Real-Space Identification ofIntermolecular Bonding with AtomicForce MicroscopyJun Zhang,1* Pengcheng Chen,1* Bingkai Yuan,1 Wei Ji,2† Zhihai Cheng,1† Xiaohui Qiu1†

We report a real-space visualization of the formation of hydrogen bonding in 8-hydroxyquinoline(8-hq) molecular assemblies on a Cu(111) substrate, using noncontact atomic force microscopy(NC-AFM). The atomically resolved molecular structures enable a precise determination of thecharacteristics of hydrogen bonding networks, including the bonding sites, orientations, andlengths. The observation of bond contrast was interpreted by ab initio density functionalcalculations, which indicated the electron density contribution from the hybridized electronicstate of the hydrogen bond. Intermolecular coordination between the dehydrogenated 8-hq andCu adatoms was also revealed by the submolecular resolution AFM characterization. The directidentification of local bonding configurations by NC-AFM would facilitate detailed investigationsof intermolecular interactions in complex molecules with multiple active sites.

Intermolecular bonding has been experimen-tally characterized mainly through crystallog-raphy via x-ray and electron diffractions, as

well as through infrared, Raman, nuclear mag-netic resonance, and near-edge extended absorp-tion fine-structure spectroscopy (1, 2). At thesingle-molecule level, state-of-the-art scanningtunneling microscopy (STM) is a technique wide-ly used to elucidate the molecular structure andchemical specificity of surface-immobilized spe-cies (3–5). The bonding interactions betweenmolecules in self-assemblies were also evidencedin scanning tunneling hydrogen microscopy (6).Nevertheless, most of the characterization tech-niques are, thus far, more sensitive to the covalentstructures of the molecules, and in many cases,theoretical calculations of intermolecular inter-action are also not as precise as those for co-valently bound species.

Recently, noncontact atomic force micros-copy (NC-AFM) has achieved superior resolutionin real-space that has enabled the identificationof the chemical structure, adsorption configura-tions, and chemical transformation of individualmolecules (7–10). For example, the differencein bond order in aromatic molecules was distin-guished via electron-density–dependent Pauli re-pulsion with CO-functionalized NC-AFM tips(11), and AFM tomography revealed the angularsymmetry of a chemical bond on surface (12).Herein, we used NC-AFM to investigate the in-termolecular interactions in 8-hydroxyquinoline(8-hq) (Fig. 1A) molecular assemblies formed onCu(111) at liquid helium (LHe) and room tempera-tures (RTs). The hydrogen bonds (H bonds) formedbetween 8-hq molecules were characterized by

high-resolution AFM images, and the local bond-ing configuration was determined with the atomicprecision.We also observe the coordination com-plex composed of dehydrogenated 8-hq and Cuadatoms. The observations were validated with abinitio density functional theory (DFT) calculations.

The 8-hq molecules deposited on Cu(111)at LHe temperature appeared as individual mole-cules or randomly assembled aggregates (fig. S1)(13). For the single 8-hq molecules, DFT calcu-lations suggest that themolecular plane is slightlytilted with respect to the substrate because ofthe weak interactions between the OH groupand the N atom of 8-hq and Cu(111) surface.Compared with the calculated total electron den-sity of the molecule shown in Fig. 1B, the STM

image (Fig. 1C) exhibits no internal features ofthe heterocycle because the tunneling current isprimarily sensitive to the local density of statesnear the Fermi level. In contrast, the AFM imageswith a CO-functionalized tip revealed the sub-molecular structure of 8-hq through the short-range Pauli repulsive force (Fig. 1, D to F). Thecalculated electron density map (Fig. 1B) qual-itatively reproduces the observed contrast in fre-quency shift (Df ) in the AFM image. Here, theAFM sensor measured the total force of threecomponents (7, 14): (i) the long-range attractiveelectrostatic forces, responsible for the overallnegative Df background in the images; (ii) theattractive van der Waals force, which contrib-uted to the dark halo surrounding the moleculewithout atomic corrugation; and (iii) the short-range Pauli repulsion, which contributed to theatomic contrast of molecular structure with re-spect to the metal substrate. When the tip heightwas decreased (Fig. 1, D to F), the increasingproportion of Pauli repulsion in the total forceenhanced contrast in the AFM images. Althougha quantitative understanding of the AFM imagingmechanism is nontrivial, a direct correlation be-tween the AFM images and the chemical struc-ture of a molecule can still be rationalized. In ourcase, the heterocyclic skeleton and the hydroxylgroup of 8-hq were readily distinguished. The pyr-idine ring in the heterocycle is slightly pronounced,which may be caused by tilting of the molecularplane on the substrate. A further interpretationof the topography need also take into account thedifference in electron density of the phenol ringand the pyridine ring.

The AFM images of the 8-hq molecular ag-gregates (Fig. 2, A and B) reveal bonding-like

1Key Laboratory of Standardization and Measurement forNanotechnology, Chinese Academy of Sciences, National Centerfor Nanoscience and Technology, Beijing 100190, China. 2De-partment of Physics, RenminUniversity of China, Beijing100872,China.

*These authors contributed equally to this work.†Corresponding author. E-mail: xhqiu@nanoctr.cn (X.Q.);chengzh@nanoctr.cn (Z.C.); wji@ruc.edu.cn (W.J.)

Fig. 1. STM and AFM measurements and DFT calculations of single 8-hq on Cu(111). (A)Chemical structure of 8-hq. (B) DFT-calculated molecular electron density maps at a distance of 150 pmabove the molecule. (C) Constant-current STM topography image (voltage V= –100mV, current I= 100 pA)with a CO-functionalized tip. (D to F) Constant-height AFM frequency shift images (V = 0 V, amplitudeA = 100 pm) at different tip heights. The tip height Dz was set with respect to a reference height givenby the STM set point above (–100 mV, 100 pA) the bare Cu(111) substrate in the vicinity of the molecule.The plus (or minus) sign denotes the increase (or decrease) of tip height. (D)Dz=+30 pm; (E)Dz=+10 pm;(F) Dz = 0 pm. The size of all images is 1.3 by 1.0 nm.

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features between adjacent molecules in the assem-blies that were reproduced in all of the observa-tions, whereas these features were not observedin the corresponding STM images at the sameregions [see fig. S3 and (13)]. A close examinationof the position and orientation of the bonding-like structures indicated that they coincide verywell with the expected locations ofH bonds formedbetween 8-hq molecules (Fig. 2, C and D). Theresults from recent theoretical and experimentalinvestigations suggest that the H bond has bothan electrostatic origin and a partly covalent char-acter (15, 16). Despite extensive studies of Hbonding in supramolecular and biological sys-tems using various techniques, direct identifica-tion of the bonding configuration of the H bondin real-space is elusive (17).

The formation of covalent bonds in uni-molecular reactions has recently been reported(10). The bond contrast in the AFM images hasbeen qualitatively compared with the bond order,where the higher local electron density leads tostronger Pauli repulsion exerted on the tip (10, 11).In our observations, the Df contrast of these inter-molecular bonds is comparable to that of intra-molecular covalent bonds in the constant-heightimages, as also evident in the force spectroscopymeasurements (fig. S4) (13). Given the clearlyidentified bonding sites, we could perform a de-tailed analysis of the H bond configurations (18).The apparent bond lengths of the intermolecularH bonds were measured, as summarized in fig.S5 (13), and can be used as a reference for dataacquired through other characterization methodsto understand the effect of the substrate on Hbonding (19).

Our study also revealed differences in the Hbond configurations in the 8-hq self-assemblieson surface and those in the bulk crystal. In ad-dition to the conventional H bond, which in-volves only the OH group and N atom of 8-hq,we also observed H bond formation between thearomatic rings and the OH group or N atom. Theseresults provide direct evidence for the influenceof substrate on the intermolecular bonding char-acteristics (1, 20).

We performed DFTcalculations on two typesof molecular clusters to further understand theorigin of the contrast of intermolecular H bondsin our observation. In Fig. 3A, the paired 8-hq mol-ecules were bonded by two H bonds of O-H···N,as illustrated by the black dotted lines in Fig. 3B(21). The calculated total electron density plottedin Fig. 3C shows a bright spot at the position ofthe O atom and a protrusion toward the adjacentmolecule around the position of the N atom. Thein-plane plot of the differential charge density(Fig. 3D), which is defined as rDCD ¼ rTotal −rSubstrate − ∑rMolecule (where rTotal is the electrondensity of 8-hq adsorbed on the Cu substrate,rSubstrate is the electron density of the Cu substrate,and rMolecule is the electron density of 8-hq), re-flects the charge redistribution after the bondforms between two 8-hq molecules and indicatesthat covalent-like characteristics developed from

charge reductions near the H and N atoms thatled to charge accumulation between them. Asexpected, the enhanced charge density at N andO is consistent with the charge transfer from H toN and O atoms, whereas the charge accumulationoffers an additional repulsive force to the tip atthe region along the H bonding direction. Thus,the observed line feature between the two 8-hqmolecules in the AFM image is attributed to ajoint effect that results from both the covalentcharge in H···N and the charge transferred fromH to N and O. The above interpretation is pri-marily based on the simplified mechanism oftip-to-sample Pauli repulsion (22). A quantitativeunderstanding of the image contrast of an H bondmay require further consideration of the relaxa-tion of the CO molecule attached on the tip apex(11). In another configuration (Fig. 3, E to H),DFTcalculations also concluded electron densityredistribution in the proximity of the newly formedbond. In this unconventional C-H···N hydrogenbond, the effect of charge accumulation betweenN andH atoms ismuchweaker comparedwith thatin the O-H···N hydrogen bond (1, 15).

When 8-hq was deposited onto Cu(111) atRT, the molecules formed highly ordered dimersand trimers, which are distinct from the H-bondedaggregates formed at the LHe temperature. Nointernal structures of these dimers and trimerscould be resolved in the high-resolution STMimages (fig. S8). The size of these molecular

aggregates did not correspond to those of theH-bonded clusters from DFT calculations. TheAFM images of the dimers and trimers (Fig. 4,A and B) allowed the identification of the outeredge of the molecules corresponding to the po-sitions of H or C atoms, but the inner edge wasblurred.

The dehydrogenation of the hydroxyl groupon Cu(111) at RT has been widely reported (23).Our experimental and theoretical calculation re-sults also suggest that the individual 8-hq mole-cules exist as radical species that are weaklybound to the substrate by O and N atoms in atilted orientation (fig. S7). Alternatively, the high-ly mobile 8-hq radicals coordinate with Cuadatoms on surface to form an organometalliccomplex (24). The proposed chemical structuresof a dimer and trimer, respectively, in whichthe dehydrogenated 8-hq is assembled via anO(N)-Cu bond, are shown in Fig. 4, C andD. Thecalculated geometric sizes of these 8-hq com-plexes agree well with the AFM observations.

When the AFM is operated in the Pauli re-pulsion regime, the repulsive force from theoutermost-shell valence electrons is also relevantto∇2ϕnðrÞ, which is in the form of kinetic energy.Here, ϕnðrÞ is the electron wave function of thenth eigenstate of the sample. The kinetic energyreflects the localization property of electrons,which can be estimated by the electron locali-zation function (ELF) (25). The ELF of the dimer

Fig. 2. AFM measurements of 8-hq assembled clusters on Cu(111). (A and B) Constant-heightfrequency shift images of typical molecule-assembled clusters and their corresponding structure models(C and D). Imaging parameters: V = 0 V, A = 100 pm, Dz = +10 pm. Image size: (A) 2.3 by 2.0 nm; (B)2.5 by 1.8 nm. The dashed lines in (C) and (D) indicate likely H bonds between 8-hq molecules. Green,carbon; blue, nitrogen; red, oxygen; white, hydrogen.

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and trimer exhibited strongly localized electrondensity donation from N to Cu, whereas the elec-trons between the Cu-Cu bonding are rather de-localized (Fig. 4, E and F). We attributed thebonding features in the central regions of thedimer and trimer to N-Cu coordination bonding,similar to the observed formation of the metal-organic coordinate bond excited by inelastic elec-trons (9, 26). According to the ELF, the O-Cubond is strongly polarized, and the most sharedelectrons of the bond are localized around O;thus, the AFM signal is negligible. The C-H···Ohydrogen bonds formed in the dimer and trimerwere detectable in AFM because of the localizedelectrons around O and H.

Structural details—including the molecularconformation, the bond configuration, and the in-teracting sites on the functional groups—acquiredfrom high-resolution noncontact AFM imagesprovided useful insights into the mechanisms ofmolecular assembly and recognition. Becausethe H bond is ubiquitous in nature and centralto biological functions, the present techniquemay provide an important and complementarycharacterization method for unraveling the fun-damental aspects of molecular interactions atthe single-molecule level. The observation of Hbonding in real-space may also stimulate theoret-ical discussion about the nature of this intermo-lecular interaction.

References and Notes1. K. Müller-Dethlefs, P. Hobza, Chem. Rev. 100, 143–168

(2000).2. C. A. Hunter, Angew. Chem. Int. Ed. 43, 5310–5324 (2004).3. H. J. Lee, W. Ho, Science 286, 1719–1722 (1999).4. R. Temirov, S. Soubatch, A. Luican, F. S. Tautz, Nature

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(2007).6. C. Weiss, C. Wagner, R. Temirov, F. S. Tautz, J. Am.

Chem. Soc. 132, 11864–11865 (2010).7. L. Gross, F. Mohn, N. Moll, P. Liljeroth, G. Meyer, Science

325, 1110–1114 (2009).8. L. Gross et al., Nat. Chem. 2, 821–825 (2010).9. F. Albrecht, M. Neu, C. Quest, I. Swart, J. Repp, J. Am.

Chem. Soc. 135, 9200–9203 (2013).10. D. G. de Oteyza et al., Science 340, 1434–1437 (2013).11. L. Gross et al., Science 337, 1326–1329 (2012).

Fig. 4. AFMmeasurements andDFTcalculations of coordination com-plexes (dehydrogenated 8-hq andcopperadatoms)onCu(111).Constant-height AFM frequency shift images(A and B), the corresponding DFT-calculated structure models (C and D),and electron localization function maps(E and F) of dimer (Cuq2) and trimer(Cu3q3) complexes (q, dehydrogenated8-hq). Imaging parameters: (A) V= 0 V,A = 100 pm, Dz = +100 pm, 2.0 by2.0 nm; (B) V = 0 V, A = 100 pm, Dz =+80pm, 2.4 by2.4 nm. The tip heightDzwas set with respect to a reference heightgiven by the STM set point (–30 mV,100 pA) above the bare Cu(111) sub-strate. The dashed lines in (C) and (D)refer to the H bonds formed in the com-plexes. The complexes were formed bydepositing8-hqonCu(111) at RT.Orangespheres represent Cu adatoms.

Fig. 3. AFM measurements andDFT calculations of 8-hq dimerson Cu(111). Constant-height fre-quency shift image of the O-H···Ndimer (A) and the N···H-Ph dimer(Ph, phenyl) (E) and their corre-sponding DFT-calculated structuremodels (B and F), electron densitymaps (C and G), and charge differ-ence maps (D and H). Imaging pa-rameters: V= 0 V, A=100 pm,Dz=+50 pm (A), Dz = +10 pm (E). Im-age size: (A) 1.6 by 1.6 nm; (E) 1.5by 2.0 nm. The dashed frames in (B)and (F) indicate the calculation re-gions in (D) and (H).

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12. J. Welker, F. J. Giessibl, Science 336, 444–449 (2012).13. Supplementary materials are available on Science Online.14. L. Gross, Nat. Chem. 3, 273–278 (2011).15. T. Steiner, Angew. Chem. Int. Ed. 41, 48–76 (2002).16. G. R. Desiraju, Angew. Chem. 123, 52–60 (2011).17. The observation of an intramolecular hydrogen bond was

tentatively proposed by Gross et al. in the study of theorganic compound cephalandole A (8).

18. The measured bond length may involve the amplificationeffect of CO on the tip apex, as discussed in (11). Itshould also be noted that the expected bending ofX−H···Y was not resolved in all of the hydrogenbonds shown in Fig. 2, A and B. The exact mechanismwas not understood.

19. G. Jones, S. J. Jenkins, D. A. King, Surf. Sci. 600,224–228 (2006).

20. J. Carrasco, A. Hodgson, A. Michaelides, Nat. Mater. 11,667–674 (2012).

21. We found that it is difficult to obtain a high-resolutionAFM image on this specific type of 8-hq dimer comparedwith single molecules or other molecular aggregates.

These dimers often accidentally dislocate during AFMimaging, indicating a weaker interactions between themolecules and the substrate. We suggested that theformation of two hydrogen bonds in the dimer weakenthe binding interaction of -OH and N of 8-hq to themetal substrate. Note that the optimal imagingparameters for this dimer (see the Fig. 3A legend) aredifferent from those used for other molecular clusters.

22. We conducted a further calculation (13) following themethod proposed in (27).

23. X. C. Guo, R. J. Madix, Surf. Sci. 341, L1065–L1071 (1995).24. J. V. Barth, G. Costantini, K. Kern, Nature 437, 671–679

(2005).25. B. Silvi, A. Savin, Nature 371, 683–686 (1994).26. F. Mohn et al., Phys. Rev. Lett. 105, 266102 (2010).27. N. Moll, L. Gross, F. Mohn, A. Curioni, G. Meyer,

New J. Phys. 14, 083023 (2012).

Acknowledgments: This project is partially supported bythe Ministry of Science and Technology of China (grants2012CB933001 and 2012CB932704), the Natural Science

Foundation of China (grants 21173058, 21203038,11274308, and 11004244), the Beijing Natural ScienceFoundation (grant 2112019), and the Basic ResearchFunds in Renmin University of China from the CentralGovernment (grant no. 12XNLJ03). W.J. was supportedby the Program for New Century Excellent Talents inUniversities. Calculations were performed at the PhysicsLab for High-Performance Computing of Renmin Universityof China and Shanghai Supercomputer Center. We thankW. Ho, P. Grutter, and L. Gross for valuable discussionand technical advice.

Supplementary Materialswww.sciencemag.org/content/342/6158/611/suppl/DC1Materials and MethodsFigs. S1 to S9References (28–32)

1 July 2013; accepted 9 September 2013Published online 26 September 2013;10.1126/science.1242603

One-Dimensional Electrical Contact toa Two-Dimensional MaterialL. Wang,1,2* I. Meric,1* P. Y. Huang,3 Q. Gao,4 Y. Gao,2 H. Tran,5 T. Taniguchi,6 K. Watanabe,6

L. M. Campos,5 D. A. Muller,3 J. Guo,4 P. Kim,7 J. Hone,2 K. L. Shepard,1† C. R. Dean1,2,8†

Heterostructures based on layering of two-dimensional (2D) materials such as graphene andhexagonal boron nitride represent a new class of electronic devices. Realizing this potential,however, depends critically on the ability to make high-quality electrical contact. Here, we reporta contact geometry in which we metalize only the 1D edge of a 2D graphene layer. In additionto outperforming conventional surface contacts, the edge-contact geometry allows a completeseparation of the layer assembly and contact metallization processes. In graphene heterostructures,this enables high electronic performance, including low-temperature ballistic transport overdistances longer than 15 micrometers, and room-temperature mobility comparable to thetheoretical phonon-scattering limit. The edge-contact geometry provides new design possibilitiesfor multilayered structures of complimentary 2D materials.

Atomically thin two-dimensional (2D) ma-terials (1, 2)—such as graphene, hexago-nal boron nitride (BN), and the transition

metal dichalcogenides (TMDCs)—offer a variety ofoutstanding properties for fundamental studiesand applications. More recently, the capabilityto assemble multiple 2D materials with comple-mentary properties into layered heterogeneousstructures presents an exciting new opportunityin materials design (2–11), but several fundamen-tal challenges remain, including making goodelectrical contact to the encapsulated 2D layers.Electrically interfacing 3D metal electrodes to 2D

materials is inherently problematic. For graphenedevices, the customary approach is to metalizethe 2D surface. However, graphene lacks surfacebonding sites, so the lack of chemical bondingand strong orbital hybridization leads to large con-tact resistance (12–19). In multilayer structures,the requirement to expose the surface for metalli-zation presents additional restrictive demands onthe fabrication process. For example, encapsulatedBN/graphene/BN heterostructures (BN-G-BN)need to be assembled sequentially so as to leavethe graphene surface accessible during metalli-zation, because no process to selectively removethe BN layers has been identified. Moreover, poly-mers used during both the layer assembly andlithography steps are difficult to remove (20).Their presence can degrade the electrical contact(21, 22) and channel mobility (23) and contam-inate the layer interfaces, causing bubbles andwrinkles that multiply with the addition of eachsuccessive layer, limiting typical device size to~1 mm (2, 4, 24).

We demonstrate a new device topologywhere 3D metal electrodes are connected to a2D graphene layer along the 1D graphene edge(14, 19, 25–27). We first encapsulate the graphene

layer in BN. The entire multilevel stack is thenetched to expose only the edge of the graphenelayer, which is in turn metalized. This contactgeometry is similar to that in conventional semi-conductor field-effect transistors (FETs), wheredoped 3D bulk regions make lateral contact toa 2D electron gas. Although carrier injection islimited only to the 1D atomic edge of the graphenesheet, the contact resistance is remarkably low(as lowas 100ohm·mmin somedevices). The edge-contact process also allows a complete separationof the layer assembly and contact metallizationprocesses, which permits implementation of apolymer-free layer assembly method. Combiningthese two techniques, we fabricated graphene de-vices with unprecedented performance exhibitingroom-temperature mobility up to 140,000 cm2/Vsand sheet resistivity below 40 ohms per square atn > 4 × 1012 cm−2, comparable to the theoreticallimit imposed by acoustic phonon scattering. Attemperatures below 40 K, we observed ballistictransport over length scales longer than 15 mm.

The edge-contact fabrication process is illus-trated in Fig. 1A. Beginning with a BN-G-BNheterostructure, a hard mask is defined on the topBN surface by electron-beam lithography (EBL)of a hydrogen-silsesquioxane (HSQ) resist. Theregions of the heterostructure outside of the maskare then plasma-etched (see supplementary ma-terials section 1.2) to expose the graphene edge.Finally, metal leads (1 nmCr/15 nmPd/60 nmAu)are deposited by electron beam evaporation tomake electrical contact along this edge (othermetal combinations showed inferior performance)(table S1). In Fig. 1B, a cross section scanningtransmission electron microscope (STEM) imageof a representative device shows the resultinggeometry of the edge-contact. In the magnifiedregion, electron energy-loss spectroscopy (EELS)mapping confirms that the graphene and metaloverlap at a well-defined interface. From the an-gle of the etch profile (~45°), we expect that thegraphene terrace is exposed only 1 to 2 atomsdeep. Within the resolution of the STEM image,there is no evidence of metal diffusion into thegraphene/BN interface, confirming the truly edge

1Department of Electrical Engineering, Columbia University,New York, NY 10027, USA. 2Department of Mechanical Engi-neering, Columbia University, New York, NY 10027, USA. 3Schoolof Applied and Engineering Physics, Cornell University, Ithaca,NY 14853, USA. 4Department of Electrical and Computer Engi-neering, University of Florida, Gainesville, FL 32611, USA. 5De-partment of Chemistry, Columbia University, New York, NY10027, USA. 6National Institute for Materials Science, 1-1 Namiki,Tsukuba 305-0044, Japan. 7Department of Physics, ColumbiaUniversity, New York, NY 10027, USA. 8Department of Physics,The City College of New York, New York, NY 10031, USA.

*These authors contributed equally to this work.†Corresponding author. E-mail: cdean@ccny.cuny.edu (C.R.D.);shepard@ee.columbia.edu (K.L.S.)

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