Swelling of Nerve Fibers Associated with Action Potentials

Iwasa, Kuni H.; Tasaki, Ichiji; Gibbons, Robert C.

doi:10.1126/science.7423196

Cited by 223 publications

(176 citation statements)

References 4 publications

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“…Several different methods were employed and the results were all consistent [43]. Independently, TERAKAWA [69,70] confirmed a part of their results.…”

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confidence: 65%

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Mechanical, thermal, and optical changes of the nerve membrane associated with excitation.

Watanabe

1986

Jpn.J.Physiol

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In this minireview, some of the recent experimental findings on the excitable membranes of nerve fibers obtained by nonelectrophysiological means are discussed. This minireview, however, does not treat the vast literature on the "optical probes of the membrane potential," which is adequately covered by other excellent reviews [14,22,23,30,52].When the nerve fiber is excited, it transiently changes many of its physical properties. From the biological point of view, the most significant is the change in membrane potential, since the transmission of information along the nerve fiber is mediated by the electric local current. Other physical changes are significant mainly because they contain information on the molecular mechanism of the excitation process. They are usually very small for an easy detection, but progress in the techniques of extracting small signals from noise allowed us to discover and examine some of these signals. In this minireview, several recent findings on mechanical, thermal, and optical signals will be discussed.

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“…Several different methods were employed and the results were all consistent [43]. Independently, TERAKAWA [69,70] confirmed a part of their results.…”

supporting

confidence: 65%

“…TASAKI and his collaborators [43] used three different methods to detect the mechanical change. The first was the most simple; the beam of light was partly blocked by a piece of the platinum which was placed on the nerve.…”

Section: A) Methods For Detecting Mechanical Responsementioning

confidence: 99%

Mechanical, thermal, and optical changes of the nerve membrane associated with excitation.

Watanabe

1986

Jpn.J.Physiol

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“…Cell swelling has also been reported to occur during normal neuronal activity, but with a negligible amplitude that is much smaller than that caused by prolonged and strong depolarization (44,56,(65)(66)(67)(68). In general, the displacements of the cell surface are on the length scale of nanometers, with a maximum displacement of several tens of nanometers, under normal electrical stimulation (65)(66)(67)(68).…”

Section: Discussionmentioning

confidence: 96%

“…In general, the displacements of the cell surface are on the length scale of nanometers, with a maximum displacement of several tens of nanometers, under normal electrical stimulation (65)(66)(67)(68). However, the surface displacement changes in the neuronal soma induced by prolonged depolarization can be ≥∼1 μm (44,56,57).…”

Section: Discussionmentioning

confidence: 99%

Assessing the sensitivity of diffusion MRI to detect neuronal activity directly

Bai

Stewart

Plenz

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Functional MRI (fMRI) is widely used to study brain function in the neurosciences. Unfortunately, conventional fMRI only indirectly assesses neuronal activity via hemodynamic coupling. Diffusion fMRI was proposed as a more direct and accurate fMRI method to detect neuronal activity, yet confirmative findings have proven difficult to obtain. Given that the underlying relation between tissue water diffusion changes and neuronal activity remains unclear, the rationale for using diffusion MRI to monitor neuronal activity has yet to be clearly established. Here, we studied the correlation between water diffusion and neuronal activity in vitro by simultaneous calcium fluorescence imaging and diffusion MR acquisition. We used organotypic cortical cultures from rat brains as a biological model system, in which spontaneous neuronal activity robustly emerges free of hemodynamic and other artifacts. Simultaneous fluorescent calcium images of neuronal activity are then directly correlated with diffusion MR signals now free of confounds typically encountered in vivo. Although a simultaneous increase of diffusion-weighted MR signals was observed together with the prolonged depolarization of neurons induced by pharmacological manipulations (in which cell swelling was demonstrated to play an important role), no evidence was found that diffusion MR signals directly correlate with normal spontaneous neuronal activity. These results suggest that, whereas current diffusion MR methods could monitor pathological conditions such as hyperexcitability, e.g., those seen in epilepsy, they do not appear to be sensitive or specific enough to detect or follow normal neuronal activity.D eveloping a direct MRI method to detect neuronal activity in vivo and noninvasively is a major focus in neuroscience. Progress in this area is required to improve our understanding of normal brain function, and in a clinical setting, to develop new tools for studying normal and abnormal development to diagnose diseases and disorders of the brain. Functional MRI (fMRI) has been widely used in the cognitive neurosciences since its invention in the 1990s (1-3). The most widely used fMRI method, blood-oxygenation-level-dependent (BOLD) MRI, detects hemodynamic changes in the brain, which only indirectly reflects neuronal activity. Moreover, its hemodynamic origin limits both its spatial and temporal resolution and its interpretation as a direct proxy for neuronal activity (4, 5).More recently, several MRI methods were proposed to provide more direct measures of neuronal excitation (6). In particular, diffusion MRI, a method to measure the apparent diffusivity of water within tissues (7-9), has been suggested as a direct functional imaging method to detect neuronal activity (10-13). Early in vivo experiments in both humans and animals reported small but significant increases in highly diffusion-weighted MRI signals, which were ascribed to changes directly induced by the underlying neuronal activity rather than indirect hemodynamic changes (10-13).In vitro experimen...

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“…Related insights may also help guide our understanding of other emerging neurophysical modalities like magnetogenetic stimulation (whose biophysics is still poorly understood [49,50]). For example, we note that membrane mechanoelectrical effects involving dimensional changes were suggested in other contexts involving changes in intramembranal forces, including action potential-related intramembrane thickness variations [51][52][53] and ultrasoundinduced formation of intramembrane cavities (or "bilayer sonophores" [54]). The neuronal intramembrane cavitation excitation theoretical framework putatively explains ultrasonic neuromodulation phenomena (suppression and excitation [55]) and predicts the results of a significant number of related experimental studies [56,57].…”

Section: Discussionmentioning

confidence: 99%

Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects

et al. 2018

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Modern advances in neurotechnology rely on effectively harnessing physical tools and insights towards remote neural control, thereby creating major new scientific and therapeutic opportunities. Specifically, rapid temperature pulses were shown to increase membrane capacitance, causing capacitive currents that explain neural excitation, but the underlying biophysics is not well understood. Here, we show that an intramembrane thermal-mechanical effect wherein the phospholipid bilayer undergoes axial narrowing and lateral expansion accurately predicts a potentially universal thermal capacitance increase rate of ∼0.3%=°C. This capacitance increase and concurrent changes in the surface charge related fields lead to predictable exciting ionic displacement currents. The new MechanoElectrical Thermal Activation theory's predictions provide an excellent agreement with multiple experimental results and indirect estimates of latent biophysical quantities. Our results further highlight the role of electro-mechanics in neural excitation; they may also help illuminate subthreshold and novel physical cellular effects, and could potentially lead to advanced new methods for neural control.

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Swelling of Nerve Fibers Associated with Action Potentials

Cited by 223 publications

References 4 publications

Mechanical, thermal, and optical changes of the nerve membrane associated with excitation.

Mechanical, thermal, and optical changes of the nerve membrane associated with excitation.

Assessing the sensitivity of diffusion MRI to detect neuronal activity directly

Thermal Transients Excite Neurons through Universal Intramembrane Mechanoelectrical Effects

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