Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties

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The dorsal and ventral premotor areas, together with the primary motor cortex, are believed to have major roles in preparing and executing limb movements. Recent studies have expanded our knowledge of the dorsal and ventral premotor areas, which occupy the lateral part of area 6 in the frontal cortex. It is becoming clear that these two premotor areas, through involvement in distinct cortical networks, take part in unique aspects of motor planning and decision making. New lines of evidence also implicate the lateral premotor areas in planning motor behavior and selecting actions.

Introduction

To achieve voluntary actions, many motor areas in the medial and lateral frontal cortex must work cooperatively. In this review, we examine the role of the lateral premotor cortex in multiple stages of controlling motor behavior (Figure 1). At the stage of preparing and executing planned movements, neurons in the lateral premotor cortex are engaged in a manner that is not readily distinguishable from that of neurons in the primary motor cortex (M1). However, when we consider behavioral stages that occur before motor preparation, neuronal activity in the premotor areas seems to differ from that in the M1. During the past two years, studies have revealed unique aspects of neuronal activity in the premotor cortex at two stages: planning actions based on available information, and selecting appropriate actions from potential options. Interestingly, neuronal activity exhibits distinct properties in the dorsal and ventral premotor areas. Taking this into account, along with the anatomical connectivity that characterizes each area, we propose a new concept — direct versus indirect sensorimotor processing — as a core aspect of operations that involve these areas.

Section snippets

Cortical non-primary motor areas

At least seven non-primary motor areas involved in controlling arm movements, such as reaching and grasping, have been delineated in the frontal cortex of primates (Figure 2) [1, 2, 3••]. Of these, four are in Brodmann's area 6: the dorsal and ventral premotor areas (PMd and PMv), which are caudal to the arcuate sulcus and rostral to the M1, and the supplementary motor and pre-supplementary motor areas (SMA and pre-SMA), which are in the superior frontal gyrus. In addition, there are three

Involvement of the PMd and PMv in motor preparation and execution

Involvement of the PMd in motor preparation was first described as set-related activity, which is defined as a neuronal activity that starts once a forthcoming movement is instructed and continues until the movement is executed [6, 7]. According to this definition, if a visual cue is used to instruct motor preparation to capture a target in space, PMd activity reflects the motor significance of the instructional cue rather than its sensory or attentional significance [8]. Subsequently, it was

Action planning

Motor planning is necessary to decide what to do and which action to perform, and the participation of the premotor areas, especially the PMd, is crucial for this process. Here, the term ‘planning’ refers to a process in which multiple sets of information on actions are collected and integrated to establish an intended action.

A useful approach in examining this process experimentally is to give multiple partial motor instructions successively — that is, to require subjects to retrieve multiple

Decision for action selection

Several studies have examined the involvement of the premotor areas in the process of selecting an appropriate action from multiple options. Ohbayashi et al. [36] investigated PMd involvement in decision making for saccadic eye movements. In the task, the first and second cues instructed the two potential saccadic targets, and the third cue indicated whether the saccades should be made in the visually displayed or reversed order. They found that PMd neurons temporarily hold information on the

Dorsal and ventral premotor areas are involved in different networks

Sanides [41] proposed a theory on the evolution of the structure of the cerebral cortex and its phylogenetic differentiation, identifying three protogradations (directions of progressive cortical differentiation) in the frontal cortex of primates (Figure 2): the medial, originating in the cingulate gyrus; the lateral, originating in the insular cortex; and the most recent protogradation in the evolution, originating in the central sulcus. In this schema, the medial and lateral protogradations

Direct comparison of neuronal activity in the PMv and PMd during action performance

Because the PMd and PMv are involved in distinct networks, it is possible that their functional roles in motor control are, at least in part, fundamentally different. Indeed, several studies have reported functional differences between the PMd and PMv. Boussaoud and Wise [62, 63] examined activity in PMd and PMv neurons while monkeys were performing a behavioral task that dissociated the representation for the visuospatial position of a cue from the visuomotor representation of arm movements.

Direct versus indirect sensorimotor processing in the PMv and PMd

Taking into consideration all of the reports discussed in previous sections, we propose that a core aspect of the functional differences between the PMd and PMv can be explained in terms of direct versus indirect sensorimotor processing. Figure 4a illustrates the concept of neuronal processes that operate in direct sensorimotor processing in the PMv. This schematic diagram shows the basic operation of a neuronal circuit that receives sensory inputs that inform the animal about a target, and

Conclusions

The PMd and PMv, which have distinct evolutionary origins, constitute largely separate cortical networks that are interconnected by different regions of the prefrontal cortex and parietal cortex. As inferred from neuroanatomical considerations, the PMd and PMv are involved in different aspects of selecting and planning motor behavior, and in preparing and executing movements. We propose that the functional specificity of the PMd and PMv can be explained by a cardinal concept of direct versus

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by the 21st Century Center of Excellence Program from the Japanese Society for the Promotion of Science, a Grant-in-Aid for Scientific Research on Priority Areas — Integrative Brain Research — from the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT; 18019032 and 16067101), and a Grant-in-Aid for Young Scientists (A) from MEXT (18680035).

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