On Combining the Dielectrophoresis and Microdevices

Investigation of Hippocampal Neuronal Viability after Implementing

Dielectrophoretic Positioning on Multi-Electrode Arrays

Tianyi Zhou

, Susan F. Perry

2,3

and Svetlana Tatic-Lucic

1,3

Department of Electrical and Computer Engineering, Lehigh University, Bethlehem, PA 18015, U.S.A.

Department of Chemical Engineering, Lehigh University, Bethlehem, PA 18015, U.S.A.

Bioengineering Program, Lehigh University, Bethlehem, PA 18015, U.S.A.

Keywords: Viability, Hippocampal Neurons, Multi-Electrode Array (MEA), Dielectrophoresis (DEP), Sucrose,

Membrane Potential.

Abstract: In this work, we have investigated the viability of embryonic mouse hippocampal neurons after

dielectrophoretic positioning on multi-electrode arrays (MEA). We present a systematic evaluation of

positive dielectrophoretic conditions, including 1) an investigation of the effect of 10% sucrose (w/v in

deionized water), a commonly used, low-conductivity buffer medium, on the viability of mouse

hippocampal neurons over different time periods, and 2) a study of the effect of the membrane potential

induced by DEP electric field on the integrity of the cell membrane. Post-DEP high neuronal viability was

achieved experimentally, and spontaneous neuronal potentials from trapped neurons on the MEA were

successfully recorded.

1 INTRODUCTION

Microsystems based on dielectrophoresis (DEP),

being flexible and label-free, have been widely used

to position, separate, and characterize particles and

biological cells (Gagnon, 2011; Li et al., 2014;

Pethig, 2010). For instance, various types of cells,

such as rat hippocampal neurons (Honegger et al.,

2013) and human liver cells and endothelial cells

(Ho et al., 2013) have been successfully manipulated

and patterned by DEP, while circulating tumor cells

(CTC) have been isolated from blood cells using

microdevices integrating DEP and microfluidics

(Gupta et al., 2012). Likewise, neuronal stem cells,

neurons and glial cells have been characterized and

separated with DEP microsystems (Prieto et al.,

2012).

On the other hand, extracellular multi-electrode

arrays (MEAs) have provided reliable platforms for

neuronal potential recording because of their non-

invasive nature (Berdondini et al., 2009; Hochberg

et al., 2006; Spira and Hai, 2013). These MEAs

facilitate the study of neuronal physiology and

communication through simultaneous in vitro

recordings and stimulations from multiple neurons.

By increasing the number of electrodes,

conventional MEAs have been widely used for

tissue-level or high-density neural culture and

recording (Berdondini et al., 2009; Stevenson and

Kording, 2011; Viventi et al., 2011).

Incorporating DEP on MEAs, as demonstrated

by the work of Jaber et al., 2009, Rozitsky et al.,

2013, and Yoshimura et al., 2014, enables a

microsystem to efficiently position individual

neurons on single electrodes, as well as to precisely

track and investigate electric signals from specific

individual neurons. According to Pohl 1978, the

polarization of a dielectric particle (e.g. a neuron),

when exposed to a non-uniform electric field, drives

the cell towards the maximum or minimum of

electric field, depending on the relative dielectric

and conductive properties of the cell and the

suspension medium. Positive dielectrophoresis

(pDEP) actively traps cells to the electrodes

(maximum of electric field), while negative

dielectrophoresis (nDEP) pushes cells away from

these areas.

In order to pattern neurons with positive

dielectrophoresis (pDEP), neurons have to survive

the implementation of pDEP, which attracts them to

the electrodes. Two factors influence the viability of

Zhou T., Perry S. and Tatic-Lucic S..

On Combining the Dielectrophoresis and Microdevices - Investigation of Hippocampal Neuronal Viability after Implementing Dielectrophoretic Positioning

on Multi-Electrode Arrays.

DOI: 10.5220/0005180200710077

In Proceedings of the International Conference on Biomedical Electronics and Devices (BIODEVICES-2015), pages 71-77

ISBN: 978-989-758-071-0

 2015 SCITEPRESS (Science and Technology Publications, Lda.)

neurons during the application of pDEP: 1) the DEP

cell-trapping solution, because its low conductivity,

which is desirable for trapping (pDEP is not possible

in high conductivity, standard culture media), is not

optimal for cell survival, and 2) electric field. The

viability of a few types of neural cells, such as

neural cortical cells and neural stem/progenitor cells

(NSPCs), in DEP manipulation was investigated

previously (Heida et al., 2001; Lu et al., 2012), and

high cell viability was achieved for short-term (1

min or less) DEP exposure. In this work, we

systematically evaluate the long-term (up to 12

hours) viability of embryonic mouse hippocampal

neurons after being actively positioned on the

electrodes of a custom-made MEA using

dielectrophoresis.

2 MATERIALS AND METHODS

2.1 Experimental Setup for the Study

of the Hippocampal Viability in

Sucrose

In order for pDEP to take effect, the polarization of

neurons should be stronger than that of surrounding

media (Jones, 1995), which requires a low-

conductivity environment. As a commonly used,

low-conductivity buffer medium, sucrose solution is

often used as the primary component of a pDEP

trapping solution (Huang et al., 2014; Pethig, 2010;

Vahey and Voldman, 2009). In our experiments, a

30% cell media DEP suspension medium, which is a

mixture of seven parts of 10% sucrose(w/v in

deionized water) and three parts of primary neuron

culture media, NbActiv1 (BrainBits, LLC.), is used

for neuronal pDEP recruiting on MEA. This

sucrose/cell media mixture, with a measured

conductivity of 0.331 S/m, has low conductivity and

appropriate physiological osmolarity for neurons to

survive (Jeng et al., 2010) during pDEP trapping.

While cell culture media does not compromise

the health of neurons, the viability of embryonic

mouse hippocampal neurons, in 10% sucrose, which

is the major component of the cell-trapping solution,

was investigated. Dissociated hippocampal cells

were resuspended in three sterile 15 mL centrifuge

tubes, each containing 5 mL 10% sucrose (w/v in

deionized water), and in another centrifuge tube of 5

mL cell media NbActiv1 as a control group. The

three sucrose samples were placed at room

temperature (RT) for 30, 60 and 90 min respectively,

and the control tube was placed at RT for 90 min.

After each associated time period, 5 mL of

phosphate buffered saline (PBS) was added to each

of the sucrose tubes, and the samples were

centrifuged at 200g for 5 min to harvest the cells.

We found the dilution with PBS, above, necessary

for pelleting the cells, because otherwise cells

remained suspended in the high-viscosity sucrose

solution, even after being centrifuged. The viability

of harvested cells was assessed through use of

Live/Dead

cell stain, (Invitrogen; Calcein, AM

2M and Ethdium Homodimer, 1M in cell media

NbActiv1). After 15 min in dark at RT, the cell

suspension was transferred to a 35 mm petri dish

using a micropipette, and five live/dead fluorescent

micrographs were taken at random positions, for

each sample, including the control group. Percent

cell viability was calculated based on the average of

five images. Typically, 30-40 cells were counted on

each of the image.

2.2 Simulation and Modeling of the

Effect of MEA Electric Field on

Hippocampal Viability

Membrane breakdown, or electroporation, is the

process where a biological cell membrane is turned

into a high-conductivity state because of a

membrane potential induced by an external electric

field (Heida et al., 2002). This process comes with

the creation of pores on the membrane. When

induced membrane potential exceeds the threshold

level, expansion of membrane pores or creation of

more pores leads to membrane breakdown, which

can be a fatal effect while trying to attract

hippocampal neurons to electrodes using pDEP.

According to Zimmermann and Neil, 1996, in an

AC electric field E, the generated membrane

potential is given by:







1.5



12



(1)

with  the static electric field, r the cell radius, α the

angle between the electric field line and a vector

from the cell center to an associated point on the

membrane, f the electric field frequency, and τ the

time constant of cell membrane expressed as (Heida

et al., 2002):













2





(2)

where 



is the effective cell membrane capacitance

per unit area, and 



and 



are the conductivities of

cell interior (cytoplasm) and surrounding medium,

respectively.

BIODEVICES2015-InternationalConferenceonBiomedicalElectronicsandDevices

From equation (1), the induced membrane

potential is frequency-dependent. Furthermore, the

maximum potential is at the membrane point facing

an electrode (assuming the cell sitting on top of a

planar electrode), where the electric field line is

parallel to the vector from cell center to the

membrane point, giving =1 or =-1. The

manipulation of cells using DEP requires a non-

uniform global electric field, as mentioned above.

However, if the local electric field is assumed to be

uniform and static (constant  ), the induced

membrane potential can be calculated based on the

protoplast (single-shell) model of a mammalian cell

(Jones, 1995; Zhou and Tatic-Lucic, 2012). In this

model, the mammalian cell is represented by a

homogeneous cell interior (cytoplasm) with ohmic

conductivity 



, and a thin capacitive cell membrane

layer with effective capacitance 



2.3 Post-DEP Hippocampal Viability

Verification

The viability of pDEP recruited hippocampal

neurons on the MEA was verified, using the same

Live/Dead

cell stain, as described above. Primary

neuron culture media NbActiv1, which was the

media neurons incubated in after the DEP

positioning, was replaced carefully by the live/dead

stain with a micropipette. The sample was placed in

dark at RT for 15 min, and visualized immediately

with a Nikon ECLIPSE E800 upright fluorescent

microscope.

3 RESULTS AND DISCUSSION

3.1 Hippocampal Viability in Sucrose

The main objective of our study was to evaluate the

effect of the cell-trapping solution on the viability of

embryonic mouse hippocampal cells. Cells were

exposed to 10% sucrose for various periods of time

(30, 60 and 90 min) and their viability analyzed, as

previously described in Section 2.1. Since the cell

media component of the trapping solution does not

compromise the health of cells, their viability was

investigated in a more severe (10% sucrose, only)

situation.

As shown in Figure 1, all three sucrose treatment

samples had acceptable hippocampal viability

compared to the control group (cell media); the

parameter that should be kept in mind is that the

entire pDEP trapping process normally lasts for less

than 30 min, thus, that is the duration of exposure to

cell trapping solution that has relevance for most of

the experimental setups. The viability decreases

slightly from 88±2% to 78±3%, as time in sucrose

increases (up to 90 min), but the detrimental effect

on cell survival is limited, confirming the feasibility

of using 10% sucrose as the major component of the

cell-trapping solution. In Figure 1, the error bars

represent the standard deviations of data from five

randomly-taken images.

Figure 1: Hippocampal viability assessment after sucrose

treatments for various periods of time.

3.2 Neuronal Membrane Potential

Simulations on MEA

Another facet of this viability study is the

investigation of the induced cell membrane potential

resulting from non-uniform DEP electric field,

which, if it exceeds certain threshold value, could

compromise neuronal health; this threshold value is

known as the breakdown potential (Heida et al.,

2002; Huang et al., 2014). Detailed simulations

were performed to ensure cell membrane integrity

with the application of a 6 Vpp, 10 MHz AC signal.

This signal was selected based on our prior studies

on the DEP parameters that secure the attraction of

neurons, only, on the electrodes, as opposed to glial

cells which are also present in the cell medium

(Zhou et al., 2014).

In order to explore the intricacies of pDEP

attraction of cells on electrodes, DEP electric field

simulation was performed with CoventorWare

(Coventor, Inc.) finite element analysis (FEA)

software (Zhou and Tatic-Lucic, 2012). A simplified

one-electrode model based on targeted device

structure was built (see Figure 2(a)). In this model, a

single electrode is sandwiched between glass

substrate and silicon oxide passivation layer, and a

via is etched through the passivation layer to open

and define the electrode site. SU-8 epoxy is patterned

OnCombiningtheDielectrophoresisandMicrodevices-InvestigationofHippocampalNeuronalViabilityafter

ImplementingDielectrophoreticPositioningonMulti-ElectrodeArrays

above the passivation layer, where different

microstructures, including microchambers and

microtrenches, are created using photolithography. In

the electrostatic simulation, +3V potential was

applied to the electrode. The simulated electric field

distribution is shown in Figure 2(b). It can be seen

that the electric field maximum area is located above

the open via, as the central red peak extending above

the surface indicates. This means the cell will be

attracted to the open via on top of the electrode when

pDEP is implemented (Zhou and Tatic-Lucic, 2012).

(a)

(b)

Figure 2: (a) FEA model of DEP MEA electrode structure.

(b) Simulated electric field distribution using Coventor.

From this electrode finite element analysis

modeling, 2-D electric field data on four different

planes of interest was extracted, as shown in Figure

3. These four planes are representative surfaces

where hippocampal neurons experience induced

membrane potential during pDEP anchoring. The

first plane (Z1) is the surface of the silicon oxide

passivation layer; the second plane (Z2) is the level

of the neuron’s center when the neuron lands on the

silicon oxide layer; the third plane (Z3) is the surface

of the SU-8 layer; and the last plane (Z4) is at the

level of the center of the neuron when the neuron is

positioned on top of the SU-8 layer. Z1 and Z2 are

established when the cell has been trapped on an

electrode; Z3 and Z4 represent the cell floating on

device surface just before anchored to the electrode

by DEP. The position and distance between each

plane are based on dimensions obtained from a

fabricated DEP MEA and from the measured radii of

hippocampal neurons (r= 4 m).

Figure 3: Four planes (Z1-Z4) where electric field data

was extracted and induced neuron membrane potential

was calculated.

As mentioned earlier, the simulated maximum

electric field is above the electrode, which is also the

center point of each 2-D plane extracted. Using this

electric field maxima and related hippocampal

neuronal dielectric properties (Chitwood et al., 1999;

Gentet et al., 2000; Heida et al., 2001; Major et al.,

1994), the frequency dependence of maximum

(=1) induced membrane potential 



on four

planes was calculated in Matlab (MathWorks, Inc.).

In Figure 4, two graphs indicate the situation where

the voltages of 3 V and 4 V were applied to the

electrode, respectively.

As can be seen in Figure 4, the induced

membrane potential is greater on lower planes

(greater electric field strength); nevertheless, the

potential on each plane decreases as frequency

increases. With different electrode configurations

and DEP conditions, Huang et al., 2014 and

LaLonde et al., 2014 reported similar results. It was

reported that an induced membrane potential below

0.4 V can probably guarantee the survival of cortical

neurons, and larger membrane potentials can be

tolerated by cortical cells at higher frequencies

(Heida et al., 2001; Heida et al., 2002). Assuming

0.4 V is also the membrane breakdown threshold for

hippocampal neurons, the membrane potentials are

BIODEVICES2015-InternationalConferenceonBiomedicalElectronicsandDevices

Figure 4: Calculated hippocampal membrane potentials induced by external electric field when (a) 3 V and (b) 4 V is

applied on the bottom electrode. Two close-up views for potentials on Z1 at 10 MHz are provided, compared with the 0.4 V

threshold.

all below this level at 10 MHz when 3 V is applied,

as indicated by the close-up view in Figure 4(a).

However, the potential is still above 0.4 V on plane

Z1 if 4 V is applied at 10 MHz, which could lead to

cell death when the neuron is anchored on top of the

electrode. For this reason, 6 Vpp (-3 V to 3 V), 10

MHz AC signal was used for hippocampal neuronal

recruiting on the MEA.

It should be mentioned, however, that this

membrane potential is not the only factor impacting

the viability of hippocampal neurons. For instance,

some neurons may have already died during the

dissociation process, even before they are exposed to

the electric field (Heida et al., 2001). Therefore,

approaches to simultaneously track the change of

neuronal membrane potential and verify the

membrane breakdown-associated cell death are in

need, as such necrosis directly relates to external

electric field during pDEP implementation.

3.3 Hippocampal Viability Verification

and Neuronal Potential Recording

The next step in our work was to experimentally

verify the viability of the neurons that were attracted

to MEA electrodes and positioned there by pDEP.

We used the DEP AC signal of 6 Vpp and 10 MHz,

and implemented live/dead staining process to

determine whether neurons survived the recruiting

procedure. Live/dead staining, which requires media

change and manual manipulation, as described in

Section 2.3, was not possible immediately following

the application of pDEP, because newly placed cells

were easily displaced. Therefore, staining was

performed 12 hours post-pDEP, for neurons to better

attach on the electrode. As can be seen in Figure 5,

after 12 hours in vitro, pDEP positioned

hippocampal neurons on MEA have better than 96%

viability (96±2%, n = 7), verifying the integrity of

the cell membrane and that neurons stayed alive in

the cell-trapping solution during pDEP positioning.

Figure 5: Live (green)/dead (red) stain of hippocampal

neurons positioned on MEA at 12 h in vitro. Viability

better than 96% was achieved.

At the same time (12 hours in vitro), spontaneous

neuronal potential was successfully detected from

neurons anchored on the MEA. In Figure 6, a

spontaneous neuronal extracellular potential spike

was recorded from electrode 11, as indicated in

Figure 5; the spontaneous neuronal spike has an

amplitude around 100 V, which is a reasonable

value according to Buzsaki et al. 2012. With the

recording of spontaneous neuronal potential, the

electrically active properties of pDEP positioned

OnCombiningtheDielectrophoresisandMicrodevices-InvestigationofHippocampalNeuronalViabilityafter

ImplementingDielectrophoreticPositioningonMulti-ElectrodeArrays

neurons on the MEA was further verified.

Figure 6: A spontaneous neuronal spike recorded from

electrode 11 in Figure 5.

4 CONCLUSIONS

Dielectrophoresis is used, with increasing frequency,

in combination with microdevices, to manipulate

biological cells. However, it is important to

understand the impact the implementation of DEP

may have on the viability of cells. In this work we

have investigated the viability of mouse

hippocampal neurons positioned on the electrodes of

microfabricated multi-electrode arrays after the

implementation of pDEP. We showed that neurons

maintained high viability after short-term exposure

to cell-trapping solution, which contained, primarily,

10% sucrose. With electric signal of appropriate

frequency and amplitude (such as 6Vpp and 10MHz),

neuron membrane breakdown was prevented during

the DEP process. Most importantly, we have

obtained electrical signals from the neurons

positioned on the MEA, 12 hours after using positive

dielectrophoresis, further confirming the health and

electrically active properties of neurons.

ACKNOWLEDGEMENTS

This work was partially funded by National Science

Foundation (NSF) grant NSF ECCS-1321356 and a

grant to Lehigh University from the Howard Hughes

Medical Institute (HHMI) through the Precollege

and Undergraduate Science Education Program.

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OnCombiningtheDielectrophoresisandMicrodevices-InvestigationofHippocampalNeuronalViabilityafter

ImplementingDielectrophoreticPositioningonMulti-ElectrodeArrays