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Imaging the Premotor Areas Nathalie Picard* and Peter L Strick†

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663 Imaging the premotor areas Nathalie Picard* and Peter L Strick† Recent imaging studies of motor function provide new insights critically on a clear definition of the location and boundaries into the organization of the premotor areas of the frontal lobe. of these cortical areas. Thus, one focus of our review The pre-supplementary motor area and the rostral portion of synthesizes the new data that is relevant to this issue. the dorsal premotor cortex, the ‘pre-PMd’, are, in many respects, more like prefrontal areas than motor areas. Recent Medial wall data also suggest the existence of separate functional divisions Pre-supplementary motor area and supplementary in the rostral cingulate zone. motor area In monkeys, it is now established that area 6 on the medial Addresses wall of the brain contains two separate areas: the supple- Department of Neurobiology, University of Pittsburgh School of mentary motor area proper (SMA) in the caudal portion of Medicine, W1640 Biomedical Science Tower, 200 Lothrop Street, area 6, and the pre-SMA in the rostral portion (Figure 1a; Pittsburgh, PA 15261, USA reviewed in [2,4]). The SMA and pre-SMA are equivalent *e-mail: [email protected] †e-mail: [email protected] to fields F3 and F6 described by Matelli et al. [5]. In humans, the level of the anterior commissure (VCA line) Current Opinion in Neurobiology 2001, 11:663–672 [6] marks the border between the two areas. The division 0959-4388/01/$ — see front matter of medial area 6 into two distinct fields is based on a © 2001 Elsevier Science Ltd. All rights reserved. collection of anatomical and functional data [2,4]. Because Abbreviations the pre-SMA was born out of a premotor area — the tradi- CCZ caudal cingulate zone tional SMA of Woolsey et al. [7] — the common perception CMAd dorsal cingulate motor area is that the pre-SMA is also a motor area. However, the CMAr rostral cingulate motor area connectivity and physiology of the pre-SMA suggest that it CMAv ventral cingulate motor area is more like a prefrontal area than a motor area. Prefrontal FEF frontal eye field fMRI functional magnetic resonance imaging areas provide cognitive, sensory or motivational inputs for M1 primary motor cortex motor behavior, whereas the motor areas are concerned PMd dorsal premotor cortex with more concrete aspects of movement (e.g. muscle PMv ventral premotor cortex patterns). Two important differences in the anatomical RCZ rostral cingulate zone RCZa anterior rostral cingulate zone connections of the SMA and pre-SMA support this view. RCZp posterior rostral cingulate zone First, only the SMA is directly connected to M1 and to the SMA supplementary motor area spinal cord [1,8–11]. Second, only the pre-SMA is inter- VCA line level of the anterior commissure connected with the prefrontal cortex [12–14]. These anatomical features, among others, are reflected by differ- Introduction ential patterns of activity in the SMA and pre-SMA [4]. Large regions of the brain located on the lateral surface and In neuroimaging studies, the pre-SMA/SMA distinction is on the medial wall of each hemisphere participate in the the clearest example of an anatomical and functional generation and control of movement. The premotor areas dissociation that emerged from the primate model [2]. In in the frontal lobe have the anatomical substrate to the following, we describe recent findings that provide influence motor output, both through connections with the further support for this dissociation. primary motor cortex (M1) and through direct projections to the spinal cord (e.g. [1]). In monkeys, the frontal lobe Initially, studies in monkeys suggested that the pre-SMA contains six well-defined premotor areas (Figure 1a). The has involved in learning sequential movements [15–17]. presence of analogous areas in humans has been inferred This motor view of pre-SMA function was supported by from functional imaging studies (Figure 1b) [2,3]. the observation that, in humans, activation of the pre-SMA However, the definition of premotor areas in humans is increased in parallel to acquisition of a motor sequence still evolving. Some associations between anatomy and task [18]. In contrast, SMA activation during the same task function proposed in the past [2] have been validated by was related simply to aspects of motor execution. More recent imaging data, and other associations are emerging. recent studies by the same group have resulted in a modi- fied view of pre-SMA function. Sakai et al. [19] recently In this review, we present the results of salient imaging compared pre-SMA activation in closely matched tasks studies that have helped to increase our understanding of that all required visuo–motor associations, but varied in the underlying anatomical and functional organization of motor and perceptual sequence components. Activation of the premotor areas. Much recent effort in the field of func- the pre-SMA occurred in all tasks related to visuo–motor tional imaging has been to examine brain regions involved association demands rather than to sequential components. in cognitive operations. The interpretation of activations In fact, pre-SMA activation was greatest in the conditional in premotor cortex during cognitive operations depends task, in which non-sequential responses were arbitrarily 664 Motor systems Figure 1 (a)Pre- (b) Motor areas of the frontal lobe in monkeys SMA SMA Pre- SMA M1 (a) and homologous areas in the human (b). SMA In humans, the border between areas 6 and 4 M1 on the lateral surface is located in the anterior CCZ bank of the central sulcus [65]. For illustration, CMAd RCZp CMAr CMAv RCZa the border is drawn on the surface of the hemisphere along the central sulcus (bottom, white dotted line). Except for the most medial portion, M1 does not occupy the precentral gyrus. Pictures of the monkey brain courtesy of Richard P Dum; pictures of the human brain reproduced with permission from [93]. PMd M1 Pre- PMd PMd FEF M1 PMv F7 F2 F1 FEF 44 45 PMv F4 F5 Current Opinion in Neurobiology determined by the color of visual cues, and showed a motor preparation, during working memory delays of a relative decrease in sequential paradigms. This important match to sample task [26] (Figure 2c). In addition, the study shows conclusively that activation of the pre-SMA in pre-SMA showed transient activation associated with shifts these tasks has little to do with motor sequence learning of attention to visual object features (shape, color, location) per se. Instead, pre-SMA activation occurs in association in a card sorting task [27]. Attending to various features of with establishing or retrieving visuo–motor associations visual stimuli was found to activate the pre-SMA equally in (see also [20,21]). The activity in the pre-SMA in associa- another context [28]. These results suggest that pre-SMA tion with visually cued changes between motor sequences function is more closely related to processing or mainte- [22,23] may also be due to the role of the pre-SMA in nance of relevant sensory information than response retrieving visuo–motor associations. selection or production. Additional studies have extended the involvement of Overall, neuroimaging studies leave no doubt that the the pre-SMA to associations based on auditory stimuli pre-SMA is fundamentally different from the SMA. [24••,25] (Figure 2a). Visual and auditory versions of a con- Activation of the SMA, caudal to the VCA line, is observed ditional choice reaction time paradigm generated pre-SMA primarily in relation to aspects of movement behavior. In activations of equal magnitude [25]. Thus, the contribu- contrast, pre-SMA activation, rostral to the VCA line, is tion of the pre-SMA to sensory–motor associations is associated with cognitive aspects of a variety of tasks (see modality-independent. In addition, the contribution of also [29–34]). These findings, together with anatomical the pre-SMA appears to be effector-independent. Similar results, suggest that the pre-SMA might be functionally regions are activated in conditional manual motor [24••,25] considered a region of prefrontal cortex. and oculomotor tasks [21] (Figure 2b). This is consistent with the poor somatotopic organization of the pre-SMA [2] Cingulate motor areas and supports the view that the pre-SMA operates at a more The cingulate sulcus contains three separate motor areas in abstract level. In contrast, SMA activation displayed only primates: the rostral cingulate motor area (CMAr), the cau- movement-related activation in visual or auditory tasks. dal cingulate motor area in the ventral bank of the sulcus (CMAv) and the caudal cingulate motor area in the dorsal It must be emphasized that pre-SMA activation during bank of the sulcus (CMAd; Figure 1a). We have proposed conditional motor behaviors was not due to response [2] that corresponding areas are also present in humans: a selection or preparation [19,24••]. In fact, activation patterns rostral cingulate zone (RCZ) with two subdivisions (anterior: of the pre-SMA during non-conditional behavior suggest RCZa, and posterior: RCZp) and a caudal cingulate that its contribution to sensory–motor association is zone (CCZ; Figure 1b). The anatomical variability of the detached from motor aspects of the task. For example, the cingulate sulcus in humans complicates functional analysis pre-SMA displayed sustained activation, independent of of this region [35–37]. As a consequence, a degree of Imaging the premotor areas Picard and Strick 665 Figure 2 Anatomical and functional distinction of the (a)Pre- (b) (c) SMA SMA and the pre-SMA in three different tasks. SMA SMA SEF (a) Top: activation in the SMA and pre-SMA during an auditory conditional task; bottom: selective activation in the pre-SMA during an CCZ auditory–motor association task.
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