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Density EEG Study of Spatial Stimulus–Response Compatibility P Cognitive Brain Research 16 (2003) 309–322 www.elsevier.com/locate/cogbrainres Research report A ttention and movement-related motor cortex activation: a high- density EEG study of spatial stimulus–response compatibility P. Praamstraa,* , R. Oostenveld b aBehavioral Brain Sciences Centre, University of Birmingham, Birmingham B15 2TT, UK bDepartments of Neurology and Medical Physics, University Medical Centre Nijmegen, Nijmegen, The Netherlands Accepted 25 November 2002 Abstract Visual spatial attentional activation of motor areas has been documented in single cell neurophysiology and functional imaging studies of the brain. Here, we investigate a candidate event-related brain potential representing visuospatial attentional activity in motor areas of the cortex. The investigation aimed to elucidate the neural origin and the functional characteristics of this brain potential, which has been labelled N2cc and is typically observed in spatial stimulus–response compatibility tasks. High-density EEG was recorded in 10 subjects while they performed a Simon-type spatial stimulus–response compatibility task and a control task where the same stimuli were assigned to Go–Nogo response alternatives. The N2cc showed a time course parallel to the posteriorly distributed N2pc, associated with visuospatial selection. Scalp distribution and current source density reconstructions allowed a spatial separation of N2pc and centrally distributed N2cc and were compatible with a source for the N2cc in the lateral premotor cortex. Comparisons across tasks demonstrated that the N2cc depends on bilateral response readiness, ruling out an exclusively attentional interpretation. Instead, the activity appears associated with visuospatial attentional processes that serve the selection and suppression of competing responses, in accord with a function of the dorsal premotor cortex in response selection. Together, the results consolidate the N2cc as a new ERP component relevant to the investigation of visuospatial motor processes. 2002 Elsevier Science B.V. All rights reserved. Theme: Motor systems and sensorimotor integration Topic: Cortex Keywords: Stimulus–response compatibility; Visual spatial attention; Visuomotor processing; Event-related potentials; Premotor cortex 1 . Introduction model developed by Kornblum et al. posits that when stimulus and response sets share certain attributes, the Behavioral research into the processes that link sensory presentation of a stimulus can elicit an automatic activation input to motor output has made abundant use of ex- of the corresponding response. perimental approaches that manipulate the spatial relation Studies pertaining to the neural basis of spatial S-R between stimulus and response. With spatially congruent compatibility effects have addressed, among other ques- stimulus–response pairings, responses are typically faster tions, whether there is neural activity that can be taken to and more accurate than with spatially incongruent pairings express automatic response activation [11,52,68]. In a [18]. According to Kornblum et al. [31], spatial stimulus– single-cell study of monkey primary motor cortex, Riehle response (S-R) compatibility effects represent one par- et al. [52] acknowledged that this entails an unresolved ticular instance of a broader set of S-R compatibility ambiguity: early neuronal activation co-varying with effects that depend on the presence of shared features stimulus location can be interpreted either as a visuospatial between stimulus and response. The dimensional overlap representation or as an automatic activation of the spatially congruent response. This ambiguity exemplifies a more *Corresponding author. Tel.: 144-121-414-7211; fax: 144-121-414- general issue in sensorimotor neurophysiology, i.e. how to 4897. distinguish between neural activity representing the E-mail address: [email protected] (P. Praamstra). stimulus that instructs an action from that associated with 0926-6410/02/$ – see front matter 2002 Elsevier Science B.V. All rights reserved. doi:10.1016/S0926-6410(02)00286-0 310 P. Praamstra, R. Oostenveld / Cognitive Brain Research 16 (2003) 309–322 the action itself (e.g. Refs. [4,5,32,57]). It is, furthermore, tasks with a vertical arrangement of stimuli and response compounded by the problem that motor cortex neuronal hands, to ensure that stimulus asymmetries and shifts of activity following an instruction stimulus may also repre- attention are confined to the vertical axis and not picked up sent the reorientation of selective spatial attention [32]. by the LRP derivation, which measures only electric While similar ambiguities arise in human EEG studies, potential differences between homologous left-right scalp scalp-recorded event-related potentials (ERPs), in particu- electrode sites. This procedure dissociates stimulus and lar the lateralised readiness potential (LRP), have been attention-related EEG activity from response-related activi- successfully exploited to elucidate spatial S-R compatibili- ty, and has helped to establish the notion that spatial ty effects. A number of relevant ERP studies have sug- stimulus attributes can elicit automatic response activation gested that spatial attentional orientation, in the context of [14,60,62]. a spatial S-R compatibility task, elicits attention-related As already stated, the present study is concerned with motor cortex activation that can be identified in lateralised the presumably attention-related EEG activity above the ERPs [44,49,63]. The present study sought to further motor cortex that is subtracted out when using a vertical clarify the generation and functional characteristics of the S-R arrangement. There are two, closely related, dis- presumed attention-related activity. Firstly, because atten- advantages to the elimination of this activity from consid- tion-related activation of motor structures has been pro- eration when studying spatial S-R compatibility. Firstly, posed to play an important role in spatial S-R compatibility eliminating attention-related EEG activity ignores the effects [53,56]. Secondly, in order to consolidate the possible role of attention and attention-related motor cortex attention-related motor area activation as an ERP com- activation in the explanation of spatial S-R compatibility ponent relevant to the investigation of visuospatial motor effects. There is evidence that spatial S-R compatibility functions. We will first describe the relation of the atten- effects crucially depend on an attention shift towards the tion-related motor cortex activity to the movement-related location of a stimulus presented outside the attentional LRP and to the N2pc, an ERP component associated with focus [53,56]. According to the premotor theory of atten- visual spatial selection. tion, shifts of attention necessarily involve activity in Movement-related EEG activity in reaction time tasks is sensorimotor circuits. Thus, to the extent that these circuits typically isolated by subtracting the activity recorded coincide or interact with the sensorimotor structures that above the motor cortex ipsilateral to the response hand support the directional motor responses under study, from the activity recorded contralaterally. This subtraction attention-related motor activation needs to be taken into is performed for both response hands and the combined account in investigations of spatial S-R compatibility. signals form the LRP (for reviews see Refs. [8,16]). By the The second disadvantage of eliminating the attention- nature of its derivation, the LRP reflects the differential related N2pc is that this component’s overlap with the LRP activation of left and right motor cortices, providing a may be due not merely to volume conduction, but also, and sensitive measure of the point in time at which response more interestingly, to a shared neural substrate in the selection has progressed to a stage where side-specific motor cortex [44]. The extension of the N2pc from its motor activation is started. In addition, it is sensitive to occipital maximum towards central electrode sites is covert, automatic response tendencies elicited by salient commonly explained as a result of passive volume conduc- stimulus features [8]. Although the LRP derivation is tion [16,62]. In contrast, Wascher and Wauschkuhn [63] designed to separate movement-related from stimulus-re- noted that the N2pc, as seen in a spatial S-R compatibility lated EEG activity, it does not always prevent overlap. task, might reflect an interaction of attention and Using a visual stimulus display in which task-relevant movement-related processes, and thus be relevant to the stimuli are presented lateral from fixation, to create spatial explanation of compatibility effects. Praamstra and Plat S-R (in)compatibility, there will usually be a lateralisation [49] reported current source density analyses of the N2pc of visual evoked EEG responses, especially at electrode that showed current extrema located over occipital and sites overlying the occipital cortex. Moreover, when the central areas of the brain, suggesting that the central visual display contains multiple elements of which only extension of the N2pc might be due to concurrent activa- one is task-relevant, the visual response is followed by a tion of visual and motor areas. As a candidate motor area lateralised ERP component related to visuospatial selec- to generate this activity, they suggested the dorsal pre- tion. This attention-related ERP component has been motor cortex (PMd), a premotor area close
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