ERP TUTORIAL 1 A Brief Introduction to the Use of Event-Related Potentials (ERPs) in Studies of Perception and Attention Geoffrey F. Woodman Vanderbilt University Vanderbilt Vision Research Center Center for Integrative and Cognitive Neuroscience Abstract Due to the precise temporal resolution of electrophysiological recordings, the event-related potential (ERP) technique has proven particularly valuable for testing theories of perception and attention. Here, I provide a brief tutorial of the ERP technique for consumers of such research and those considering the use of human electrophysiology in their own work. My discussion begins with the basics regarding what brain activity ERPs measure and why they are well suited to reveal critical aspects of perceptual processing, attentional selection, and cognition that are unobservable with behavioral methods alone. I then review a number of important methodological issues and often forgotten facts that should be considered when evaluating or planning ERP experiments. Electroencephalogram (EEG) technique continue to make it one of the most recordings were the first method developed for widely used methods to study the architecture direct and noninvasive measurements brain of cognitive processing. activity from human subjects (Adrian & The primary goal of this tutorial is to Yamagiwa, 1935; Berger, 1929; Jasper, 1937, introduce researchers who are unfamiliar with 1948). By noting when stimuli were presented ERPs to their use, interpretation, and and tasks were performed, early studies dissemination in studies of sensation, examining the raw EEG sought to characterize perception, attention, and cognition. I hope the changes in the state of electrical activity that the uninitiated readers will become better during sensory processing and the consumers of ERP research. For those who performance of simple-detection tasks (e.g., P. plan to conduct ERP research and add human A. Davis, 1939; Walter, 1938). However, electrophysiology to your methodological when scientists began to take advantage of toolbox, I strongly urge you to read the more signal averaging the event-related potential detailed resources that are afforded the space (ERP) technique quickly became the primary to cover the theoretical and practical issues tool of the cognitive neuroscientist (Cooper, with which practicing electrophysiologist Winter, Crow, & Walter, 1965; H. Davis, should be familiar (Handy, 2005; Hillyard & 1964; Donchin, 1969; Donchin & Cohen, Picton, 1987; Luck, 2005; Nunez & 1967; Spong, Haider, & Lindsley, 1965; Srinivasan, 2006; Regan, 1989; Rugg & Coles, Sutton, Braren, Zubin, & John, 1965; Sutton, 1995).1 Tueting, Zubin, & John, 1967; Walter, Cooper, I will cover three general topics in this Aldridge, McCallum, & Winter, 1964). tutorial. First, I will provide an extremely Despite the rise of modern neuroimaging brief review of the biophysical basis of the methods, several advantages of the ERP EEG and the averaged ERPs which make them ERP TUTORIAL 2 ideal for studying perception and attention. appears to account for a number of Second, I will present advice for conducting observations. Early electrophysiologists and evaluating ERP studies that test specific hypothesized that the EEG and intracranially hypotheses. Third, I will discuss several often recorded field potentials (local-field potentials forgotten characteristics of ERPs that should or LFPs) were due to postsynaptic activity of be considered when designing new neural ensembles (Adrian & Yamagiwa, 1935; experiments and interpreting ERP findings. Li, McLennan, & Jasper, 1952). This view is The topics covered here were selected based widely accepted today (Logothetis, Pauls, on my experience reviewing and publishing Augath, Trinath, & Oeltermann, 2001; Luck, manuscripts reporting findings from ERP 2005; Nunez & Srinivasan, 2006), although experiments. A large number of ERP the biological basis of the EEG and ERPs has experiments, including my own, that have been periodically debated (e.g., Fox & serious trouble during the review process are O'Brien, 1965; Galambos & Jahasz, 1997). in such a state because the waveforms do not This means that instead of recording a afford unambiguous interpretation due to one summation of the action potentials generated or more of a handful of common problems. by individual neurons, we believe that the Before discussing the characteristics that EEG and averaged ERPs are measuring readers should look for in ERP studies, I will electrical potentials generated in the quickly review some basics about this extracellular fluid as ions flow across cell electrophysiological technique. membranes and neurons talk to one another via neurotransmitters. Why ERPs are Well Suited to Study To create electrical fields large enough Perception and Attention? to propagate through the brain, dura, skull, and With their spectacular spatial skin, a large number of neurons must be active resolution, it is reasonable to ask, “Why have simultaneously (i.e., in the ballpark of 107 imaging techniques not made ERPs obsolete?” neurons, see Cooper et al., 1965; Ebersole, The most direct answer to this question is 1997). In addition, this large group of neurons simple: time. By time, I mean that ERPs have not only needs to be active synchronously but a temporal resolution that allows for the also to have a geometry that is perpendicular measurement of brain activity from one relative to the surface of the skull and not millisecond to the next, and many aspects of cancelled out by other neuronal ensembles attention and perception appear to operate on a active at the same time and with an opposite scale of tens of milliseconds. As the brain is orientation (Luck, 2005; Nunez & Srinivasan, essentially a wet electrical device, these 2006). The simultaneously active neurons electrophysiological recordings provide a must have approximately the same orientation direct measure of the currency of the system for the potentials to summate and this means we study. Also, given the nature of electrical that ERPs are primarily generated by the activity and the tissue in which ERPs are postsynaptic potentials of cortical pyramidal generated and propagated, there is no cells (which are perpendicular to the cortical measurable conduction delay between the surface). Given the location and orientation of brain activity generated inside the head and the a specific neural generator in the brain, we can potentials recorded from the scalp (Nunez & predict the pattern of voltage that will be Srinivasan, 2006). observed across the head. This is known as What exactly generates the voltage the forward problem and is easily solved, fluctuations recorded outside the head? We unlike its evil twin, the inverse problem. The operate under a working hypothesis that inverse problem states that if we are given a ERP TUTORIAL 3 distribution of electrical potential across a Sheatz, 1962). This same period saw the volume conductor, like the head, then we development of the 10/20 system for cannot know where it is generated if we do not standardized electrode placement which made know the number of simultaneously active ERP findings far easier to integrate and generators a priori (Helmholtz, 1853). replicate across studies (Jasper, 1958). Practically, this means that we cannot The peaks and troughs of a stimulus- definitively localize the neural generators of locked ERP waveform allow us to visualize ERP effects within the head from the data cognitive processing as it unfolds during a recorded outside of it. Thus, the outstanding trial. Figure 1 shows idealized waveforms temporal resolution of ERPs comes with the time locked to the presentation of a visual cost of living with an unknown degree to stimulus during a target discrimination task. spatial resolution. First things first, you will note that voltage is Although the inability to resolve the plotted with negative going up. Stories about activity of individual neurons may seem like a the origin of this convention abound. It is large drawback of the ERP technique, it clear that this method of presentation has been, appears that the functional unit of analysis that and continues to be, a contentious issue as ERPs measure fortuitously maps on to the efforts have been made to flip the voltage axis cognitive processes that psychologists (Bach, 1998; Luck, 2005). In my own work, I frequently hypothesize about. Specifically, follow the decades-old convention of plotting ERPs allow us to observe a series of cognitive negative up for practical reasons. Specifically, operations that take place from before the the vast majority of existing ERP papers delivery of sensory information to the plotted their waveforms with negative going peripheral nervous system until even after a up and perceptual learning has made such behavioral response is made. The earliest waveforms significantly easier for me to studies showed that stereotyped fluctuations in interpret than those with negative plotted potential were elicited by the presentation of down. sensory stimuli (e.g., P. A. Davis, 1939). The series of voltage fluctuations However, ERP research really gained shown in Figure 1 index a sequence processes popularity when a study demonstrated that the as the brain transforms information from raw cognitive activity related to preparing for a sensory input to the appropriate behavioral task could be measured. The Contingent response. First, we see the C1 component Negative Variation (CNV) was shown to build which flips polarity based in whether the