Review PaperThe role of supplementary eye field in goal-directed behavior
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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2021, Clinical Neurology and NeurosurgeryCitation Excerpt :SCEF has also been more broadly referred to as a region within the premotor cortex (PMC), or area 6 [36]. Current literature regarding the precise function of SCEF is not clear, but demonstrates that it is activated during observation of others’ movements and imagining ones’ own self performing a movement, and it also participates in a wide range of different oculomotor functions related to the selection, monitoring and control of visual behavior [37]. SCEF may be a critical frontal area involved in the dorso-dorsal pathway, which plays a role in online visuospatial processing of variable affordances [11,38].
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2021, NeuroImage: ClinicalCitation Excerpt :Finally, we also found that individuals with schizophrenia had reduced mean inhibitory influence from the FEF to the SEF and to the superior colliculus. This reduced inhibitory influence from the FEF may reflect less propagated information about activity in visual, movement, and fixation neurons in FEF, information that the SEF uses to assess trial-by-trial proactive control demands (Stuphorn, 2015) and that contributes to movement plans in the superior colliculus (Matsumoto et al., 2018). Broadly, the finding that effective connectivity across the task showed widespread alterations in individuals with schizophrenia aligns with our ROI analyses that revealed greater activity on no-step trials in individuals with schizophrenia compared to controls, resulting in reduced differential activity between redirect and no-step trials, and suggesting a broad alteration in task-related activity.
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2018, Microvascular ResearchCitation Excerpt :The SEF plays a critical role in the saccadic eye movements (Fujii et al., 2002; Parton et al., 2007). Besides, the SEF is involved in goal-directed behavior (Stuphorn, 2015). In addition, the SEF plays an important role in proactive preparation of sequential saccades (Sharika et al., 2013).
Inactivation of Medial Frontal Cortex Changes Risk Preference
2018, Current BiologyCitation Excerpt :Instead, it suggests that SEF activity contributes to self-control by suppressing automatic, but maladaptive, responses and promoting behavior that maximizes long-term reward. Such a role would be consistent with the well-known contribution of SEF to other forms of executive control [5, 51]. In conclusion, our results demonstrate for the first time the causal role of SEF in mediating the effect of risk preference on decisions under uncertainty.
Special issue: Neural basis of adaptive control
2015, Journal of Physiology Paris