ReviewImaging the premotor areas
Introduction
Large regions of the brain located on the lateral surface and on the medial wall of each hemisphere participate in the generation and control of movement. The premotor areas in the frontal lobe have the anatomical substrate to influence motor output, both through connections with the primary motor cortex (M1) and through direct projections to the spinal cord (e.g. [1]). In monkeys, the frontal lobe contains six well-defined premotor areas (Fig. 1a). The presence of analogous areas in humans has been inferred from functional imaging studies (Fig. 1b) 2., 3.. However, the definition of premotor areas in humans is still evolving. Some associations between anatomy and function proposed in the past [2] have been validated by recent imaging data, and other associations are emerging.
In this review, we present the results of salient imaging studies that have helped to increase our understanding of the underlying anatomical and functional organization of the premotor areas. Much recent effort in the field of functional imaging has been to examine brain regions involved in cognitive operations. The interpretation of activations in premotor cortex during cognitive operations depends critically on a clear definition of the location and boundaries of these cortical areas. Thus, one focus of our review synthesizes the new data that is relevant to this issue.
Section snippets
Pre-supplementary motor area and supplementary motor area
In monkeys, it is now established that area 6 on the medial wall of the brain contains two separate areas: the supplementary motor area proper (SMA) in the caudal portion of area 6, and the pre-SMA in the rostral portion (Fig. 1a; reviewed in 2., 4.). The SMA and pre-SMA are equivalent to fields F3 and F6 described by Matelli et al. [5]. In humans, the level of the anterior commissure (VCA line) [6] marks the border between the two areas. The division of medial area 6 into two distinct fields
The dorsal part of the lateral premotor cortex
In monkeys, the dorsal part of the lateral premotor cortex (PMd) has been divided into rostral (F7, PMdr) and caudal (F2, PMdc) subdivisions 5., 52., on the basis of anatomical and physiological differences (Fig. 1a). These differences are analogous to those that generate the pre-SMA/SMA split. In fact, in a number of important respects, the caudal portion of the PMd has much in common with the SMA proper. Both areas project to the primary motor cortex and directly to the spinal cord 1., 8., 52.
Conclusions
The data presented in this review help to clarify the location and boundaries of the premotor areas in the frontal lobe of humans. For many of these areas, there is a clear correspondence with a specific premotor area in the monkey. For other regions, such as the motor fields in inferior frontal cortex, the correspondence with areas in the monkey brain remains to be established. Two regions have generally been considered to be motor fields: the rostral part of area 6 on the medial wall of the
Acknowledgements
Our work is supported by the Veterans Administration Medical Research and Rehabilitation Research and Development Services (PL Strick), and United States Public Health Service grant NS24328 (PL Strick).
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
•of special interest
••of outstanding interest
References (93)
- et al.
Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized ‘premotor’ areas
Brain Res
(1979) - et al.
Spatial distribution of cingulate cells projecting to the primary, supplementary, and pre-supplementary motor areas: a retrograde multiple labeling study in the macaque monkey
Neurosci Res
(2001) - et al.
The effect of stimulus-response compatibility on cortical motor activation
Neuroimage
(2001) - et al.
Stimulus-response incompatibility activates cortex proximate to three eye fields
Neuroimage
(2001) - et al.
The effect of switching between sequential and repetitive movements on cortical activation
Neuroimage
(2000) - et al.
Transient neural activity in the medial superior frontal gyrus and precuneus time locked with attention shift between object features
Neuroimage
(1999) - et al.
Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed
Cogn Brain Res
(2001) - et al.
Subregions within the supplementary motor area activated at different stages of movement preparation and execution
Neuroimage
(1999) - et al.
An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli
Pain
(2000) - et al.
Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks
Neuroimage
(2001)
Corticocortical inputs to the dorsal and ventral aspects of the premotor cortex of macaque monkeys
Neurosci Res
Attention versus intention in the primate premotor cortex
Neuroimage
Correlations between reaction time and cerebral blood flow during motor preparation
Neuroimage
Pattern of cytochrome oxidase activity in frontal agranular cortex of the macaque monkey
Behav Brain Res
The organization of the cortical motor system: new concepts
Electroencephalogr Clin Neurophysiol
Spatial maps for the control of movement
Curr Opin Neurobiol
Visuomotor neurons: ambiguity of the discharge or ‘motor’ perception?
Int J Psychophysiol
Language within our grasp
Trends Neurosci
Premotor cortex activation during observation and naming of familiar tools
Neuroimage
Brain activation during silent word generation evaluated with functional MRI
Brain Lang
A common language network for comprehension and production: a contribution to the definition of language epicenters with PET
Neuroimage
Cortical correlates of gesture processing: clues to the cerebral mechanisms underlying apraxia during the imitation of meaningless gestures
Neuroimage
The origin of corticospinal projections from the premotor areas in the frontal lobe
J Neurosci
Medial wall motor areas: a review of their location and functional activation
Cereb Cortex
Multiple nonprimary motor areas in the human cortex
J Neurophysiol
Functional neuroanatomy of the primate isocortical motor system
Anat Embryol
Architecture of superior and medial area 6 and the adjacent cingulate cortex in the macaque monkey
J Comp Neurol
Coplanar Stereotaxic Atlas of the Human Brain
Patterns of localization in precentral and ‘supplementary’ motor areas and their relation to the concept of a premotor area
Assoc Res Nerv Ment Disord
Spinal cord terminations of the medial wall motor areas in macaque monkeys
J Neurosci
Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere
J Neurosci
Prefrontal connections of medial motor areas in the rhesus monkey
J Comp Neurol
Corticocortical connections of area F3 (SMA-proper) and area F6 (Pre-SMA) in the macaque monkey
J Comp Neurol
Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe
J Comp Neurol
Neuronal activity in medial frontal cortex during learning of sequential procedures
J Neurophysiol
Effects of local inactivation of monkey medial frontal cortex in learning of sequential procedures
J Neurophysiol
Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements
J Neurophysiol
Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study
J Neurophysiol
Presupplementary motor area activation during sequence learning reflects visuo-motor association
J Neurosci
Role for cells in the presupplementary motor area in updating motor plans
Proc Natl Acad Sci USA
Activation of the dorsal premotor cortex and pre-supplementary motor area of humans during an auditory conditional motor task
J Neurophysiol
What and when: parallel and convergent processing in motor control
J Neurosci
Sustained activity in the medial wall during working memory delays
J Neurosci
Medial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate
J Neurophysiol
Partially overlapping neural networks for real and imagined hand movements
Cereb Cortex
Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow
Brain
Cited by (1015)
Probing intrahemispheric interactions with a novel dual-site TMS setup
2024, Clinical NeurophysiologyPMd and action preparation: bridging insights between TMS and single neuron research
2023, Trends in Cognitive SciencesLinking individual variability in functional brain connectivity to polygenic risk in major depressive disorder
2023, Journal of Affective DisordersThe predictive value of cortical activity during motor imagery for subacute spinal cord injury-induced neuropathic pain
2023, Clinical Neurophysiology