Expectancy and response strategy in a three-choice visual task

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Electroencephalography and clinical Neurophysiology 99 (1996) 491-493

Short communication

Expectancy and response strategy in a three-choice visual task Tom,is Ortiz*, Fernando Maestri, Alberto Fem~indez Departamenro de Psicobiologfa, Universidad Complutense de Madrid, Campus de Somosaguas, 28223 Madrid, Spain Accepted for publication: 24 May 1996

Abstract We investigated the relationship between sensorial discrimination and motor response by means of movement-related potentials, in a task where subjects had to discriminate between 3 stimuli presented visually in a random way. The results indicate that subjects anticipate the response to each type of stimulus by following a probabilistic criterion in the absence of a warning stimulus. This criterion entails an erroneous lateralization of cerebral activation and a significant increase in reaction time, despite the reduction of errors.

Keywords: Lateralized readiness potential; Reaction time; Expectancy

1. Introduction

2. Methods and materials

In recent years a large number of articles have appeared focusing on the way the brain discriminates between two or more stimuli to make or choose a suitable response (Meyer et al., 1988; Osman et al., 1992). Within the field of movement-related potentials, Komhuber and Deecke (1965) discovered the existence of a negative component, labelled as Bereischaftpotential (BP), which appears contralaterally to the limb used before executing a voluntary movement. Later, Coles (1989) renamed this component using the term 'LRP' (lateralized readiness potential). Generally, studies in this cognitive domain (see Logan and Cowan, 1984; Coles et al., 1988; Gratton et al., 1988) use a research paradigm where subjects receive a warning stimulus prior to the presentation of two stimuli. Recently, Goodin et al. (1993) have carded on a new stimulation method which includes the presentation of 3 stimuli without warning. This methodology raises some doubts about the usefulness of LRP (see Gehring and Coles, 1994; Goodin and Aminoff, 1994). Our work tries to replicate the results obtained by Goodin et al. (1993), by using visual stimuli, which enables us to cast some light on this controversy.

Ten subjects (5 men and 5 women) aged 25.3 + 4 years old (mean + SD), voluntarily participated in these studies with the approval of the Ethical Committee of the Hospital Universitario San Carlos. All subjects were strictly righthanded for all daily living activities and scored 10 out of 10 points for right-handedness in the Edinburgh Handedness Inventory for hand preference (Oldfield, 1971). Visual stimuli were presented in the middle of a screen, with a sequence of 300 black circles, squares and triangles (300 ms duration, 9 cm diameter of visual objects and 16 cm diameter of all the visual field), on a white background, at a subtended visual angle of 10 °, and at a rate of one visual stimulus every 2 s. Subjects sat approximately 1 m away from a computer-driver video screen. The circles (frequent stimuli) appeared in 75% of the trials; the squares (rarel stimuli) appeared in 20% of the trials; and the triangles (rare2 stimuli) appeared in 5% of the trials. For each run, 300 visual stimuli (225 frequent, 60 rarel, 15 rare2) were presented pseudorandomly. Three experimental tasks were designed. In the first task, subjects responded to frequent stimuli by extending the middle finger of both hands simultaneously and as quickly as possible. In the second task (R1R), subjects responded to rarel stimulus by extending the right middle finger, and to rare2 stimulus by extending the left middle finger. In the third task (R1L), subjects extended the left

* Corresponding author. TeL: +34 91 3943070; fax: +34 91 3943189.

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middle finger in response to rare l, and the right middle finger in response to rare2. Each run was repeated to ensure replicability of the findings. Cerebral evoked potentials were recorded continuously from C3, Cz and C4 electrode positions on the scalp, according to the International 10/20 System: Eye movements were monitored by an electrode placed infraorbitally, referenced to linked ear electrodes A1/A2. The electromyogram (EMG) was recorded continuously from an electrode placed over the motor point of the extensor digitorum of each middle finger, referenced to an inactive electrode placed over the dorsum of the ipsilateral hand. Bandpass recordings were 0.25-70 Hz and the impedance was < 5 K for all electrodes, with a continuous sampling of 410 Hz and an A/D ratio of 12 bits. Cerebral and EMG responses were backward and forward averaged (500 ms in either direction) from the onset of the initial negative component of the compound muscle action potential (CMAP). Onset of the CMAP was initially determined by computer search and then confirmed by visual inspection prior to inclusion in the analysis. Trials containing substantial artifact or contaminated by eye movements were excluded from subsequent analysis. FREQUENT

Data analysis included trials where subjects responded correctly to the frequent visual stimuli (CF trials), to the rarel (CR1 trials), to the rare2 (CR2 trials), or incorrectly (errors) to the rarel (ER1 trials), and to the rare2 (ER2 trials). LRPs were computed according to Coles' method (Coles, 1989), using the formula: LRP = [mean [C3 - C4] left hand + mean [C4 - C3] right hand)/2, where C3 and C4 refer to single-trial digitized waveforms recorded from the C3 and C4 electrode placements on the scalp. Slopes of the LRP were measured for each trial in each subject exactly at the point where a positive or negative continuous deflection differing more than +1 mV from zero baseline appeared, and compared in the different response conditions using the Student t test. 3. Results The rate of error was significantly higher (P < 0.001) for rare visual stimuli (22.48% to rarel stimuli and 12.10% for the rare2 stimuli) than for the frequent stimuli (6%). Average response latency (means + SD) for the correct responses to the frequent stimuli (281.75 + 13.15) was

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Fig. 1. LRP components of the cerebral response, presented as grand averages, computed for the 3 correct two incorrect response outcomes. For rarel a downward deflection from baseline indicates a correct lateralization of the anticipatory LRP contralateral to the hand moved, whereas an upward deflection in rare2 indicates an incorrect (ipsilateral) lateralization. For frequent outcomes, both upward and downward deflections indicate incorrect preparation, because both hands must respond to the frequent stimulus. For errors an upward deflection indicates an incorrect lateralization of the response. On the time axis, 0 ms indicates the onset of the averaged CMAP. Thin arrows indicate the averaged time of stimulus onset for the different outcomes. Dashed lines indicate the end of the LRP, The vertical calibration line represents 4 ~V.

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significantly (P < 0.001) faster than the average response latency to either rarel stimuli (380.29 + 21.5) or rare2 stimuli (433.64 + 29.1). Fig. 1 shows the LRP computed for CF, CR1, CR2, ER1 and ER2 trials. In the correct responses a LRP is seen prior to EMG onset, indicating that subjects were prepared to respond to this stimulus prior to its occurrence. For the frequent visual stimuli, the LRP is flat, as expected if preparation of simultaneous movement were bilateral. The lateralization of the LRP is different for CR1 and CR2 trials. Within CR1 trials, LRP is correctly lateralized over the hemisphere contralateral to the movement to be executed, as judged by a slope that differed significantly from zero baseline in a negative direction (-2.5 + 0.5 mV). In contrast, for CR2 trials the lateralization of the LRP is incorrect, as evidenced by a slope that differed significantly from zero in a positive direction (+2 + 0.3 mV). In the analysis of errors to rarel and rare2 stimuli (ER1, ER2), these results are more clearly seen. Both ER1 and ER2 show an incorrect lateralization of the LRP as evidenced by a slope that differed significantly from zero in a positive direction (+3 + 0.8 and 3.9 + 0.5, respectively).

LRP are carried out with two-choice tasks, they forget that most of them use the presentation of a warning stimulus that reduces uncertainty or, in other words, the probability of responding with one limb or another (Gratton et al., 1988). When this warning stimulus is erroneous subjects tend to respond with the wrong limb; when this warning stimulus is neutral or does not exist, subjects carry out a guessing strategy (Gratton et al., 1988). If they 'get it right' the observed lateralization is correct; if they 'get it wrong', the lateralization is erroneous. For rare2, subjects, facing a situation where the stimuli have a marked difference in their probability, with no external element to reduce it, tend to prepare or activate their response to the most probable stimulus, the rarel. This interpretation is corroborated by the figure representing the cerebral response generated by errors to rare2 stimuli. There we find an even greater positive tendency, which demonstrates an ipsilateral, incorrect preparation of the response. A similar result is found in the graph representing LRP generated by errors to rarel. Once again we observe a positive tendency, although of much smaller magnitude, which supports the tendency of subjects to anticipate the response to rarel situation.

4. Discussion

References

Data presented here are similar to those found by Goodin et al. (1993). We coincide in the presence of a positive (incorrect) LRP when subjects respond to rare2 stimuli, in contrast with rarels where this process is correct. This positive deviation would suggest an erroneous anticipation of the responding hand. However, our interpretation of these findings differs slightly from that made by Goodin et al. (1993), as they claimed that the appearance of an incorrect positive response before rare2s 'raises doubt about the functional significance of the so-called premovement readiness potential'. On the other hand, Gehring and Coles' argumentation centers round the unexpected anticipatory response to rare2 stimuli. According to their argument, there is clear 'contamination' in the ~rare2 data, mainly because discrimination of these stimuli is quicker than for rarels, and this would be reflected in the smaller number of errors in this condition, a reduced P300 latency, and an increase in LRP preceding the correct response. One reason may be the control of pitch effect over rare2 stimuli, since the stimulus analysis time varies inversely with this variable (Woods et al., 1993). Our findings are a cc,nsequence of using visual stimuli with an identical area and intensity, eliminating the possibility of experimental contamination over stimulus evaluation time as suggested by Gehring and Coles (1994). Thus, when these authors point out that most of the papers on

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