Do excited molecules relaxing to their ground state pass through a 'seam' connecting the potential energy profiles of the states? Experimental data suggest the answer to this long-standing question is 'yes'. See Letter p. 440
Most of the modern understanding of chemistry, including the very notion of a well-defined molecular structure, rests on the concept of a potential energy surface (PES) — a 3N-dimensional 'landscape' that plots the total energy of a collection of N atoms as a function of the atomic positions. The PES can be used to determine several useful features, such as the most stable configuration of atoms, or the pathway along which atoms 'travel' during a reaction. Intersections of these surfaces (known as conical intersections) are thought to have an important role in transitions from excited states to ground states of molecules, but direct evidence of this has been hard to find. Reporting on page 440 of this issue, Polli et al.1 use ultrafast optical spectroscopy to follow the motion of the molecule retinal — whose light-induced isomerization forms the basis of vision — through a conical intersection. This provides much-needed experimental evidence of the involvement of conical intersections in de-excitations.
In order to define a PES, one must first invoke the Born–Oppenheimer approximation (BOA), which assumes that the electrons of an atomic system relax instantaneously to their lowest energy distribution. The electrons can then be taken out of the problem, so that the PES on which the atoms move becomes simply the electronic energy as a function of the atomic coordinates, plus energy contributions from the Coulombic repulsion of the positively charged nuclei. The success of the PES concept implies (correctly) that the BOA is normally an excellent approximation for molecules at room temperature.
The situation becomes dramatically different when electrons are excited, for example by absorption of a photon when molecules are exposed to light. Although the PES may remain a valid concept for some time after photoexcitation (the molecular motion of the excited electrons is simply governed by a different PES from that of the ground state), the electrons must eventually 'cool' and the molecule will return to the electronic ground state, violating the assumptions of the BOA. Because electrons are strongly quantum mechanical, this cooling is usually not a gradual energy transfer from electrons to molecular vibrations. Instead, it is often an ultrafast process that occurs most efficiently at molecular geometries in which two (or more) electronic states are isoenergetic2,3. Such geometries constitute conical intersections, and can be thought of as transition states in the relaxation of an electronically excited molecule. But unlike the transition states associated with ground-state reactions, conical intersections are not isolated molecular geometries. Rather, they are collections of geometries that form a high-dimensional 'seam', any point of which can serve as a doorway through which molecules may pass to reach the ground electronic state.
Although the mathematical possibility of conical intersections was noted shortly after the dawn of quantum mechanics4, the idea that they were critical to understanding excited-state reactivity was not immediately accepted. Over the past decade, evidence for these intersections from theoretical studies and molecular simulations has mounted, yet experimental evidence has mostly been circumstantial. One reason for this is the fleeting existence of molecules at the intersections. Like transition states for reactions in the electronic ground state, the conical intersection is energetically unstable, and so molecules rarely linger in its vicinity. Thus, the best hope for direct evidence of conical intersections comes from the femtosecond spectroscopy techniques (a femtosecond is 10−15 seconds) that have already successfully captured molecules at transition states5.
The added wrinkle is that conclusive identification of a conical intersection also requires observation of at least one of its signatures — such as the narrowing energy gap between two electronic states as they approach an intersection. For spectroscopic characterization, this requires the use of ultrafast laser pulses in the long-wavelength region of the spectrum that corresponds to these small energy gaps. Such pulses have only recently been obtained, and Polli et al.1 have now exploited them to provide the most compelling experimental evidence to date for the existence of a conical intersection in one of the most important photochemical reactions: the light-induced conformational change (isomerization) of the cofactor retinal in the protein rhodopsin, an event that initiates visual reception.
Polli et al. excited retinal in rhodopsin and then followed the molecule as it returned to its electronic ground state. By monitoring stimulated emission and absorption of light from the molecule, they mapped out the energy gap between the ground and excited electronic states as a function of time after excitation. These data revealed an initial decrease and a subsequent increase of the energy gap, consistent with passage through a conical intersection. The authors also simulated the excited-state dynamics of retinal in rhodopsin. These simulations were in good agreement with the measured data, which allowed the authors to infer the time-evolution of the geometry of retinal after excitation — effectively generating a molecular movie of the first step in vision.
The researchers found that, once excited, retinal reaches its conical intersection seam within an astonishingly short 75 femtoseconds, implying that the molecule makes a beeline for the intersection after excitation. This time is essentially the same as that predicted by theoretical simulations of retinal in the gas phase6,7,8. The similarity is surprising because, unlike in the gas-phase simulations, Polli et al. followed the isomerization of retinal in a crowded protein environment. Clearly, the binding pocket for retinal in rhodopsin must be ideally organized to both promote and accommodate the observed conformational change. Is this a coincidence, or has biology exploited the ultrafast nature of the reaction to efficiently capture photon energy? The answer to this long-standing question will become clearer through further application of techniques such as those described by Polli and colleagues.
As already mentioned, conical intersections are not isolated geometries, but form a seam. Polli et al. performed computational simulations of excited retinal in rhodopsin that provided insights into which of the geometries along the seam is responsible for the ultrafast de-excitation in rhodopsin. They found that the intersection has a strongly 'peaked' topography (Fig. 1). So perhaps it is not surprising that the passage of retinal through the conical intersection is nearly perfectly efficient — spectral signatures of part of the molecular wavepacket remaining on the excited state are largely absent from the experimental data.
An open question is how the topography around a seam affects the efficiency of transitions between electronic states at conical intersections. Further experimental studies tracing the paths of molecules through conical intersections that have different topographies would go a long way to answering this question, and on the basis of Polli and colleagues' study now seem to be feasible1. For example, one could investigate the dynamics of retinal de-excitation in rhodopsin mutants.
Finally, there is a unique telltale signature of conical intersections that Polli et al. did not directly observe: a quantum mechanical phase factor2 known as the geometric or Berry's phase. This phase should be manifest by otherwise unexpected interference effects between the different paths that molecules can take through or around an intersection (for example, when passing slightly to the left or right of the intersection). A remaining experimental challenge is to observe not only the decreasing energy gap between the excited and ground states around conical intersections, but also the effects of Berry's phase.
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Formation of a supramolecular charge-transfer complex. Ultrafast excited state dynamics and quantum-chemical calculations
Photochemical & Photobiological Sciences (2019)