentralbl Neurochir Suppl:1481998 (Abstract)Hitselberger WE: Auditory brain stem implant. Zentralbl Neurochir Suppl:148 1998 (Abstract)

  • 13.

    Hitselberger WEHouse WFEdgerton BJet al: Cochlear nucleus implants. Otolaryngol Head Neck Surg 92:52541984Hitselberger WE House WF Edgerton BJ et al: Cochlear nucleus implants. Otolaryngol Head Neck Surg 92:52–54 1984

  • 14.

    Hudson LCHamilton WP: Atlas of Feline Anatomy for Veterinarians. Philadelphia: WB Saunders1993Hudson LC Hamilton WP: Atlas of Feline Anatomy for Veterinarians. Philadelphia: WB Saunders 1993

  • 15.

    Laszig RSollmann WPMarangos Net al: Nucleus 20-channel and 21-channel auditory brain stem implants: first European experiences. Ann Otol Rhinol Laryngol Suppl 166:28301995Laszig R Sollmann WP Marangos N et al: Nucleus 20-channel and 21-channel auditory brain stem implants: first European experiences. Ann Otol Rhinol Laryngol Suppl 166:28–30 1995

  • 16.

    Liu XMcPhee GSeldon HLet al: Acute study on the efficacy and safety of an auditory brainstem prosthesis. Acta Otolaryngol 118:37451998Liu X McPhee G Seldon HL et al: Acute study on the efficacy and safety of an auditory brainstem prosthesis. Acta Otolaryngol 118:37–45 1998

  • 17.

    Liu XMcPhee GSeldon HLet al: Histological and physiological effects of the central auditory prosthesis: surface versus penetrating electrodes. Hear Res 114:2642741997Liu X McPhee G Seldon HL et al: Histological and physiological effects of the central auditory prosthesis: surface versus penetrating electrodes. Hear Res 114:264–274 1997

  • 18.

    Liu XSeldon HLClark GM: Chronic study on the neuronal excitability of the cochlear nuclei of the cat following electrical stimulation. Acta Otolaryngol 118:5245291998Liu X Seldon HL Clark GM: Chronic study on the neuronal excitability of the cochlear nuclei of the cat following electrical stimulation. Acta Otolaryngol 118:524–529 1998

  • 19.

    Matthies CSamii MThomas Set al: Indication, surgical and monitoring principles and results of auditory brainstem implants in patients with neurofibromatosis-II. Zentralbl Neurochir Suppl:611998 (Abstract)Matthies C Samii M Thomas S et al: Indication surgical and monitoring principles and results of auditory brainstem implants in patients with neurofibromatosis-II. Zentralbl Neurochir Suppl:61 1998 (Abstract)

  • 20.

    McCreery DBShannon RVMoore JKet al: Accessing the tonotopic organization of the ventral cochlear nucleus by intranuclear microstimulation. IEEE Trans Rehabil Eng 6:3913991998McCreery DB Shannon RV Moore JK et al: Accessing the tonotopic organization of the ventral cochlear nucleus by intranuclear microstimulation. IEEE Trans Rehabil Eng 6:391–399 1998

  • 21.

    McCreery DBYuen TGAgnew WFet al: A characterization of the effects on neuronal excitability due to prolonged micro-stimulation with chronically implanted microelectrodes. IEEE Trans Biomed Eng 44:9319391997McCreery DB Yuen TG Agnew WF et al: A characterization of the effects on neuronal excitability due to prolonged micro-stimulation with chronically implanted microelectrodes. IEEE Trans Biomed Eng 44:931–939 1997

  • 22.

    McCreery DBYuen TGAgnew WFet al: Stimulation with chronically implanted microelectrodes in the cochlear nucleus of the cat: histologic and physiologic effects. Hear Res 62:42561992McCreery DB Yuen TG Agnew WF et al: Stimulation with chronically implanted microelectrodes in the cochlear nucleus of the cat: histologic and physiologic effects. Hear Res 62:42–56 1992

  • 23.

    McCreery DBYuen TGAgnew WFet al: Stimulus parameters affecting tissue injury during microstimulation in the cochlear nucleus of the cat. Hear Res 77:1051151994McCreery DB Yuen TG Agnew WF et al: Stimulus parameters affecting tissue injury during microstimulation in the cochlear nucleus of the cat. Hear Res 77:105–115 1994

  • 24.

    McElveen JT JrHitselberger WEHouse WFet al: Electrical stimulation of cochlear nucleus in man. Am J Otol Suppl:88911985McElveen JT Jr Hitselberger WE House WF et al: Electrical stimulation of cochlear nucleus in man. Am J Otol Suppl:88–91 1985

  • 25.

    Moore JK: Cochlear nuclei: relationship to the auditory nerve in Altschuler RAHoffmann DWBobbin RP (eds): Neurobiology of Hearing: The Cochlea. New York: Raven Press1986 pp 283301Moore JK: Cochlear nuclei: relationship to the auditory nerve in Altschuler RA Hoffmann DW Bobbin RP (eds): Neurobiology of Hearing: The Cochlea. New York: Raven Press 1986 pp 283–301

  • 26.

    Moore JK: The human auditory brain stem: a comparative view. Hear Res 29:1321987Moore JK: The human auditory brain stem: a comparative view. Hear Res 29:1–32 1987

  • 27.

    Moore JK: The human auditory brain stem as a generator of auditory evoked potentials. Hear Res 29:33431987Moore JK: The human auditory brain stem as a generator of auditory evoked potentials. Hear Res 29:33–43 1987

  • 28.

    Nguyen BHJavel ELevine SC: Physiologic identification of eighth nerve subdivisions: direct recordings with bipolar and monopolar electrodes. Am J Otol 20:5225341999Nguyen BH Javel E Levine SC: Physiologic identification of eighth nerve subdivisions: direct recordings with bipolar and monopolar electrodes. Am J Otol 20:522–534 1999

  • 29.

    Niparko JKAltschuler RAEvans DAet al: Auditory brainstem prosthesis: biocompatibility of stimulation. Otolaryngol Head Neck Surg 101:3443521989Niparko JK Altschuler RA Evans DA et al: Auditory brainstem prosthesis: biocompatibility of stimulation. Otolaryngol Head Neck Surg 101:344–352 1989

  • 30.

    Niparko JKAltschuler RAXue XLet al: Surgical implantation and biocompatibility of central nervous system auditory prostheses. Ann Otol Rhinol Laryngol 98:9659701989Niparko JK Altschuler RA Xue XL et al: Surgical implantation and biocompatibility of central nervous system auditory prostheses. Ann Otol Rhinol Laryngol 98:965–970 1989

  • 31.

    Otto SRHouse WFBrackmann DEet al: Auditory brain stem implant: effect of tumor size and preoperative hearing level on function. Ann Otol Rhinol Laryngol 99:7897901990Otto SR House WF Brackmann DE et al: Auditory brain stem implant: effect of tumor size and preoperative hearing level on function. Ann Otol Rhinol Laryngol 99:789–790 1990

  • 32.

    Portillo FMobley PMoore Jet al: Feasibility of a central nervous system auditory prosthesis: penetrating microelectrode insertion force studies. Ann Otol Rhinol Laryngol Suppl 166:31331995Portillo F Mobley P Moore J et al: Feasibility of a central nervous system auditory prosthesis: penetrating microelectrode insertion force studies. Ann Otol Rhinol Laryngol Suppl 166:31–33 1995

  • 33.

    Quester RSchroder R: Topographic anatomy of the cochlear nuclear region at the floor of the fourth ventricle in humans. J Neurosurg 91:4664761999Quester R Schroder R: Topographic anatomy of the cochlear nuclear region at the floor of the fourth ventricle in humans. J Neurosurg 91:466–476 1999

  • 34.

    Ranck JB Jr: Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:4174401975Ranck JB Jr: Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440 1975

  • 35.

    Robblee LSMcHardy JAgnew WFet al: Electrical stimulation with Pt electrodes. VII. Dissolution of Pt electrodes during electrical stimulation of the cat cerebral cortex. J Neurosci Methods 9:3013081983Robblee LS McHardy J Agnew WF et al: Electrical stimulation with Pt electrodes. VII. Dissolution of Pt electrodes during electrical stimulation of the cat cerebral cortex. J Neurosci Methods 9:301–308 1983

  • 36.

    Rosahl SKRosahl SWalter GFet al: Cochlear region of the brainstem. J Neurosurg 93:7247272000 (Letter)Rosahl SK Rosahl S Walter GF et al: Cochlear region of the brainstem. J Neurosurg 93:724–727 2000 (Letter)

  • 37.

    Rosahl SKTatagiba MGharabaghi Aet al: Acoustic evoked response following transection of the eighth nerve in the rat. Acta Neurochir 142:103710452000Rosahl SK Tatagiba M Gharabaghi A et al: Acoustic evoked response following transection of the eighth nerve in the rat. Acta Neurochir 142:1037–1045 2000

  • 38.

    Rosahl SKTatagiba MMatthies Cet al: Restitution of auditory function—experimental approaches in Sanna MTaibah ARusso Aet al (eds): Acoustic Neurinoma and Other CPA Tumors. Rome: Monduzzi Editore1999 pp 673677Rosahl SK Tatagiba M Matthies C et al: Restitution of auditory function—experimental approaches in Sanna M Taibah A Russo A et al (eds): Acoustic Neurinoma and Other CPA Tumors. Rome: Monduzzi Editore 1999 pp 673–677

  • 39.

    Rose JEGalambos RHughes JR: Microelectrode studies of the cochlear nuclei of the cat. Johns Hopkins Hosp Bull 104:2112511959Rose JE Galambos R Hughes JR: Microelectrode studies of the cochlear nuclei of the cat. Johns Hopkins Hosp Bull 104:211–251 1959

  • 40.

    Rose JEGalambos RHughes JR: Organization of frequency sensitive neurons in the cochlear nuclear complex of the cat in Rasmussen GLWindle WF (eds): Neural Mechanisms of the Auditory and Vestibular Systems. Springfield, IL: CC Thomas1960 pp 116136Rose JE Galambos R Hughes JR: Organization of frequency sensitive neurons in the cochlear nuclear complex of the cat in Rasmussen GL Windle WF (eds): Neural Mechanisms of the Auditory and Vestibular Systems. Springfield IL: CC Thomas 1960 pp 116–136

  • 41.

    Schrader CRosahl SKovacs Ret al: Histomorphologic evaluation of neural damage caused by electrode carriers in the parietal cortex of the rat. Zentralbl Neurochir Suppl:331999 (Abstract)Schrader C Rosahl S Kovacs R et al: Histomorphologic evaluation of neural damage caused by electrode carriers in the parietal cortex of the rat. Zentralbl Neurochir Suppl:33 1999 (Abstract)

  • 42.

    Shannon RV: Quantitative comparison of electrically and acoustically evoked auditory perception: implications for the location of perceptual mechanisms. Prog Brain Res 97:2612691993Shannon RV: Quantitative comparison of electrically and acoustically evoked auditory perception: implications for the location of perceptual mechanisms. Prog Brain Res 97:261–269 1993

  • 43.

    Shannon RV: Threshold functions for electrical stimulation of the human cochlear nucleus. Hear Res 40:1731771989Shannon RV: Threshold functions for electrical stimulation of the human cochlear nucleus. Hear Res 40:173–177 1989

  • 44.

    Shannon RVFayad JMoore Jet al: Auditory brainstem implant: II. Postsurgical issues and performance. Otolaryngol Head Neck Surg 108:6346421993Shannon RV Fayad J Moore J et al: Auditory brainstem implant: II. Postsurgical issues and performance. Otolaryngol Head Neck Surg 108:634–642 1993

  • 45.

    Shannon RVMoore JKMcCreery DBet al: Threshold-distance measures from electrical stimulation of human brainstem. IEEE Trans Rehabil Eng 5:70741997Shannon RV Moore JK McCreery DB et al: Threshold-distance measures from electrical stimulation of human brainstem. IEEE Trans Rehabil Eng 5:70–74 1997

  • 46.

    Shannon RVOtto SR: Psychophysical measures from electrical stimulation of the human cochlear nucleus. Hear Res 47:1591681990Shannon RV Otto SR: Psychophysical measures from electrical stimulation of the human cochlear nucleus. Hear Res 47:159–168 1990

  • 47.

    Shore SEWiler JAAnderson DJ: Evoked vertex and inferior colliculus responses to electrical stimulation of the cochlear nucleus. Ann Otol Rhinol Laryngol 99:5715761990Shore SE Wiler JA Anderson DJ: Evoked vertex and inferior colliculus responses to electrical stimulation of the cochlear nucleus. Ann Otol Rhinol Laryngol 99:571–576 1990

  • 48.

    Terr LIEdgerton BJ: Surface topography of the cochlear nuclei in humans: two- and three-dimensional analysis. Hear Res 17:51591985Terr LI Edgerton BJ: Surface topography of the cochlear nuclei in humans: two- and three-dimensional analysis. Hear Res 17:51–59 1985

  • 49.

    Terr LIFayad JHitselberger WEet al: Cochlear nucleus anatomy related to central electroauditory prosthesis implantation. Otolaryngol Head Neck Surg 102:7177211990Terr LI Fayad J Hitselberger WE et al: Cochlear nucleus anatomy related to central electroauditory prosthesis implantation. Otolaryngol Head Neck Surg 102:717–721 1990

  • 50.

    Terr LISSinha UKHouse WF: Anatomical relationships of the cochlear nuclei and the pontobulbar body: possible significance for neuroprosthesis placement. Laryngoscope 97:100910111987Terr LIS Sinha UK House WF: Anatomical relationships of the cochlear nuclei and the pontobulbar body: possible significance for neuroprosthesis placement. Laryngoscope 97:1009–1011 1987

  • 51.

    Waring MD: Auditory brain-stem responses evoked by electrical stimulation of the cochlear nucleus in human subjects. Electroencephalogr Clin Neurophysiol 96:3383471995Waring MD: Auditory brain-stem responses evoked by electrical stimulation of the cochlear nucleus in human subjects. Electroencephalogr Clin Neurophysiol 96:338–347 1995

  • 52.

    Waring MD: Refractory properties of auditory brain-stem responses evoked by electrical stimulation of human cochlear nucleus: evidence of neural generators. Electroencephalogr Clin Neurophysiol 108:3313441998Waring MD: Refractory properties of auditory brain-stem responses evoked by electrical stimulation of human cochlear nucleus: evidence of neural generators. Electroencephalogr Clin Neurophysiol 108:331–344 1998

  • 53.

    Yuen TGAgnew WFBullara LAet al: Biocompatibility of electrodes and materials in the central nervous system in Agnew WFMcCreery DB (eds): Neural Prostheses: Fundamental Studies. Englewood Cliffs, NJ: Prentice-Hall1990 pp 198219Yuen TG Agnew WF Bullara LA et al: Biocompatibility of electrodes and materials in the central nervous system in Agnew WF McCreery DB (eds): Neural Prostheses: Fundamental Studies. Englewood Cliffs NJ: Prentice-Hall 1990 pp 198–219

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 50 50 14
Full Text Views 127 127 3
PDF Downloads 58 58 1
EPUB Downloads 0 0 0

PubMed

Google Scholar