Abstract:Cochlear implant (CI) recipients with preserved acoustic low-frequency hearing in the implanted ear are a growing group among traditional CI users who benefit from hybrid electric-acoustic stimulation (EAS). However, combined ipsilateral electric and acoustic stimulation also introduces interactions between the two modalities that can affect the performance of EAS users. A computational model of a single auditory nerve fiber that is excited by EAS was developed to study the interaction between electric and aco… Show more
“…These terms can also be re-arranged to estimate the contribution of spontaneous APs and pulse-induced APs to F separately (See Methods). Prior work by our group and others has attempted to capture these interactions using simplifying equations 26,28 , but those attempts do not provide a complete description of the effects observed in our simulation described below.…”
Section: Resultsmentioning
confidence: 99%
“…Our simulations show a number of effects of pulsatile stimulation on axon channel dynamics that can prevent other pulses from producing APs and override spontaneous activity. The resulting PFRs resemble pulse effects demonstrated across neural systems: high-frequency facilitation (row 1) has been observed in auditory nerve fibers 27,30 ; the PPB effect that leads to a bend in PFR (row 2) has been observed auditory nerve fibers 25 and dorsal column axons 22,27,30 ; high amplitude block is observed in the sciatic nerve (row 3) 31 ; amplitude-dependent growth of firing rates has been observed in the auditory nerve 32 ; experiments on hippocampal neurons 33 , auditory fibers 28 and spinal cord proprioceptive fibers 21 demonstrate pulse-spontaneous additive and blocking effects (Fig. 4a).…”
Electrical stimulation of neural responses is used both scientifically in brain mapping studies and in many clinical applications such as cochlear, vestibular, and retinal implants. Due to safety considerations, stimulation of the nervous system is restricted to short biphasic pulses. Despite decades of research and development, neural implants are far from optimal in their ability to restore function and lead to varying improvements in patients. In this study, we provide an explanation for how pulsatile stimulation affects individual neurons and therefore leads to variability in restoration of neural responses. The explanation is grounded in the physiological response of channels in the axon and represented with mathematical rules that predict firing rate as a function of pulse rate, pulse amplitude, and spontaneous activity. We validate these rules by showing that they predict recorded vestibular afferent responses in macaques and discuss their implications for designing clinical stimulation paradigms and electrical stimulation-based experiments.
“…These terms can also be re-arranged to estimate the contribution of spontaneous APs and pulse-induced APs to F separately (See Methods). Prior work by our group and others has attempted to capture these interactions using simplifying equations 26,28 , but those attempts do not provide a complete description of the effects observed in our simulation described below.…”
Section: Resultsmentioning
confidence: 99%
“…Our simulations show a number of effects of pulsatile stimulation on axon channel dynamics that can prevent other pulses from producing APs and override spontaneous activity. The resulting PFRs resemble pulse effects demonstrated across neural systems: high-frequency facilitation (row 1) has been observed in auditory nerve fibers 27,30 ; the PPB effect that leads to a bend in PFR (row 2) has been observed auditory nerve fibers 25 and dorsal column axons 22,27,30 ; high amplitude block is observed in the sciatic nerve (row 3) 31 ; amplitude-dependent growth of firing rates has been observed in the auditory nerve 32 ; experiments on hippocampal neurons 33 , auditory fibers 28 and spinal cord proprioceptive fibers 21 demonstrate pulse-spontaneous additive and blocking effects (Fig. 4a).…”
Electrical stimulation of neural responses is used both scientifically in brain mapping studies and in many clinical applications such as cochlear, vestibular, and retinal implants. Due to safety considerations, stimulation of the nervous system is restricted to short biphasic pulses. Despite decades of research and development, neural implants are far from optimal in their ability to restore function and lead to varying improvements in patients. In this study, we provide an explanation for how pulsatile stimulation affects individual neurons and therefore leads to variability in restoration of neural responses. The explanation is grounded in the physiological response of channels in the axon and represented with mathematical rules that predict firing rate as a function of pulse rate, pulse amplitude, and spontaneous activity. We validate these rules by showing that they predict recorded vestibular afferent responses in macaques and discuss their implications for designing clinical stimulation paradigms and electrical stimulation-based experiments.
“…In terms of neurostimulation, most computational work has focused on the mechanisms underlying DBS of the basal ganglia for motor disorders such as Parkinson's disease (Rubin and Terman, 2004;Pirini et al, 2009;Mina et al, 2013;Ebert et al, 2014), peripheral nerve stimulation (Rattay et al, 2003;Kipping and Nogueira, 2022), spinal cord stimulation (Rattay et al, 2000;Capogrosso et al, 2013), or has remained generic (Basu et al, 2018). However, models investigating neurostimulation of hippocampal circuits are scarce (Hendrickson et al, 2016;Bingham et al, 2018), and do not take into account the effects on theta-gamma oscillations.…”
Neurostimulation of the hippocampal formation has shown promising results for modulating memory but the underlying mechanisms remain unclear. In particular, the effects on hippocampal theta-nested gamma oscillations and theta phase reset, which are both crucial for memory processes, are unknown. Moreover, these effects cannot be investigated using current computational models, which consider theta oscillations with a fixed amplitude and phase velocity. Here, we developed a novel computational model that includes the medial septum, represented as a set of abstract Kuramoto oscillators producing a dynamical theta rhythm with phase reset, and the hippocampal formation, composed of biophysically-realistic neurons and able to generate theta-nested gamma oscillations under theta drive. We showed that this system can exhibit bistability in a specific range of parameters and that a single stimulation pulse could switch the network behavior from non-oscillatory to a state producing theta-nested gamma oscillations. Next, we demonstrated that for a theta input too weak to generate theta-nested gamma oscillations, pulse train stimulation at the theta frequency could restore seemingly physiological oscillations. Importantly, the presence of phase reset influenced whether these two effects depended on the phase at which stimulation onset was delivered, which has practical implications for designing neurostimulation protocols that are triggered by the phase of ongoing theta oscillations. This novel model opens new avenues for studying the effects of neurostimulation on the hippocampal formation. Furthermore, our hybrid approach that combines different levels of abstraction could be extended in future work to other neural circuits that produce dynamical brain rhythms.
“…In terms of neurostimulation, most computational work has focused on the mechanisms under-lying DBS of the basal ganglia for motor disorders such as Parkinson’s disease ( Rubin and Terman, 2004 ; Pirini et al, 2009 ; Mina et al, 2013 ; Ebert et al, 2014 ), peripheral nerve stimulation ( Rattay et al, 2003 ; Kipping and Nogueira, 2022 ), spinal cord stimulation ( Rattay et al, 2000 ; Capogrosso et al, 2013 ), or has remained generic ( Basu et al, 2018 ). However, models investigating neurostimulation of hippocampal circuits are scarce ( Hendrickson et al, 2016 ; Bingham et al, 2018 ), and do not take into account the effects on theta-gamma oscillations.…”
Neurostimulation of the hippocampal formation has shown promising results for modulating memory but the underlying mechanisms remain unclear. In particular, the effects on hippocampal theta-nested gamma oscillations and theta phase reset, which are both crucial for memory processes, are unknown. Moreover, these effects cannot be investigated using current computational models, which consider theta oscillations with a fixed amplitude and phase velocity. Here, we developed a novel computational model that includes the medial septum, represented as a set of abstract Kuramoto oscillators producing a dynamical theta rhythm with phase reset, and the hippocampal formation, composed of biophysically-realistic neurons and able to generate theta-nested gamma oscillations under theta drive. We showed that this system can exhibit bistability in a specific range of parameters and that a single stimulation pulse could switch the network behavior from non-oscillatory to a state producing theta-nested gamma oscillations. Next, we demonstrated that for a theta input too weak to generate theta-nested gamma oscillations, pulse train stimulation at the theta frequency could restore seemingly physiological oscillations. Importantly, the presence of phase reset influenced whether these two effects depended on the phase at which stimulation onset was delivered, which has practical implications for designing neurostimulation protocols that are triggered by the phase of ongoing theta oscillations. This novel model opens new avenues for studying the effects of neurostimulation on the hippocampal formation. Furthermore, our hybrid approach that combines different levels of abstraction could be extended in future work to other neural circuits that produce dynamical brain rhythms.
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