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1 < \documentclass[aps,pre,twocolumn,amssymb,showpacs]{revtex4}
2 < %\documentclass[aps,pre,preprint,amssymb,showpacs]{revtex4}
1 > %\documentclass[aps,pre,twocolumn,amssymb,showpacs,floatfix]{revtex4}
2 > \documentclass[aps,pre,preprint,amssymb,showpacs]{revtex4}
3   \usepackage{graphicx}
4  
5   \begin{document}
# Line 26 | Line 26 | stabilized by long-range antiferroelectric ordering.  
26   distorted lattices.  The translational freedom of the dipoles allows
27   triangular lattices to find states that break out of the normal
28   orientational disorder of frustrated configurations and which are
29 < stabilized by long-range antiferroelectric ordering.  In order to
29 > stabilized by long-range anti-ferroelectric ordering.  In order to
30   break out of the frustrated states, the dipolar membranes form
31   corrugated or ``rippled'' phases that make the lattices effectively
32   non-triangular.  We observe three common features of the corrugated
# Line 64 | Line 64 | bilayers are known to form a corrugated or ``rippled''
64  
65   Buckling behavior in liquid crystalline and biological membranes is a
66   well-known phenomenon.  Relatively pure phosphatidylcholine (PC)
67 < bilayers are known to form a corrugated or ``rippled'' phase
68 < ($P_{\beta'}$) which appears as an intermediate phase between the gel
69 < ($L_\beta$) and fluid ($L_{\alpha}$) phases.  The $P_{\beta'}$ phase
70 < has attracted substantial experimental interest over the past 30
71 < years. Most structural information of the ripple phase has been
72 < obtained by the X-ray diffraction~\cite{Sun96,Katsaras00} and
73 < freeze-fracture electron microscopy (FFEM).~\cite{Copeland80,Meyer96}
74 < Recently, Kaasgaard {\it et al.} used atomic force microscopy (AFM) to
75 < observe ripple phase morphology in bilayers supported on
76 < mica.~\cite{Kaasgaard03} The experimental results provide strong
77 < support for a 2-dimensional triangular packing lattice of the lipid
78 < molecules within the ripple phase.  This is a notable change from the
79 < observed lipid packing within the gel phase.~\cite{Cevc87} There have
80 < been a number of theoretical
67 > bilayers form a corrugated or ``rippled'' phase ($P_{\beta'}$) which
68 > appears as an intermediate phase between the gel ($L_\beta$) and fluid
69 > ($L_{\alpha}$) phases.  The $P_{\beta'}$ phase has attracted
70 > substantial experimental interest over the past 30 years. Most
71 > structural information of the ripple phase has been obtained by the
72 > X-ray diffraction~\cite{Sun96,Katsaras00} and freeze-fracture electron
73 > microscopy (FFEM).~\cite{Copeland80,Meyer96} Recently, Kaasgaard {\it
74 > et al.} used atomic force microscopy (AFM) to observe ripple phase
75 > morphology in bilayers supported on mica.~\cite{Kaasgaard03} The
76 > experimental results provide strong support for a 2-dimensional
77 > triangular packing lattice of the lipid molecules within the ripple
78 > phase.  This is a notable change from the observed lipid packing
79 > within the gel phase.~\cite{Cevc87} There have been a number of
80 > theoretical
81   approaches~\cite{Marder84,Goldstein88,McCullough90,Lubensky93,Misbah98,Heimburg00,Kubica02,Bannerjee02}
82   (and some heroic
83   simulations~\cite{Ayton02,Jiang04,Brannigan04a,deVries05,deJoannis06})
# Line 90 | Line 90 | Another interesting properties of elastic membranes co
90   detailed enough to rule in favor of (or against) any of these
91   explanations for the $P_{\beta'}$ phase.
92  
93 < Another interesting properties of elastic membranes containing
94 < electrostatic dipoles is the phenomenon of flexoelectricity,\cite{}
95 < which is the ability of mechanical deformations of the membrane to
96 < result in electrostatic organization of the membrane.  This phenomenon
97 < is a curvature-induced membrane polarization which can lead to
98 < potential differences across a membrane.  Reverse flexoelectric
99 < behavior (in which applied alternating currents affect membrane
100 < curvature) has also been observed.  Explanations of the details of
101 < these effects have typically utilized membrane polarization parallel
102 < to the membrane normal.\cite{}
93 > Membranes containing electrostatic dipoles can also exhibit the
94 > flexoelectric effect,\cite{Todorova2004,Harden2006,Petrov2006} which
95 > is the ability of mechanical deformations to result in electrostatic
96 > organization of the membrane.  This phenomenon is a curvature-induced
97 > membrane polarization which can lead to potential differences across a
98 > membrane.  Reverse flexoelectric behavior (in which applied currents
99 > effect membrane curvature) has also been observed.  Explanations of
100 > the details of these effects have typically utilized membrane
101 > polarization perpendicular to the face of the
102 > membrane,\cite{Petrov2006} and the effect has been observed in both
103 > biological,\cite{Raphael2000} bent-core liquid
104 > crystalline,\cite{Harden2006} and polymer-dispersed liquid crystalline
105 > membranes.\cite{Todorova2004}
106  
107   The problem with using atomistic and even coarse-grained approaches to
108   study membrane buckling phenomena is that only a relatively small
# Line 140 | Line 143 | membranes and in in the $P_{\beta'}$ ripple phase have
143   The point of developing this model was to arrive at the simplest
144   possible theoretical model which could exhibit spontaneous corrugation
145   of a two-dimensional dipolar medium.  Since molecules in polymerized
146 < membranes and in in the $P_{\beta'}$ ripple phase have limited
146 > membranes and in the $P_{\beta'}$ ripple phase have limited
147   translational freedom, we have chosen a lattice to support the dipoles
148   in the x-y plane.  The lattice may be either triangular (lattice
149   constants $a/b =
# Line 163 | Line 166 | r_{ij}-\sigma \right)^2 \right)
166   \label{eq:pot}
167   \end{eqnarray}
168  
166
169   In this potential, $\mathbf{\hat u}_i$ is the unit vector pointing
170   along dipole $i$ and $\mathbf{\hat r}_{ij}$ is the unit vector
171   pointing along the inter-dipole vector $\mathbf{r}_{ij}$.  The entire
# Line 180 | Line 182 | k_r / 2}$).
182   reduced distances, ($r^{*} = r / \sigma$), temperatures ($T^{*} = 2
183   k_B T / k_r \sigma^2$), densities ($\rho^{*} = N \sigma^2 / L_x L_y$),
184   and dipole moments ($\mu^{*} = \mu / \sqrt{4 \pi \epsilon_0 \sigma^5
185 < k_r / 2}$).
185 > k_r / 2}$).  It should be noted that the density ($\rho^{*}$) depends
186 > only on the mean particle spacing in the $x-y$ plane; the lattice is
187 > fully populated.
188  
189   To investigate the phase behavior of this model, we have performed a
190   series of Metropolis Monte Carlo simulations of moderately-sized (34.3
# Line 193 | Line 197 | interaction was set to 4.3 $\sigma$. Since dipole-dipo
197   system sizes were 1360 dipoles for the triangular lattices and
198   840-2800 dipoles for the distorted lattices.  Two-dimensional periodic
199   boundary conditions were used, and the cutoff for the dipole-dipole
200 < interaction was set to 4.3 $\sigma$. Since dipole-dipole interactions
201 < decay rapidly with distance, and since the intrinsic three-dimensional
202 < periodicity of the Ewald sum can give artifacts in 2-d systems, we
203 < have chosen not to use it in these calculations.  Although the Ewald
204 < sum has been reformulated to handle 2-D
205 < systems,\cite{Parry75,Parry76,Heyes77,deLeeuw79,Rhee89} these methods
206 < are computationally expensive,\cite{Spohr97,Yeh99} and are not
200 > interaction was set to 4.3 $\sigma$.  This cutoff is roughly 2.5 times
201 > the typical real-space electrostatic cutoff for molecular systems.
202 > Since dipole-dipole interactions decay rapidly with distance, and
203 > since the intrinsic three-dimensional periodicity of the Ewald sum can
204 > give artifacts in 2-d systems, we have chosen not to use it in these
205 > calculations.  Although the Ewald sum has been reformulated to handle
206 > 2-D systems,\cite{Parry75,Parry76,Heyes77,deLeeuw79,Rhee89} these
207 > methods are computationally expensive,\cite{Spohr97,Yeh99} and are not
208   necessary in this case.  All parameters ($T^{*}$, $\mu^{*}$, and
209   $\gamma$) were varied systematically to study the effects of these
210   parameters on the formation of ripple-like phases.
# Line 225 | Line 230 | the polarization of the perfect antiferroelectric syst
230   for dipole $i$.  $P_2$ will be $1.0$ for a perfectly-ordered system
231   and near $0$ for a randomized system.  Note that this order parameter
232   is {\em not} equal to the polarization of the system.  For example,
233 < the polarization of the perfect antiferroelectric system is $0$, but
234 < $P_2$ for an antiferroelectric system is $1$.  The eigenvector of
233 > the polarization of the perfect anti-ferroelectric system is $0$, but
234 > $P_2$ for an anti-ferroelectric system is $1$.  The eigenvector of
235   $\mathsf{S}$ corresponding to the largest eigenvalue is familiar as
236   the director axis, which can be used to determine a privileged dipolar
237   axis for dipole-ordered systems.  The top panel in Fig. \ref{phase}
# Line 240 | Line 245 | between the dipolar ordered (antiferroelectric) and di
245   a function of temperature for both triangular ($\gamma = 1.732$) and
246   distorted ($\gamma = 1.875$) lattices.  Bottom Panel: The phase
247   diagram for the dipolar membrane model.  The line denotes the division
248 < between the dipolar ordered (antiferroelectric) and disordered phases.
248 > between the dipolar ordered (anti-ferroelectric) and disordered phases.
249   An enlarged view near the triangular lattice is shown inset.}
250   \end{figure}
251  
# Line 251 | Line 256 | ordered phase is antiferroelectric.  We have verified
256   lattice is significantly lower than for the distorted lattices, and
257   the bulk polarization is approximately $0$ for both dipolar ordered
258   and disordered phases.  This gives strong evidence that the dipolar
259 < ordered phase is antiferroelectric.  We have verified that this
259 > ordered phase is anti-ferroelectric.  We have verified that this
260   dipolar ordering transition is not a function of system size by
261   performing identical calculations with systems twice as large.  The
262   transition is equally smooth at all system sizes that were studied.
# Line 261 | Line 266 | This phase diagram is remarkable in that it shows an a
266   shows that the triangular lattice is a low-temperature cusp in the
267   $T^{*}-\gamma$ phase diagram.
268  
269 < This phase diagram is remarkable in that it shows an antiferroelectric
270 < phase near $\gamma=1.732$ where one would expect lattice frustration
271 < to result in disordered phases at all temperatures.  Observations of
272 < the configurations in this phase show clearly that the system has
273 < accomplished dipolar orderering by forming large ripple-like
274 < structures.  We have observed antiferroelectric ordering in all three
275 < of the equivalent directions on the triangular lattice, and the dipoles
276 < have been observed to organize perpendicular to the membrane normal
277 < (in the plane of the membrane).  It is particularly interesting to
278 < note that the ripple-like structures have also been observed to
279 < propagate in the three equivalent directions on the lattice, but the
280 < {\em direction of ripple propagation is always perpendicular to the
281 < dipole director axis}.  A snapshot of a typical antiferroelectric
282 < rippled structure is shown in Fig. \ref{fig:snapshot}.
269 > This phase diagram is remarkable in that it shows an
270 > anti-ferroelectric phase near $\gamma=1.732$ where one would expect
271 > lattice frustration to result in disordered phases at all
272 > temperatures.  Observations of the configurations in this phase show
273 > clearly that the system has accomplished dipolar ordering by forming
274 > large ripple-like structures.  We have observed anti-ferroelectric
275 > ordering in all three of the equivalent directions on the triangular
276 > lattice, and the dipoles have been observed to organize perpendicular
277 > to the membrane normal (in the plane of the membrane).  It is
278 > particularly interesting to note that the ripple-like structures have
279 > also been observed to propagate in the three equivalent directions on
280 > the lattice, but the {\em direction of ripple propagation is always
281 > perpendicular to the dipole director axis}.  A snapshot of a typical
282 > anti-ferroelectric rippled structure is shown in
283 > Fig. \ref{fig:snapshot}.
284  
285   \begin{figure}
286   \includegraphics[width=\linewidth]{snapshot}
287   \caption{\label{fig:snapshot} Top and Side views of a representative
288   configuration for the dipolar ordered phase supported on the
289 < triangular lattice. Note the antiferroelectric ordering and the long
289 > triangular lattice. Note the anti-ferroelectric ordering and the long
290   wavelength buckling of the membrane.  Dipolar ordering has been
291   observed in all three equivalent directions on the triangular lattice,
292   and the ripple direction is always perpendicular to the director axis
# Line 293 | Line 299 | The height-dipole correlation function ($C(r, \cos \th
299   long-wavelength phenomenon, with occasional steep drops between
300   adjacent lines of anti-aligned dipoles.
301  
302 < The height-dipole correlation function ($C(r, \cos \theta)$) makes the
303 < connection between dipolar ordering and the wave vector of the ripple
304 < even more explicit.  $C(r, \cos \theta)$ is an angle-dependent pair
305 < distribution function. The angle ($\theta$) is defined by the
306 < intermolecular vector $\vec{r}_{ij}$ and direction of dipole $i$,
302 > The height-dipole correlation function ($C_{\textrm{hd}}(r, \cos
303 > \theta)$) makes the connection between dipolar ordering and the wave
304 > vector of the ripple even more explicit.  $C_{\textrm{hd}}(r, \cos
305 > \theta)$ is an angle-dependent pair distribution function. The angle
306 > ($\theta$) is the angle between the intermolecular vector
307 > $\vec{r}_{ij}$ and direction of dipole $i$,
308   \begin{equation}
309 < C(r, \cos \theta) = \frac{\langle \sum_{i}
310 < \sum_{j} h_i \cdot h_j \delta(r - r_{ij}) \delta(\cos \theta_{ij} -
309 > C_{\textrm{hd}} = \frac{\langle \frac{1}{n(r)} \sum_{i}\sum_{j>i}
310 > h_i \cdot h_j \delta(r - r_{ij}) \delta(\cos \theta_{ij} -
311   \cos \theta)\rangle} {\langle h^2 \rangle}
312   \end{equation}
313   where $\cos \theta_{ij} = \hat{\mu}_{i} \cdot \hat{r}_{ij}$ and
314 < $\hat{r}_{ij} = \vec{r}_{ij} / r_{ij}$.   Fig. \ref{fig:CrossCorrelation}
315 < shows contours of this correlation function for both anti-ferroelectric, rippled
316 < membranes as well as for the dipole-disordered portion of the phase diagram.  
314 > $\hat{r}_{ij} = \vec{r}_{ij} / r_{ij}$.  $n(r)$ is the number of
315 > dipoles found in a cylindrical shell between $r$ and $r+\delta r$ of
316 > the central particle. Fig. \ref{fig:CrossCorrelation} shows contours
317 > of this correlation function for both anti-ferroelectric, rippled
318 > membranes as well as for the dipole-disordered portion of the phase
319 > diagram.
320  
321   \begin{figure}
322   \includegraphics[width=\linewidth]{hdc}
# Line 323 | Line 333 | intermolecular vectors that are not dipole-aligned.}
333   intermolecular vectors that are not dipole-aligned.}
334   \end{figure}
335  
336 + The height-dipole correlation function gives a map of how the topology
337 + of the membrane surface varies with angular deviation around a given
338 + dipole.  The upper panel of Fig. \ref{fig:CrossCorrelation} shows that
339 + in the anti-ferroelectric phase, the dipole heights are strongly
340 + correlated for dipoles in head-to-tail arrangements, and this
341 + correlation persists for very long distances (up to 15 $\sigma$).  For
342 + portions of the membrane located perpendicular to a given dipole, the
343 + membrane height becomes anti-correlated at distances of 10 $\sigma$.
344 + The correlation function is relatively smooth; there are no steep
345 + jumps or steps, so the stair-like structures in
346 + Fig. \ref{fig:snapshot} are indeed transient and disappear when
347 + averaged over many configurations.  In the dipole-disordered phase,
348 + the height-dipole correlation function is relatively flat (and hovers
349 + near zero).  The only significant height correlations are for axial
350 + dipoles at very short distances ($r \approx
351 + \sigma$).
352 +
353   \subsection{Discriminating Ripples from Thermal Undulations}
354  
355   In order to be sure that the structures we have observed are actually
# Line 391 | Line 418 | not} thermal undulations is obtained from the 2-d four
418   \begin{figure}
419   \includegraphics[width=\linewidth]{logFit}
420   \caption{\label{fig:fit} Evidence that the observed ripples are {\em
421 < not} thermal undulations is obtained from the 2-d fourier transform
421 > not} thermal undulations is obtained from the 2-d Fourier transform
422   $\langle |h^{*}(\vec{q})|^2 \rangle$ of the height profile ($\langle
423   h^{*}(x,y) \rangle$). Rippled samples show low-wavelength peaks that
424   are outliers on the Landau free energy fits by an order of magnitude.
# Line 425 | Line 452 | fourier transform of $h(q_{\mathrm{rip}})$.  Amplitude
452   axis by projecting heights of the dipoles to obtain a one-dimensional
453   height profile, $h(q_{\mathrm{rip}})$. Ripple wavelengths can be
454   estimated from the largest non-thermal low-frequency component in the
455 < fourier transform of $h(q_{\mathrm{rip}})$.  Amplitudes can be
455 > Fourier transform of $h(q_{\mathrm{rip}})$.  Amplitudes can be
456   estimated by measuring peak-to-trough distances in
457   $h(q_{\mathrm{rip}})$ itself.
458  
# Line 465 | Line 492 | surface tension (i.e. by increasing $k_r$ or equivalen
492   \end{figure}
493  
494   The ripples can be made to disappear by increasing the internal
495 < surface tension (i.e. by increasing $k_r$ or equivalently, reducing
495 > elastic tension (i.e. by increasing $k_r$ or equivalently, reducing
496   the dipole moment).  The amplitude of the ripples depends critically
497   on the strength of the dipole moments ($\mu^{*}$) in Eq. \ref{eq:pot}.
498   If the dipoles are weakened substantially (below $\mu^{*}$ = 20) at a
# Line 479 | Line 506 | average nearest-neighbor spacing constant. The antifer
506  
507   We have also investigated the effect of the lattice geometry by
508   changing the ratio of lattice constants ($\gamma$) while keeping the
509 < average nearest-neighbor spacing constant. The antiferroelectric state
509 > average nearest-neighbor spacing constant. The anti-ferroelectric state
510   is accessible for all $\gamma$ values we have used, although the
511   distorted triangular lattices prefer a particular director axis due to
512   the anisotropy of the lattice.
513  
514   Our observation of rippling behavior was not limited to the triangular
515 < lattices.  In distorted lattices the antiferroelectric phase can
515 > lattices.  In distorted lattices the anti-ferroelectric phase can
516   develop nearly instantaneously in the Monte Carlo simulations, and
517   these dipolar-ordered phases tend to be remarkably flat.  Whenever
518   rippling has been observed in these distorted lattices
# Line 541 | Line 568 | form of electrostatic dipoles) and a weak surface tens
568  
569   We have been able to show that a simple dipolar lattice model which
570   contains only molecular packing (from the lattice), anisotropy (in the
571 < form of electrostatic dipoles) and a weak surface tension (in the form
571 > form of electrostatic dipoles) and a weak elastic tension (in the form
572   of a nearest-neighbor harmonic potential) is capable of exhibiting
573   stable long-wavelength non-thermal surface corrugations.  The best
574   explanation for this behavior is that the ability of the dipoles to
575   translate out of the plane of the membrane is enough to break the
576 < symmetry of the triangular lattice and allow the energetic benefit from
577 < the formation of a bulk antiferroelectric phase.  Were the weak
578 < surface tension absent from our model, it would be possible for the
576 > symmetry of the triangular lattice and allow the energetic benefit
577 > from the formation of a bulk anti-ferroelectric phase.  Were the weak
578 > elastic tension absent from our model, it would be possible for the
579   entire lattice to ``tilt'' using $z$-translation.  Tilting the lattice
580   in this way would yield an effectively non-triangular lattice which
581 < would avoid dipolar frustration altogether.  With the surface tension
582 < in place, bulk tilt causes a large strain, and the simplest way to
583 < release this strain is along line defects.  Line defects will result
584 < in rippled or sawtooth patterns in the membrane, and allow small
585 < ``stripes'' of membrane to form antiferroelectric regions that are
586 < tilted relative to the averaged membrane normal.
581 > would avoid dipolar frustration altogether.  With the elastic tension
582 > in place, bulk tilt causes a large strain, and the least costly way to
583 > release this strain is between two rows of anti-aligned dipoles.
584 > These ``breaks'' will result in rippled or sawtooth patterns in the
585 > membrane, and allow small stripes of membrane to form
586 > anti-ferroelectric regions that are tilted relative to the averaged
587 > membrane normal.
588  
589   Although the dipole-dipole interaction is the major driving force for
590   the long range orientational ordered state, the formation of the
591   stable, smooth ripples is a result of the competition between the
592 < surface tension and the dipole-dipole interactions.  This statement is
592 > elastic tension and the dipole-dipole interactions.  This statement is
593   supported by the variation in $\mu^{*}$.  Substantially weaker dipoles
594   relative to the surface tension can cause the corrugated phase to
595   disappear.
# Line 569 | Line 597 | and would not be able to pack in triangular arrangemen
597   The packing of the dipoles into a nearly-triangular lattice is clearly
598   an important piece of the puzzle.  The dipolar head groups of lipid
599   molecules are sterically (as well as electrostatically) anisotropic,
600 < and would not be able to pack in triangular arrangements without the
601 < steric interference of adjacent molecular bodies.  Since we only see
602 < rippled phases in the neighborhood of $\gamma=\sqrt{3}$, this implies
603 < that there is a role played by the lipid chains in the organization of
604 < the triangularly ordered phases which support ripples in realistic
605 < lipid bilayers.
600 > and would not pack in triangular arrangements without the steric
601 > interference of adjacent molecular bodies.  Since we only see rippled
602 > phases in the neighborhood of $\gamma=\sqrt{3}$, this implies that
603 > even if this dipolar mechanism is the correct explanation for the
604 > ripple phase in realistic bilayers, there would still be a role played
605 > by the lipid chains in the in-plane organization of the triangularly
606 > ordered phases which could support ripples.  The present model is
607 > certainly not detailed enough to answer exactly what drives the
608 > formation of the $P_{\beta'}$ phase in real lipids, but suggests some
609 > avenues for further experiments.
610  
611   The most important prediction we can make using the results from this
612   simple model is that if dipolar ordering is driving the surface
# Line 598 | Line 630 | replaced the somewhat artificial lattice packing and t
630   behaviors.  It would clearly be a closer approximation to the reality
631   if we allowed greater translational freedom to the dipoles and
632   replaced the somewhat artificial lattice packing and the harmonic
633 < ``surface tension'' with more realistic molecular modeling
634 < potentials.  What we have done is to present an extremely simple model
635 < which exhibits bulk non-thermal corrugation, and our explanation of
636 < this rippling phenomenon will help us design more accurate molecular
637 < models for corrugated membranes and experiments to test whether
638 < rippling is dipole-driven or not.
633 > elastic tension with more realistic molecular modeling potentials.
634 > What we have done is to present a simple model which exhibits bulk
635 > non-thermal corrugation, and our explanation of this rippling
636 > phenomenon will help us design more accurate molecular models for
637 > corrugated membranes and experiments to test whether rippling is
638 > dipole-driven or not.
639  
640   \begin{acknowledgments}
641   Support for this project was provided by the National Science

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