Elsevier

Journal of Physiology-Paris

Volume 109, Issues 1–3, February–June 2015, Pages 118-128
Journal of Physiology-Paris

Review Paper
The role of supplementary eye field in goal-directed behavior

https://doi.org/10.1016/j.jphysparis.2015.02.002Get rights and content

Highlights

  • SEF’s role in various control and monitoring functions has been studied in monkeys.

  • SEF signals the context-dependent action value of possible oculomotor behaviors.

  • SEF does not have the ability to directly select eye movements.

  • Instead, action value signals influence the activity in primary oculomotor areas.

  • Evaluation signals in SEF allow updating of the contextual action value signals.

Abstract

The medial frontal cortex has been suggested to play a role in the control, monitoring, and selection of behavior. The supplementary eye field (SEF) is a cortical area within medial frontal cortex that is involved in the regulation of eye movements. Neurophysiological studies in the SEF of macaque monkeys have systematically investigated the role of SEF in various behavioral control and monitoring functions. Inhibitory control studies indicate that SEF neurons do not directly participate in the initiation of eye movements. Instead, recent value-based decision making studies suggest that the SEF participates in the control of eye movements by representing the context-dependent action values of all currently possible oculomotor behaviors. These action value signals in SEF would be useful in directing the activity distribution in more primary oculomotor areas, to guide decisions towards behaviorally optimal choices. SEF also does not participate in the fast, inhibitory control of eye movements in response to sudden changes in the task requirements. Instead, it participates in the long-term regulation of oculomotor excitability to adjust the speed-accuracy tradeoff. The context-dependent control signals found in SEF (including the action value signals) have to be learned and continuously adjusted in response to changes in the environment. This is likely the function of the large number of different response monitoring and evaluation signals in SEF. In conclusion, the overall function of SEF in goal-directed behavior seems to be the learning of context-dependent rules that allow predicting the likely consequences of different eye movements. This map of action value signals could be used so that eye movements are selected that best fulfill the current long-term goal of the agent.

Introduction

Voluntary or goal-directed behavior requires the ability to flexibly choose a behavioral response that fits the current overall goal of the organism and the current state of the environment. However, the state of the environment can change and actions might have an unanticipated effect. Accordingly, the organism has to constantly monitor the outcome of each action. If the selected responses do not match the requirements of the environment or the overall behavioral goal, the selection process needs to be adjusted appropriately. Thus, goal directed behavior requires to the ability to freely select behavior, to monitor and evaluate behavior, and to control behavior. For successful goal-directed behavior all three of these functions are necessary.

In primates, a large neuronal network is involved in generating goal-directed behavior, including frontal and parietal cortical regions, as well as a number of subcortical nuclei that are connected with these cortical areas. Among these different brain regions, the medial frontal cortex (MFC) has long been suggested to be of central importance for response selection, evaluation, and control. MFC consists of a number of different areas along the medial frontal cortex, including a group of cortical areas that have long been recognized as playing a role in higher-order motor control. These areas are the anterior cingulate cortex (ACC), the pre-supplementary motor area (pre-SMA), supplementary motor area (SMA), and the supplementary eye field (SEF). These motor-related areas contain neurons that are active during movements of various body parts. Some of these areas, such as the ACC and the pre-SMA, seem to be involved in the control of many different types of motor responses (Sumner et al., 2007). In contrast, the SMA seems to be specialized in the control of skeletomotor movements, such as movements of the arm and the hand (Fujii et al., 2002). The pre-SMA and SMA, which are reciprocally connected, differ in their connectivity, with pre-SMA connected to prefrontal cortex but not motor regions, and SMA to motor regions but not prefrontal cortex (Johansen-Berg et al., 2004, Luppino et al., 1991, Tanji, 1996).

The SEF is a region adjacent to the SMA that can be seen as an oculomotor extension of the SMA. SEF has been suggested to be involved in the supervisory control of eye movements (Stuphorn and Schall, 2002). SEF has appropriate connections for such a role, since it receives input from areas that represent value, such as the OFC and the amygdala, and from regions that represent contextual cognitive signals, such as dorsolateral prefrontal cortex (Ghashghaei et al., 2007, Huerta and Kaas, 1990). Through these inputs, SEF receives information about the state of the environment, including the presence of possible behavioral goals, and the set of behavioral rules that currently determine the relationship between actions and their outcomes. SEF projects in turn to oculomotor areas, such as frontal eye field (FEF), lateral intraparietal (LIP) cortex, and superior colliculus (SC) (Huerta and Kaas, 1990). This set of anatomical connections indicates that SEF is in a unique position to control and regulate the selection and generation of oculomotor behavior.

Section snippets

Experimental evidence for the function of SEF

The principles governing goal-directed behavior seem to be similar across different effector systems (Stuphorn and Schall, 2002). Understanding the role of SEF in the control of goal-directed eye movements might therefore allow general insights in the role of MFC in the control of more complex behavior. With this goal in mind, a series of experiments was performed to study the function of SEF in the selection, evaluation, and control of saccadic eye movements. In the following, we will first

Overall function of SEF

Our research in SEF has demonstrated that this brain region participates in the selection, monitoring, and control of oculomotor behavior. The fact that this one cortical area in the dorsomedial frontal cortex is involved in such a wide range of different functions leads to the question of their relationship and whether they all can be explained as components of one overarching function.

An important difference between SEF and other oculomotor areas is the fact that SEF neurons do not have the

Conclusions

The medial frontal cortex has been suggested to play a role in the control, monitoring, and selection of behavior. Evidence from different recording studies in the SEF of macaque monkeys has systematically investigated the role of SEF in these various suggested behavioral functions. SEF neurons participate in the selection of eye movements by representing the context-dependent action value of various possible oculomotor behaviors (So and Stuphorn, 2010). SEF does not have the ability to

Acknowledgement

This work was supported by the National Eye Institute through Grant R01-EY019039 to VS.

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