CHEMICAL PHYSICS
Simultaneous observation of nuclear and electronic
dynamics by ultrafast electron diffraction
Jie Yang1,2†, Xiaolei Zhu1,2,3†, J. Pedro F. Nunes^4 , Jimmy K. Yu2,3,5, Robert M. Parrish1,2,3,
Thomas J. A. Wolf1,2, Martin Centurion^4 , Markus Gühr^6 , Renkai Li^1 ‡, Yusong Liu^7 , Bryan Moore^4 ,
Mario Niebuhr^6 , Suji Park^1 §, Xiaozhe Shen^1 , Stephen Weathersby^1 , Thomas Weinacht^7 ,
Todd J. Martinez1,2,3, Xijie Wang^1 *
Simultaneous observation of nuclear and electronic motion is crucial for a complete understanding
of molecular dynamics in excited electronic states. It is challenging for a single experiment to
independently follow both electronic and nuclear dynamics at the same time. Here we show that
ultrafast electron diffraction can be used to simultaneously record both electronic and nuclear
dynamics in isolated pyridine molecules, naturally disentangling the two components. Electronic
state changes (S 1 →S 0 internal conversion) were reflected by a strong transient signal in small-angle
inelastic scattering, and nuclear structural changes (ring puckering) were monitored by large-angle
elastic diffraction. Supported by ab initio nonadiabatic molecular dynamics and diffraction simulations,
our experiment provides a clear view of the interplay between electronic and nuclear dynamics of the
photoexcited pyridine molecule.
N
onadiabatic processes exhibit a complex
interplay between the electronic and
nuclear degrees of freedom. For elec-
tronically excited polyatomic molecules,
the vibronic or nonadiabatic couplings
become so strong that the Born-Oppenheimer
approximation often fails ( 1 ). This mixing be-
tween electronic and nuclear degrees of free-
dom presents great challenges to common
experimental and theoretical approaches. Spe-
cifically, it is experimentally challenging to
measure both electronic and nuclear dynamics
independently within a single experiment. For
time-resolved measurement of photoexcited
molecules, most pump-probe spectroscopy
focuses on the population dynamics between
electronic states. Valence electron spectros-
copy could be sensitive to both electron and
nuclear dynamics, but the two contributions
are often difficult to disentangle ( 2 ). Core
electron spectroscopy, such as extended x-ray
absorption fine structure, can resolve the struc-
turaldynamicsaroundalocalsitebuttypically
requiresthepresenceofoneormoreheavy
atoms ( 3 ). Time-resolved diffraction (TRD)
techniques, including ultrafast electron diffrac-
tion (UED) pioneered by Zewail and colleagues
in the 1990s ( 4 ) and time-resolved x-ray dif-
fraction (TRXD) enabled recently by x-ray free-
electron lasers, are able to resolve motion of
atomic nuclei during photochemical reactions
with femtosecond temporal resolution and
sub-angstrom spatial resolution ( 5 – 7 )buthave
so far been insensitive to electronic dynamics.
In most TRD experiments, the independent
atom model (IAM), in which the electron re-
distribution due to bond formation is com-
pletely ignored, is invoked to interpret the
diffraction patterns. A recent TRXD study by
Stankuset al. included the valence electron
contribution to the elastic scattering signal in
a Rydberg excitation, where the diffraction
signature of electronic and nuclear dynamics
is intertwined ( 7 ). As suggested from theory
( 8 , 9 ), the inelastic scattering signal is expected
to reflect electronic dynamics but, to the best
of our knowledge, has yet to be used in a TRD
experiment. In this work, we used UED to
study the photophysics of pyridine excited to
the S 1 (np*) state. We show that the inelastic
electron scattering modulates the scattering
pattern exclusively at small angles and thus
is a sensitive observable related directly to the
excited state population. Bycontrast, elastic scat-
tering signals at higher angles encode geo-
metric information. The clean separation of
elastic and inelastic scattering signals enables
a single UED experiment to simultaneously re-
solve both electronic [S 1 →S 0 internal conversion
(IC)] and nuclear (ring-puckering) dynamics
of the S 1 (np*) state in pyridine.
Pyridine is one of the simplest heterocyclic
compounds with rich nonadiabatic dynamics.
The investigation of its photophysics is central
to the understanding of interplay between
pp*andnp* states in heterocyclic compounds,which is critical for the photoprotection mech-
anism of nucleobases ( 10 ). It has been shown
that the radiationless transition of the pyridine
S 1 (np*) state is extremely sensitive to excess
vibrational energy: Higher excess vibrational
energy increases IC anddecreases intersystem
crossing quantum yield ( 11 ). This behavior is
reminiscent of the“channel-three”decay in
benzene and has drawn considerable interest
in past decades ( 12 , 13 ). Despite being exten-
sively studied, the photophysics of such a sim-
ple molecule is still under heated debate. Lim
( 14 ) proposed a proximity effect mechanism,
in which a pseudo–Jahn-Teller effect between
the close-lying np*andpp* states promotes
an out-of-plane torsional motion, which then
greatly enhances the Franck-Condon factor
for S 1 →S 0 IC. The strong dependence of the
(S 1 →S 0 )/(S 1 →T 1 ) branching ratio on the excess
vibrational energy is explained by a higher
energy barrier for the IC pathway. This mod-
el is supported by experimental absorption,
fluorescence, and time-resolved photofrag-
ment spectroscopy ( 13 , 15 , 16 ). Sobolewski and
Domcke ( 17 ) and Chachisvilis and Zewail ( 18 )
proposed that a crossing of the S 2 (pp*) and
S 1 (np*) states leads to the formation of a pre-
fulvenic structure. Zhonget al.( 19 ) proposed an
isomerization to Dewar and Hückel structures
after passing through a conical intersection
(CI). Lobastovet al.( 20 ) and Srinivasanet al.
( 21 ) reported ring opening of pyridine as the
dominant pathway after excitation with 267-nm
light. These conflicting models, each with its
own experimental evidence, persist in part be-
cause none of the previous experiments directly
measured the electronic and structural dynam-
ics independently and simultaneously.
In most UED experiments, data are analyzed
with the IAM, which ignores all electronic
redistribution due to chemical bonding or
electronic excitation. Specifically, this model
neglects two effects: the binding effect that
comes from the redistribution of average
electron density due to bond formation (one-
electron effect) and the correlation effect that
comes from electrons avoiding each other be-
cause of Coulomb repulsion and Pauli exclu-
sion (two-electron effect) ( 22 – 27 ). Iijimaet al.
( 22 ) and Bartell and Gavin ( 23 ) showed that
the binding and correlation effects exclusively
contribute to elastic and inelastic scattering,
respectively (see supplementary materials).
Typically, UED experiments use detectors with-
out energy selectivity, and thus elastic and
inelastic scattering are recorded together with-
out distinction.
Our experimental setup has been introduced
previously ( 5 , 6 , 28 ) and is schematically shown
inFig.1A.Briefly,the265-nmpumplaserand
the 3.7-MeV probe electrons intersected the
target gas jet almost colinearly, and the overall
instrumental response function (IRF) had a
full width at half maximum of ~150 fs ( 28 ). ToRESEARCH
Yanget al.,Science 368 , 885–889 (2020) 22 May 2020 1of5
(^1) SLAC National Accelerator Laboratory, Menlo Park, CA,
USA.^2 Stanford PULSE Institute, SLAC National Accelerator
Laboratory, Menlo Park, CA, USA.^3 Department of Chemistry,
Stanford University, Stanford, CA, USA.^4 Department of
Physics and Astronomy, University of Nebraska–Lincoln,
Lincoln, NE, USA.^5 Biophysics Program, Stanford
University, Stanford, CA, USA.^6 Institut für Physik und
Astronomie, Universität Potsdam, Potsdam, Germany.
(^7) Department of Physics and Astronomy, Stony Brook
University, Stony Brook, NY, USA.
*Corresponding author. Email: [email protected] (J.Y.);
[email protected] (T.J.M.); [email protected]
(X.W.)
†These authors contributed equally to this work.
‡Present address: Department of Engineering Physics, Tsinghua
University, Beijing, China.
§Present address: Center for Functional Nanomaterials, Brookhaven
National Laboratory, Upton, NY, USA.