Impact of Nanosecond Pulsed Electric Fields on
Primary Hippocampal Neurons
Caleb C. Roth
1
, Jason A. Payne
2
, Marjorie A. Kuipers
2
, Gary L. Thompson
3
, Gerald J. Wilmink
2
,
Bennett L. Ibey
2
1
General Dynamics Information Technology, Fort Sam Houston, TX, USA
2
Radio Frequency Bioeffects Branch, Human Effectiveness Directorate, Air Force Research
Laboratory, Fort Sam Houston TX, USA
3
National Research Council, Fort Sam Houston, TX USA
ABSTRACT
Cellular exposure to nanosecond pulsed electric fields (nsPEF) are believed to cause immediate creation of
nanopores in the plasma membrane. These nanopores enable passage of small ions, but remain impermeable to
larger molecules like propidium iodide. Previous work has shown that nanopores are stable for minutes after
exposure, suggesting that formation of nanopores in excitable cells could lead to prolonged action potential
inhibition. Previously, we measured the formation of nanopores in neuroblastoma cells by measuring the influx of
extracellular calcium by preloading cells with Calcium Green-AM. In this work, we explored the impact of changing
the width of a single nsPEF, at constant amplitude, on uptake of extracellular calcium ions by primary hippocampal
neurons (PHN). Calcium Green was again used to measure the influx of extracellular calcium and FM1-43 was used
to monitor changes in membrane conformation. The observed thresholds for nanopore formation in PHN by nsPEF
were comparable to those measured in neuroblastoma. This work is the first study of nsPEF effects on PHN and
strongly suggests that neurological inhibition by nanosecond electrical pulses is highly likely at doses well below
irreversible damage.
Keywords: Nanopores, nanosecond electrical pulses, membrane damage, primary hippocampal neurons, calcium
green, FM1-43
1. INTRODUCTION
Nanosecond pulsed electric fields (nsPEF) are high voltage square wave pulses with duration (τ) under 1 µs.
Originally engineered for plasma formation, various biological applications of nsPEF are being pursued including
electromuscular incapacitation, cancer therapy, gene transfection, and pain suppression.
1-7
When applied directly to
mammalian cells, multifarious effects have been observed including nuclear granulation, cellular swelling, bleb
formation, and apoptosis.
1,2
Recent studies have shown that when nsPEF are applied directly to cells small pores,
termed nanopores, are preferentially formed in the plasma membrane.
8
In contrast to classical electroporation, these
nanopores are believed to have a diameter of only a few nanometers and therefore do not readily allow large
molecules such as propidium iodide to enter the cell.
8,9
Therefore, unlike longer duration pulses, nsPEF enable the
manipulation of cellular function without a high degree of mortality. Further distinguishing nsPEF induced-
nanopores, many unique properties have been identified using a variety of techniques including patch clamp,
fluorescent microscopy, direct ion measurement in bulk solution, and flow cytometry.
10,11,12
Specifically, the
direction of ion flow appears predominantly inward, they open and close regularly at a slower rate than protein ion
channels, and they have a lifetime at room temperature over many minutes.
8
Interestingly, nsPEFs may provide a unique technique for controlling the activity of neurons within deep tissue by
causing either stimulation (at low dose) or inhibition (at high dose). Previous work by Rogers has shown that low
voltage nsPEFs can trigger action potentials (AP) leading to contractions in isolated frog muscle.
13
It was believed
that nsPEF can cause AP generation by activating the release of acetylcholine into the synaptic cleft.
6
Jiang and
Cooper demonstrated that a single, 12 ns pulse at 403 V/cm was capable of activating skin nociceptors. They
demonstrated this same effect at 100 pulses delivered at 4000 Hz with very low voltages (16.7 V/cm) without any
Photonic Therapeutics and Diagnostics VIII, edited by Nikiforos Kollias, et al., Proc. of SPIE Vol. 8207, 820763
© 2012 SPIE · CCC code: 1605-7422/12/$18 · doi: 10.1117/12.911802
Proc. of SPIE Vol. 8207 820763-1
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