Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System

Nowadays, the majority of the progress in the development of implantable neuroprostheses has been achieved by improving the knowledge of brain functions so as to restore sensorial impairments. Intracortical microstimulation (ICMS) is a widely used technique to investigate site-specific cortical resp...

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Main Authors: Maria Giovanna Bianco, Salvatore Andrea Pullano, Rita Citraro, Emilio Russo, Giovambattista De Sarro, Etienne de Villers Sidani, Antonino S. Fiorillo
Format: Article
Language:English
Published: MDPI AG 2020-03-01
Series:Bioengineering
Subjects:
Online Access:https://www.mdpi.com/2306-5354/7/1/23
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author Maria Giovanna Bianco
Salvatore Andrea Pullano
Rita Citraro
Emilio Russo
Giovambattista De Sarro
Etienne de Villers Sidani
Antonino S. Fiorillo
author_facet Maria Giovanna Bianco
Salvatore Andrea Pullano
Rita Citraro
Emilio Russo
Giovambattista De Sarro
Etienne de Villers Sidani
Antonino S. Fiorillo
author_sort Maria Giovanna Bianco
collection DOAJ
description Nowadays, the majority of the progress in the development of implantable neuroprostheses has been achieved by improving the knowledge of brain functions so as to restore sensorial impairments. Intracortical microstimulation (ICMS) is a widely used technique to investigate site-specific cortical responses to electrical stimuli. Herein, we investigated the neural modulation induced in the primary auditory cortex (A1) by an acousto-electric transduction of ultrasonic signals using a bio-inspired intracortical microstimulator. The developed electronic system emulates the transduction of ultrasound signals in the cochlea, providing bio-inspired electrical stimuli. Firstly, we identified the receptive fields in the primary auditory cortex devoted to encoding ultrasonic waves at different frequencies, mapping each area with neurophysiological patterns. Subsequently, the activity elicited by bio-inspired ICMS in the previously identified areas, bypassing the sense organ, was investigated. The observed evoked response by microstimulation resulted as highly specific to the stimuli, and the spatiotemporal dynamics of neural oscillatory activity in the alpha, beta, and gamma waves were related to the stimuli preferred by the neurons at the stimulated site. The alpha waves modulated cortical excitability only during the activation of the specific tonotopic neuronal populations, inhibiting neural responses in unrelated areas. Greater neuronal activity in the posterior area of A1 was observed in the beta band, whereas a gamma rhythm was induced in the anterior A1. The results evidence that the proposed bio-inspired acousto-electric ICMS triggers high-frequency oscillations, encoding information about the stimulation sites and involving a large-scale integration in the brain.
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spelling doaj.art-16ef24a471f84322b6ad92b51ddcd0472023-09-02T01:29:44ZengMDPI AGBioengineering2306-53542020-03-01712310.3390/bioengineering7010023bioengineering7010023Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic SystemMaria Giovanna Bianco0Salvatore Andrea Pullano1Rita Citraro2Emilio Russo3Giovambattista De Sarro4Etienne de Villers Sidani5Antonino S. Fiorillo6Department of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyDepartment of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyDepartment of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyDepartment of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyDepartment of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyMontreal Neurological Institute, McGill University, Montreal, QC H3A 2B4, CanadaDepartment of Health Sciences, Magna Græcia University of Catanzaro, 88100 Catanzaro, ItalyNowadays, the majority of the progress in the development of implantable neuroprostheses has been achieved by improving the knowledge of brain functions so as to restore sensorial impairments. Intracortical microstimulation (ICMS) is a widely used technique to investigate site-specific cortical responses to electrical stimuli. Herein, we investigated the neural modulation induced in the primary auditory cortex (A1) by an acousto-electric transduction of ultrasonic signals using a bio-inspired intracortical microstimulator. The developed electronic system emulates the transduction of ultrasound signals in the cochlea, providing bio-inspired electrical stimuli. Firstly, we identified the receptive fields in the primary auditory cortex devoted to encoding ultrasonic waves at different frequencies, mapping each area with neurophysiological patterns. Subsequently, the activity elicited by bio-inspired ICMS in the previously identified areas, bypassing the sense organ, was investigated. The observed evoked response by microstimulation resulted as highly specific to the stimuli, and the spatiotemporal dynamics of neural oscillatory activity in the alpha, beta, and gamma waves were related to the stimuli preferred by the neurons at the stimulated site. The alpha waves modulated cortical excitability only during the activation of the specific tonotopic neuronal populations, inhibiting neural responses in unrelated areas. Greater neuronal activity in the posterior area of A1 was observed in the beta band, whereas a gamma rhythm was induced in the anterior A1. The results evidence that the proposed bio-inspired acousto-electric ICMS triggers high-frequency oscillations, encoding information about the stimulation sites and involving a large-scale integration in the brain.https://www.mdpi.com/2306-5354/7/1/23sensor systempiezoelectric transducersecog recordingneuromodulationneuroprosthetics
spellingShingle Maria Giovanna Bianco
Salvatore Andrea Pullano
Rita Citraro
Emilio Russo
Giovambattista De Sarro
Etienne de Villers Sidani
Antonino S. Fiorillo
Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
Bioengineering
sensor system
piezoelectric transducers
ecog recording
neuromodulation
neuroprosthetics
title Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
title_full Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
title_fullStr Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
title_full_unstemmed Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
title_short Neural Modulation of the Primary Auditory Cortex by Intracortical Microstimulation with a Bio-Inspired Electronic System
title_sort neural modulation of the primary auditory cortex by intracortical microstimulation with a bio inspired electronic system
topic sensor system
piezoelectric transducers
ecog recording
neuromodulation
neuroprosthetics
url https://www.mdpi.com/2306-5354/7/1/23
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