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Virtual Journal for Biomedical Optics

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  • Editor: Gregory W. Faris
  • Vol. 5, Iss. 7 — Apr. 26, 2010
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Inversion of gradient forces for high refractive index particles in optical trapping

L. A. Ambrosio and H. E. Hernández-Figueroa  »View Author Affiliations


Optics Express, Vol. 18, Issue 6, pp. 5802-5808 (2010)
http://dx.doi.org/10.1364/OE.18.005802


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Abstract

The unexpected fact that a spherical dielectric particle with refractive index higher than the surrounding medium will not always be attracted towards high intensity regions of the trapping beam is fully demonstrated here using a simple ray optics approach. This unusual situation may happen due to the inversion of gradient forces, as shown here. Therefore, conventional schemes, such the one based on the use of two counter-propagating beams to cancel the scattering forces, will fail to trap the particle. However, effective trapping still can be obtained by adopting suitable incident laser beams.

© 2010 OSA

1. Introduction

Experiments on optical trapping using one single beam were only carried out in the middle 80’s, providing efficient full tridimensional trapping [1

1. A. Ashkin, J. M. Dziedzic, J. E. Bjorkholm, and S. Chu, “Observation of a single-beam gradient force optical trap for dielectric particles,” Opt. Lett. 11(5), 288–290 (1986). [CrossRef] [PubMed]

]. Since then, optical tweezers have found enormous applications in medical and biological researches [2

2. A. Ashkin and J. M. Dziedzic, “Optical trapping and manipulation of viruses and bacteria,” Science 235(4795), 1517–1520 (1987). [CrossRef] [PubMed]

5

5. V. Emiliani, D. Cojoc, E. Ferrari, V. Garbin, C. Durieux, M. Coppey-Moisan, and E. Di Fabrizio, “Wave front engineering for microscopy of living cells,” Opt. Express 13(5), 1395–1405 (2005). [CrossRef] [PubMed]

].

It is widely expected that dielectric particles with refractive index np higher than that of the surrounding medium (nm), be directed towards regions of high intensity of the impinging laser beam, due to the exerted gradient and scattering total forces. The contrary would happen if the particle had a refractive index lower than that of the medium. In this case, it would be repelled from these high intensity regions.

The explanation is based on momentum transfer from the incident photons to the particle, as illustrated in Fig. 1(a)
Fig. 1 (a). Ray optics analysis showing an incident ray R1 and its first two refracted rays R2 and R3. Looking at the momentum transfer without considering the infinite series of refracted/reflected rays which appears as a consequence of R1 leads to an erroneous interpretation and to the conclusion that the particle would experience a force directed to the high intensity region, i.e., to the centre of the beam. (b). the complete picture taking into account the infinite series of refracted/reflected rays.
. Considering the incident ray and only the first two refracted rays and using conservation of the momentum, it is quite straightforward to show that the particle will always be attracted into high intensity regions of the beam.

This truncated ray optics picture is, however, not completely correct. In fact, a sequence of infinite rays emerges from the particle after it is impinged by the incident ray, and the power of each of these rays is strongly dependent upon the relative refractive index nrel between the particle and the surrounding medium (from Fresnel’s reflectivity and transmittivity coefficients), as can be appreciated in Fig. 1(b) for an incident ray with power P.

Although Ashkin confirms that scattering forces prevail over gradient forces for this situation [6

6. A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992). [CrossRef] [PubMed]

] and subsequent works have found ways of trapping and manipulating these particles using two counter-propagating beams [7

7. S. B. Smith, Y. Cui, and C. Bustamante, “Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules,” Science 271(5250), 795–799 (1996). [CrossRef] [PubMed]

10

10. P. J. Rodrigo, V. R. Daria, and J. Glückstad, “Real-time three-dimensional optical micromanipulation of multiple particles and living cells,” Opt. Lett. 29(19), 2270–2272 (2004). [CrossRef] [PubMed]

], here it is numerically demonstrated that even those clever apparatus [7

7. S. B. Smith, Y. Cui, and C. Bustamante, “Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules,” Science 271(5250), 795–799 (1996). [CrossRef] [PubMed]

10

10. P. J. Rodrigo, V. R. Daria, and J. Glückstad, “Real-time three-dimensional optical micromanipulation of multiple particles and living cells,” Opt. Lett. 29(19), 2270–2272 (2004). [CrossRef] [PubMed]

] are unable to provide a fully tridimensional trap for particles with nrel >> 1 because gradient forces can also become repulsive.

Let us start by analyzing a single incident ray to have an insight into the problem, then we will generalize the phenomenon for an incident Gaussian beam with wavelength λ much smaller than the dimensions of the particle, thus satisfying the ray optics requirements. Results are immediate and intuitive. A final example is provided for a Bessel beam, demonstrating that these multi-ringed shaped beams are well suited alternatives for trappings where nrel >> 1.

The final conclusion is that optical trapping using one single beam and even counter-propagating beams for nrel >> 1 are of limited use, and other experimental schemes or different kinds of laser beams may be necessary to be adopted.

2. Theoretical analysis – single ray incidence

Different from Fig. 1(a), the complete situation for an incident ray is depicted in Fig. 1(b), where the infinite series of reflected/refracted rays can be appreciated for np > nm. Scattering and gradient forces (parallel and perpendicular to the ray, respectively) FS and Fg are given by the known expressions [6

6. A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992). [CrossRef] [PubMed]

]:
FS=nmcPnmPRccos(π+2θi)l=0nmPcT2Rlcos(α+lβ)=nmPc{1+Rcos2θiT2[cos(2θi2θt)+Rcos2θi]1+R2+2Rcos2θt}=nmPcQS,
(1)
Fg=nmPRcsin(π+2θi)l=0nmPcT2Rlsin(α+lβ)=nmPc{Rsin2θiT2[sin(2θi2θt)+Rsin2θi]1+R2+2Rcos2θt}=nmPcQg,
(2)
where P is the power of the incident ray, R and T are the Fresnel coefficients of reflection and transmission, respectively, c is the speed of light, θi the incident angle, α = 2θi – 2θt and β = π – 2θt, θt being the transmission angle. The summation in (1) and (2) reflects the multiple rays transmitted through the particle and is essential to the correctness of the theory.

Using Fig. 1(a) for explaining the optical trapping of a particle is equivalent to take l’s upper limit as 0 in the above equations and to reject the first reflected ray given by the cos(π + 2θi) and sin(π + 2θi) terms for FS and Fg, respectively, meaning that we are approximating the real situation.

Maybe one reason for using this approximation to explain the capabilities of optical tweezers in trapping biological particles is that most of these have refractive indices close to the surrounding medium. Thus, for a medium with nm = 1.33, typical of experiments, R is satisfactorily low for highly focused beams with a numerical aperture less than 66°. But as nrel increases, R increases as well, as can be appreciated in Fig. 2
Fig. 2 Reflectivity for nm = 1.33 and np = 1.6, 2.4, 3.2 and 4.0 for (a) perpendicular polarization and (b) parallel polarization. If the laser is designed for case (b), then the incident rays can be chosen so that only the contribution of those with incidence angles close to regions of low reflectivity are relevant.
. If R increases significantly, the first reflected ray carrying a power PR will dominate over all the other rays that emerge from the particle (multiple transmitted rays) with associate powers PT2, PT2R and so on, all included in (1) and (2) by the summation over l. This happens because T = 1- R tends to zero.

Notice that, even if the scattering force could dominate over the gradient one for high refractive index, making optical trapping difficult to be achieved, here we find an inversion of the gradient force, that is, even if scattering forces could hypothetically be canceled, gradient forces become repulsive. Therefore, the statement that particles, having a refractive index higher than the medium, would be attracted to the optical axis of the beam is not always true, not only because of the well-known longitudinal pushing, but also because of this repulsive force perpendicular to the ray. So, Fig. 1(a) must be used cautiously when explaining the behavior of a particle in an optical tweezers system.

Still for a single ray, Fig. 3
Fig. 3 (a) Gradient Force (normalized over nmP/c) for a single ray and its dependence on both incident angle and refractive index. (b) The equivalent contour plot, emphasizing the gradient zero-force line. As the refractive index increases, Fg becomes positive, i.e., repulsive, indicating the trapping impossibility.
shows the gradient force as a function of the incidence angle θi and np. It is clear that, according to the coordinate system in Fig. 1(b), when np increases, the gradient forces become positive in y, i.e., repulsive. Here, we suppose a circularly polarized ray, i.e., we use both R and T for perpendicular and parallel polarizations, taking the mean average in (2). It can be easily checked that, as nrel (e.g., np for fixed nm) → ∞, QS2cos2θi and Qgsin2θi, i.e., there is a limit for the maximum force exerted by each ray and, consequently, for any designed beam or trapping setup in the ray optics regime. However, in this high nrel case, all forces are purely repulsive.

3. Theoretical analysis – beam incidence

Total forces for a Gaussian beam can be calculated as described elsewhere [6

6. A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992). [CrossRef] [PubMed]

]. For a circularly polarized TEM00 Gaussian beam with a numerical aperture of 66°, typical of the microscopes used in experimental setups, gradient and scattering total forces (considered here as the components of the total force vector, perpendicular and parallel to the optical axis of the beam, respectively) as functions of the distance r between the focus of the beam and the centre of the spherical particle for geometrical optics is shown in Fig. 4
Fig. 4 Gradient (a) and scattering (b) total forces for a circularly polarized TEM00 Gaussian beam as functions of the distance r between the centre of the particle and the beam focus when both are on a horizontal plane perpendicular to the optical axis of the beam. The attractive/repulsive pattern depends on the value of the refractive index np for a fixed nm.
for several values of np (nm fixed). The optical axis of the beam is taken along the vertical + z coordinate with both focus and centre of the particle in a horizontal plane. The efficiency of optical trapping is significantly reduced as np increases. A particle of radius a = 10λ, λ = 1064 nm, is assumed.

This does not means that high nrel particles cannot be trapped; rather, it confirms the need for new experimental setups like the two counter propagating laser beams, or dual-beam trap, recently tested [9

9. A. van der Horst, P. D. J. van Oostrum, A. Moroz, A. van Blaaderen, and M. Dogterom, “High trapping forces for high-refractive index particles trapped in dynamic arrays of counterpropagating optical tweezers,” Appl. Opt. 47(17), 3196 (2008). [CrossRef] [PubMed]

]. Notice, however, that even those arrangements are inadequate for the case of np = 6.4 in Fig. 4, because this circularly polarized beam would repeal the particle perpendicularly to the optical axis.

Referring to Fig. 5(a)
Fig. 5 (a). Coordinate system for total force numerical calculations. (b) Scattering factor QS and (c) gradient factor Qg as functions of the angle γ between the optical axis of the beam and the vector connecting its focus to the centre of the particle. Higher repulsive scattering total forces are seen as np increases, whereas the gradient total forces become repulsive.
, suppose that the impinging Gaussian beam propagates along -z and has a focus on the origin of the y-z plane. Any incident ray hits the spherical dielectric particle of vector radius a at some distance d from the focus with an incident angle θi. The angle between the z axis and the vector r which connects the focus and the center of the particle is denoted by γ. Total forces can be found by numerically summing up all individual gradient and scattering forces of each ray of the beam (see Ref [11

11. L. A. Ambrosio and H. E. Hernández-Figueroa, “Trapping double negative particles in the ray optics regime using optical tweezers with focused beams,” Opt. Express 17(24), 21918–21924 (2009). [CrossRef] [PubMed]

]. for further details).

A full analysis for a fixed distance between the center of the particle and the beam focus is provided based on the coordinate system of Fig. 5(a) for r = 0.5a and γ ranging from 0° to 360°. Results for scattering total forces are depicted in Fig. 5(b) for the same values of np as used before. These forces increase significantly over the equivalent gradient total forces in Fig. 5(c).

Notice that, for the chosen spherical particles and according to the convention of Fig. 5(a), the only trappable particle for a single beam would be the one with np = 1.6, as FS becomes attractive (positive) towards the focus in the range 100° < γ < 260°, i.e., quite below the plane perpendicular to the optical axis and that crosses the focus.

There are, however, efficient ways of trapping high refractive index particles. Easy laser trapping could be achieved simply by replacing the counter propagating Gaussian beams by multi-ringed shaped beams, like Bessel beams. As the scattering forces are cancelled, gradient forces are enhanced, and several high refractive index particles could be efficiently trapped in the regions of low intensity profiles of these beams. Figure 6
Fig. 6 Gradient total forces profile for a particle in a zero-order Bessel beam with λ = 1064 nm and a spot of 28.89 μm. The particle has a radius of a = 10.64 μm. For np = 8.0, points at r/a = 2.8 and 6.3 become points of stable equilibrium, and the use of two counter propagating Bessel beams present themselves as excellent alternatives for trapping these high refractive index particles.
illustrates the gradient total force profile for a particle with a = 10λ, λ = 1064 nm, as the distance r changes, for a zero-order Bessel beam with a spot of 28.89 μm, which is equivalent to an axicon angle of 0.0141 rad. In order to calculate the gradient total force, we again summed up all incident rays assuming that all of them are parallel to the optical axis of the beam and differing among them only in its carried power, P.

For this beam – and for a Bessel beam of any order – the radial repulsion from high intensity regions of the beam does not exclude trapping because the particle would tend to move to the low intensity zones, where it is eventually captured (in the case of Fig. 6, for example, at approximate distances 28 μm (r/a = 2,8) and 67 μm (r/a = 6.3) for np = 8.0, which are points of stable equilibrium).

It is difficult to find anything organic or biological having a refractive index higher than 3 [12

12. W. Poon, School of Physics & Astronomy, University of Edinburgh, Edinburgh, EH9 3JZ, UK (personal communication, 2009).

], although at least one biological complex found in fungi presents an interesting behavior: when attempting to trap it using an optical tweezers, it is naturally repelled, even though its refractive index is higher than the surrounding medium, as confirmed by phase-contrast microscopy, where it appears as a phase-dark object [13

13. G. D. Wright, J. Arlt, W. C. K. Poon, and N. D. Read, “Experimentally manipulating fungi with optical tweezers,” Mycoscience 48(1), 15 (2007). [CrossRef]

,14

14. D. R. Burnham, G. D. Wright, N. D. Read, and D. McGloin, “Holographic and single beam optical manipulation of hyphal growth in filamentous fungi,” J. Opt. A, Pure Appl. Opt. 9(8), S172–S179 (2007). [CrossRef]

]. This complex, called Spitzenkörper, seems to be important in fungi growth, but no refractive index has been assigned to it yet [15

15. N. D. Read, Fungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Rutherford Building, Edinburgh EH9 3JH, UK (personal communication, 2009).

]. We may speculate that following [13

13. G. D. Wright, J. Arlt, W. C. K. Poon, and N. D. Read, “Experimentally manipulating fungi with optical tweezers,” Mycoscience 48(1), 15 (2007). [CrossRef]

,16

16. C. G. Reynaga-Peña and S. Bartnicki-García, “Cytoplasmic contractions in growing fungal hyphae and their morphogenetic consequences,” Arch. Microbiol. 183(4), 292–300 (2005). [CrossRef] [PubMed]

,17

17. A. Virag and S. D. Harris, “The Spitzenkörper: a molecular perspective,” Mycol. Res. 110(1), 4–13 (2006). [CrossRef]

] (λ ~785 nm and dimensions of the complex of the order of one micron), this complex could behave as an inhomogeneous particle having an overall effective refractive index much higher than expected, then being pushed away. Of course, other hypothesis may offer more plausible or effective explanations for this phenomenon.

All simulations in this paper were performed for spherical particles in the ray optics regime, and the limiting value between attractive/repulsive gradient forces can significantly change, for a given external medium, depending on the internal structure and the geometry of the particle and the ratio between its radius and the wavelength, i.e., the optical regime.

4. Conclusions

High refractive index particles request schemes of trapping different from the ones available in the literature. Even one single or two counter propagating Gaussian beams based on the strategy of scattering forces cancellation may not be capable of manipulating these particles because of the presence of repulsive gradient forces. Therefore, for nrel >> 1, alternative experimental setups should be realized, as the use of two anti-parallel multi-ringed shaped Bessel beams, for instance.

Acknowledgements

This work was supported by FAPESP – Fundação de Amparo à Pesquisa e ao Ensino do Estado de São Paulo, under contract 2005/51689-2 (CePOF, Optics and Photonics Research Center), and by CNPq – Conselho Nacional de Desenvolvimento Científico e Tecnológico, under contract 151090/2009-2.

References

1.

A. Ashkin, J. M. Dziedzic, J. E. Bjorkholm, and S. Chu, “Observation of a single-beam gradient force optical trap for dielectric particles,” Opt. Lett. 11(5), 288–290 (1986). [CrossRef] [PubMed]

2.

A. Ashkin and J. M. Dziedzic, “Optical trapping and manipulation of viruses and bacteria,” Science 235(4795), 1517–1520 (1987). [CrossRef] [PubMed]

3.

R. W. Steubing, S. Cheng, W. H. Wright, Y. Numajiri, and M. W. Berns, “Laser induced cell fusion in combination with optical tweezers: the laser cell fusion trap,” Cytometry 12(6), 505–510 (1991). [CrossRef] [PubMed]

4.

M. W. Berns, W. H. Wright, B. J. Tromberg, G. A. Profeta, J. J. Andrews, and R. J. Walter, “Use of a laser-induced optical force trap to study chromosome movement on the mitotic spindle,” Proc. Natl. Acad. Sci. U.S.A. 86(12), 4539–4543 (1989). [CrossRef] [PubMed]

5.

V. Emiliani, D. Cojoc, E. Ferrari, V. Garbin, C. Durieux, M. Coppey-Moisan, and E. Di Fabrizio, “Wave front engineering for microscopy of living cells,” Opt. Express 13(5), 1395–1405 (2005). [CrossRef] [PubMed]

6.

A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992). [CrossRef] [PubMed]

7.

S. B. Smith, Y. Cui, and C. Bustamante, “Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules,” Science 271(5250), 795–799 (1996). [CrossRef] [PubMed]

8.

W. Wang, A. E. Chiou, G. J. Sonek, and M. W. Berns, “Self-aligned dual-beam optical laser trap using photo-refractive phase conjugation,” J. Opt. Soc. Am. B 14(4), 697–704 (1997). [CrossRef]

9.

A. van der Horst, P. D. J. van Oostrum, A. Moroz, A. van Blaaderen, and M. Dogterom, “High trapping forces for high-refractive index particles trapped in dynamic arrays of counterpropagating optical tweezers,” Appl. Opt. 47(17), 3196 (2008). [CrossRef] [PubMed]

10.

P. J. Rodrigo, V. R. Daria, and J. Glückstad, “Real-time three-dimensional optical micromanipulation of multiple particles and living cells,” Opt. Lett. 29(19), 2270–2272 (2004). [CrossRef] [PubMed]

11.

L. A. Ambrosio and H. E. Hernández-Figueroa, “Trapping double negative particles in the ray optics regime using optical tweezers with focused beams,” Opt. Express 17(24), 21918–21924 (2009). [CrossRef] [PubMed]

12.

W. Poon, School of Physics & Astronomy, University of Edinburgh, Edinburgh, EH9 3JZ, UK (personal communication, 2009).

13.

G. D. Wright, J. Arlt, W. C. K. Poon, and N. D. Read, “Experimentally manipulating fungi with optical tweezers,” Mycoscience 48(1), 15 (2007). [CrossRef]

14.

D. R. Burnham, G. D. Wright, N. D. Read, and D. McGloin, “Holographic and single beam optical manipulation of hyphal growth in filamentous fungi,” J. Opt. A, Pure Appl. Opt. 9(8), S172–S179 (2007). [CrossRef]

15.

N. D. Read, Fungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Rutherford Building, Edinburgh EH9 3JH, UK (personal communication, 2009).

16.

C. G. Reynaga-Peña and S. Bartnicki-García, “Cytoplasmic contractions in growing fungal hyphae and their morphogenetic consequences,” Arch. Microbiol. 183(4), 292–300 (2005). [CrossRef] [PubMed]

17.

A. Virag and S. D. Harris, “The Spitzenkörper: a molecular perspective,” Mycol. Res. 110(1), 4–13 (2006). [CrossRef]

OCIS Codes
(080.0080) Geometric optics : Geometric optics
(170.4520) Medical optics and biotechnology : Optical confinement and manipulation
(350.4855) Other areas of optics : Optical tweezers or optical manipulation

ToC Category:
Optical Trapping and Manipulation

History
Original Manuscript: October 30, 2009
Revised Manuscript: January 4, 2010
Manuscript Accepted: March 1, 2010
Published: March 9, 2010

Virtual Issues
Vol. 5, Iss. 7 Virtual Journal for Biomedical Optics

Citation
L. A. Ambrosio and H. E. Hernández-Figueroa, "Inversion of gradient forces for high refractive index particles in optical trapping," Opt. Express 18, 5802-5808 (2010)
http://www.opticsinfobase.org/vjbo/abstract.cfm?URI=oe-18-6-5802


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References

  1. A. Ashkin, J. M. Dziedzic, J. E. Bjorkholm, and S. Chu, “Observation of a single-beam gradient force optical trap for dielectric particles,” Opt. Lett. 11(5), 288–290 (1986). [CrossRef] [PubMed]
  2. A. Ashkin and J. M. Dziedzic, “Optical trapping and manipulation of viruses and bacteria,” Science 235(4795), 1517–1520 (1987). [CrossRef] [PubMed]
  3. R. W. Steubing, S. Cheng, W. H. Wright, Y. Numajiri, and M. W. Berns, “Laser induced cell fusion in combination with optical tweezers: the laser cell fusion trap,” Cytometry 12(6), 505–510 (1991). [CrossRef] [PubMed]
  4. M. W. Berns, W. H. Wright, B. J. Tromberg, G. A. Profeta, J. J. Andrews, and R. J. Walter, “Use of a laser-induced optical force trap to study chromosome movement on the mitotic spindle,” Proc. Natl. Acad. Sci. U.S.A. 86(12), 4539–4543 (1989). [CrossRef] [PubMed]
  5. V. Emiliani, D. Cojoc, E. Ferrari, V. Garbin, C. Durieux, M. Coppey-Moisan, and E. Di Fabrizio, “Wave front engineering for microscopy of living cells,” Opt. Express 13(5), 1395–1405 (2005). [CrossRef] [PubMed]
  6. A. Ashkin, “Forces of a single-beam gradient laser trap on a dielectric sphere in the ray optics regime,” Biophys. J. 61(2), 569–582 (1992). [CrossRef] [PubMed]
  7. S. B. Smith, Y. Cui, and C. Bustamante, “Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules,” Science 271(5250), 795–799 (1996). [CrossRef] [PubMed]
  8. W. Wang, A. E. Chiou, G. J. Sonek, and M. W. Berns, “Self-aligned dual-beam optical laser trap using photo-refractive phase conjugation,” J. Opt. Soc. Am. B 14(4), 697–704 (1997). [CrossRef]
  9. A. van der Horst, P. D. J. van Oostrum, A. Moroz, A. van Blaaderen, and M. Dogterom, “High trapping forces for high-refractive index particles trapped in dynamic arrays of counterpropagating optical tweezers,” Appl. Opt. 47(17), 3196 (2008). [CrossRef] [PubMed]
  10. P. J. Rodrigo, V. R. Daria, and J. Glückstad, “Real-time three-dimensional optical micromanipulation of multiple particles and living cells,” Opt. Lett. 29(19), 2270–2272 (2004). [CrossRef] [PubMed]
  11. L. A. Ambrosio and H. E. Hernández-Figueroa, “Trapping double negative particles in the ray optics regime using optical tweezers with focused beams,” Opt. Express 17(24), 21918–21924 (2009). [CrossRef] [PubMed]
  12. W. Poon, School of Physics & Astronomy, University of Edinburgh, Edinburgh, EH9 3JZ, UK (personal communication, 2009).
  13. G. D. Wright, J. Arlt, W. C. K. Poon, and N. D. Read, “Experimentally manipulating fungi with optical tweezers,” Mycoscience 48(1), 15 (2007). [CrossRef]
  14. D. R. Burnham, G. D. Wright, N. D. Read, and D. McGloin, “Holographic and single beam optical manipulation of hyphal growth in filamentous fungi,” J. Opt. A, Pure Appl. Opt. 9(8), S172–S179 (2007). [CrossRef]
  15. N. D. Read, Fungal Cell Biology Group, Institute of Cell Biology, University of Edinburgh, Rutherford Building, Edinburgh EH9 3JH, UK (personal communication, 2009).
  16. C. G. Reynaga-Peña and S. Bartnicki-García, “Cytoplasmic contractions in growing fungal hyphae and their morphogenetic consequences,” Arch. Microbiol. 183(4), 292–300 (2005). [CrossRef] [PubMed]
  17. A. Virag and S. D. Harris, “The Spitzenkörper: a molecular perspective,” Mycol. Res. 110(1), 4–13 (2006). [CrossRef]

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