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The Speeding of Voluntary Reaction by a Warning Signal

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The Speeding of Voluntary Reaction by a Warning Signal Psychophysiology, 46 (2009), 225–233. Wiley Periodicals, Inc. Printed in the USA. Copyright r 2009 Society for Psychophysiological Research DOI: 10.1111/j.1469-8986.2008.00716.x PRESIDENTIAL ADDRESS, 2006 The speeding of voluntary reaction by a warning signal STEVEN A. HACKLEY Department of Psychological Sciences, University of Missouri-Columbia, Columbia, Missouri, USA Abstract Warning signals can shorten reaction time (RT) via either a top-down mechanism, temporal attention, or a bottom-up one, phasic arousal. The goal of this review article is to identify the locus at which these processes influence RT. Electrophysiological and behavioral evidence indicate that the chronometric locus for both modulatory effects lies mainly within a narrow window at the center of the stimulus–response interval. This interval presumably encompasses late perceptual, response selection, and early motor processes. Phasic arousal is theorized to reduce the threshold for response selection within a circuit involving the supramarginal gyrus. A blind-sight study indicates that conscious, cortical level processing is necessary for temporal attention, at least when the warning signal is visual. Descriptors: Temporal attention, Phasic arousal, ERP/fMRI/EMG, Parkinson’s disease, Blind sight In the field of attention and performance, warning effects used to temporal orienting is associated with a pattern of brain activation be somewhat dismissively characterized as ‘‘nonselective.’’ that differs substantially from that observed during visuospatial Whereas perceptual resources are selectively focused on ear of orienting. entry in Hillyard’s classical paradigm (Hillyard, Hink, Schwent, The study of temporal orienting began with an experiment & Picton, 1973) or on a particular visuospatial location in performed by the founder of scientific psychology, Wilhelm Posner’s paradigm (Posner, 1980), only diffuse, nonspecific Wundt (1880, pp. 238–239). A simple reaction time (RT) task processes were thought to be engaged by a neutral warning was employed in which the subject released a telegraph key upon signal. This view changed dramatically with the introduction by hearing the impact of a steel ball against a metal plate upon which Coull and Nobre (1998) of a temporal analog of Posner’s it had been dropped. On half of the trials the participant was visuospatial orienting paradigm. The authors argued that allowed to witness the action of the electromagnetic release neutral warning signals do elicit a type of selective attention. It mechanism. This served as the warning signal. As expected, re- is a type of attention in which the individual orients to a particular action times were much shorter on warned than on unwarned point in time. In their revised version of Posner’s well-known task, trials (M 5 125 and 259 ms, respectively). Foreperiod duration a symbolic precue indicates the moment at which an imperative was manipulated by dropping the ball from a height of 5 versus stimulus is likely to occur. Key press latencies are shorter if 25 cm. The warning effect was larger with the longer foreperiod, the imperative does in fact occur at that moment (‘‘valid trials’’) a phenomenon that was later to be investigated systematically by as opposed to at some other point in time (‘‘invalid trials’’). Woodrow (1914). Neuroimaging methods allowed Coull and Nobre to show that Wundt (1896, p. 225) used what we would now call a ‘‘mixture analysis’’ of the RT distribution, coupled with introspective evidence, to argue for separable attention effects involving This article is based on a presidential address given at the 46th annual sensory and motor processes. In his view, subjects can adopt meeting of the Society for Psychophysiological Research. I acknowledge either a sensorial set, in which they wait for a clear perception of my coauthors whose work is reviewed here and the neurological patients the stimulus before responding, or a muscular set, in which who served as participants in the clinical studies. The theoretical devel- they focus on the action of releasing the key. Psychophysiology opment owes a special debt to two previous review papers for which mere now offers abundant evidence that precuing attention citation is not adequate, Niemi and Na¨a¨ta¨nen (1981) and Jennings and toward characteristics of the stimulus or of the response can van der Molen (2005). Finally, I express special appreciation to Jeff selectively modulate sensory and motor processes, respectively Miller, who was my principal collaborator during the early years of my (e.g., Bonnet, Requı´n, & Stelmach, 1991; Mangun, 1995). independent career, and to Fernando Valle-Incla´n, who has played this The purpose of the present review is to consider which processes role in more recent years. Address reprint requests to: Steven A. Hackley, Department of Psy- are modulated by a neutral warning signal, that is to say, one that chological Sciences, University of Missouri-Columbia, 210 McAlester precues only the imperative’s time of arrival. More specifically, Hall, Columbia, MO 65211, USA. E-mail: [email protected] the goal is to help explain the RTeffect discovered by Wundt the 225 226 S.A. Hackley year following his creation of the first laboratory of experimental a ‘‘simple systems’’ approach. There are few effects on either RT psychology. or reflex latency as large and robust as those produced by warn- ing, and the basic phenomena have been well conserved across the span of phylogeny. Comparing warning effects on voluntary and reflexive reac- Why Does This Still Matter? tions may be helpful toward understanding temporal orienting because the modulatory patterns are often parallel. For example, Warning effects merit a central role in the field of attention and per- a3 Â 3 manipulation of modalities showed that shortening of formance because of the fundamental nature of space and time. If blink latency and voluntary RT occurs for all combinations of understanding how we orient our attention spatially within the visual, acoustic, and cutaneous warning and response stimuli environment is important, then surely an understanding of tem- (Zeigler, Graham, & Hackley, 2001). Blink latency and volun- poral attention is of similar value. Casting the problem in these tary RT both decrease as a function of foreperiod duration when terms emphasizes the generality of temporal orienting. This type foreperiods of differing lengths are intermixed randomly within a of selective attention may underlie such diverse phenomena as block (e.g., Hackley & Graham, 1987). If the speeding of reflex- Pavlovian conditioning, the Contingent Negative Variation ive eyeblink and voluntary key-press responses obeys similar (CNV), prepulse facilitation, and anticipatory cardiac decelera- laws, then the underlying mechanisms might be the same. For tion, just to mention topics from within psychophysiology. example, if a warning signal facilitates synaptic transmission at Another motivation for studying warning effects is the hope alpha motor neurons or within the earliest segment of the sensory that it will lead to a better understanding of clinical phenomena, pathway, then similar effects of various manipulations should be such as the bradykinesia that characterizes Parkinson’s Disease observed for voluntary and reflexive reactions. (PD). Prior to our work on the topic, several purely behavioral In our Parkinson’s disease study, groups of patients, healthy studies had shown that patients with PD are able to some extent older adults, and college students performed a simple RT task in to benefit from a warning signal, and this benefit varies as a which the imperative stimulus was either an intense white-noise function of foreperiod duration (e.g., Jahanshahi, Brown, & burst or an air puff to the forehead (Jurkowski et al., 2005). Marsden, 1992). However, animal research implied that the loss Participants quickly squeezed a wooden dowel when either of of dopaminergic cells in PD should lead to a reduced effect of these stimuli was received. The warning signal was a visual grat- foreperiod duration (e.g., Brown & Robbins, 1991; MacDonald ing presented randomly 1.5, 4, or 6 s before the imperative. Be- & Meck, 2004). Also, the effect of foreperiod duration is exag- cause the cutaneous and acoustic imperative stimuli were gerated in schizophrenia (Zahn, Rosenthal, & Shakow, 1963), a reflexogenic, it was possible to record eyeblink reflexes in addi- disorder believed to involve excessive sensitivity to dopamine. tion to the voluntary, hand-grip responses. Given the involvement of neuromodulators in mediating warning What we observed was that foreperiod effects on reflexes were effects (discussed below), my colleagues and I thought it impor- quite similar across groups. For voluntary reactions, by contrast, tant to attempt to resolve this discrepancy (Jurkowski, Stepp, & only neurologically normal individuals (younger and older con- Hackley, 2005). To this end, we used electromyographic (EMG) trols) exhibited a variable foreperiod effect. These results con- recordings of voluntary and reflexive reactions to assess forepe- verge with animal data (e.g., Brown & Robbins, 1991) in riod duration effects in individuals whose dopamine system had implying that dopaminergic pathways contribute to temporal been compromised by Parkinson’s disease. attention. Previous studies have identified norepinephrine as the According to a widely held view, random variation of fore- key neuromodulator underlying warning effects (Coull, Jones, period influences temporal attention by
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