Supplementary eye field

Last updated
Figure 1. Motor Cortex of the Monkey Brain: Pictured above are the approximate locations of the SEF and FEF in the monkey brain which we know today. Motor Cortex monkey.jpg
Figure 1. Motor Cortex of the Monkey Brain: Pictured above are the approximate locations of the SEF and FEF in the monkey brain which we know today.

Supplementary eye field (SEF) is the name for the anatomical area of the dorsal medial frontal lobe of the primate cerebral cortex that is indirectly involved in the control of saccadic eye movements. Evidence for a supplementary eye field was first shown by Schlag, and Schlag-Rey. [1] Current research strives to explore the SEF's contribution to visual search and its role in visual salience. [2] [3] The SEF constitutes together with the frontal eye fields (FEF), the intraparietal sulcus (IPS), and the superior colliculus (SC) one of the most important brain areas involved in the generation and control of eye movements, particularly in the direction contralateral to their location. [2] [4] Its precise function is not yet fully known. [2] Neural recordings in the SEF show signals related to both vision and saccades somewhat like the frontal eye fields and superior colliculus, but currently most investigators think that the SEF has a special role in high level aspects of saccade control, like complex spatial transformations, [5] learned transformations, [6] and executive cognitive functions. [7] [8]

Contents

History (research)

Figure 2. Ferrier's Monkey Brain Map (1874). The highlighted area labeled 'EF' is the area he observed to cause eye and head movements when electrically stimulated. Dr. David Ferrier's Original Eye Field Brain Map in Monkeys.png
Figure 2. Ferrier's Monkey Brain Map (1874). The highlighted area labeled 'EF' is the area he observed to cause eye and head movements when electrically stimulated.

In 1874, David Ferrier, a Scottish neurologist first described the frontal eye fields (FEF). He noted that unilateral electrical stimulation of the frontal lobe of macaque monkeys caused "turning of the eyes and head to the opposite side" (Fig. 2). [9] The brain area allotted to the FEF by Ferrier's original map was actually quite large and also encompassed the area which we now call the SEF. A century's worth of experimental findings following Ferrier's work have led to shrinking the FEF's size. [10]

During the 1950s, surgical treatment of epileptic patients was being conducted. Neurosurgeons were removing lesions and other parts of the brain thought to be involved in causing the patient's seizures. Treatment of these epileptic patients lead to the discovery of many new brain areas by observant neurosurgeons concerned with the post-surgical implications of removing sections of the brain. Through electrical stimulation studies an area called the supplementary motor area (SMA) was observed and documented by the neurosurgeon Wilder Penfield in 1950. [11] [12] As Penfield had noted the induction of gaze shifts by stimulation of the rostral part of the SMA, another eye field's existence was postulated.

In 1987, the SEF was finally characterized by Schlag and Schlag-Rey as an area where low intensity electrical stimulation could evoke saccades, similar to the FEF. It was named as such to complement the SMA's name. [1]

Characteristics

Location

Figure 3. Brodmann Brain Map: The SEF is located in the rostral supplementary motor area which corresponds to Area 6 in the above map. For reference, the FEF is located in Area 8. Gray726-Brodman.svg
Figure 3. Brodmann Brain Map: The SEF is located in the rostral supplementary motor area which corresponds to Area 6 in the above map. For reference, the FEF is located in Area 8.

The eye field originally defined by Ferrier's map of the frontal cortex extended medially to the dorsal surface of the brain (Fig. 2). [9] But the FEF proper has since shrunk into the rostral back of the arcuate sulcus (Fig. 1). [10] Experimenters have since established that the FEF and SEF are two separate and distinct brain areas responsible for saccade initiation through cerebral blood flow, and subdural electrode array studies. [11] [13] [14] [15]

In humans, the SEF is located in the rostral supplementary motor area (SMA). [16] It is located in Brodmann area 6 (BA6) which corresponds to area F7, the premotor cortex. [17] Based on single unit recording and microstimulation it has been established that the SEF is caudally contiguous with the parts of the SMA which represent orofacial, and forelimb movements. [1] [18]

The FEF is located in Brodmann area 8 which is just anterior to the premotor cortex (BA6) (Fig. 3). [19]

Role

As opposed to the FEF, the SEF plays an indirect but executive role in saccade initiation. For example, the activity of SEF neurons is not sufficient to control saccade initiation in macaque monkeys performing stop signal go/no-go tasks. [3] In this kind of task a trained monkey is to make a particular response (in this case move its eyes, or produce a saccade) to a stimulus on a screen such as a flashing dot. For the go-task, the monkey is to look at the dot. But for the no-go task, the go signal will appear and be followed by the no-go signal, testing whether the saccade initiation can be inhibited. [20]

In other words, the SEF does not immediately or directly contribute to saccade initiation. But, the SEF is thought to improve saccade production by using prior knowledge of anticipated task requirements to influence saccadic eye movements. It does so by balancing gaze holding and gaze shifting actions, yielding a modest improvement in performance in stop signal tasks by delaying saccade initiation when necessary. [2] [3] It can be thought that the FEF does the driving part of saccade initiation, while the SEF acts as a backseat passenger, advising the driver as to what to do based on past insights. The SEF has recently been found to encode reward prediction error, suggesting that the SEF may actively evaluate decisions based on a value system on an occulomotor basis, independent of other brain regions. [21]

Significance

The visual system is sensitive to sudden change. [22] If something distracting occurs while a person is performing a task—reading a newspaper, for example—this immediately captures one's attention. [23] [24] [25] This sudden shift can be a distraction but it has been also thought to be a reflex of great importance as identifying and reacting to environmental changes quickly (when needed) can be imperative to survival. [24] [26] [27] [28] [29] Saccadic latency, the time delay between the appearance of a target and the initiation of a saccade, is an important parameter for learning which occulomotor neurons and structures of the brain play what specific roles in saccade initiation. [30] [31] There is much research being conducted on the role of SEF in determining visually salient objects and occurrences, using saccadic latency as the parameter of interest. [2] [26] [32] [33] [34]

SEF activity has been found to govern decisions in smooth pursuit but not the decision itself. [35]

Sensory processes

The SEF responds to auditory stimuli as well as visual stimuli. [20] Visual responses from the SEF happen later and are much weaker than that observed in the FEF, though. SEF neurons also exhibit non-retinal modulation including anticipation and reward prediction. [3] [36]

Methodology of study

Finding the SEF

The SEF was defined by the Schlags as a region where low currents (<50μA) evoke saccades. It is still found using this characterization as well as the known neighboring anatomy (Fig. 1). [1] [10]

Monkey models

SEF research is conducted mainly in monkey models. Typically trained rhesus macaque monkeys are used and surgically implanted with recording chambers. In this fashion, spike and local field potential (LFP) data can be acquired from SEF neurons, using microelectrodes in the recording chamber. Eye movements can also be monitored using eye-tracking camera equipment. [2]

Experiments obviously vary, but to give an example: the monkey might be made to partake in a color visual search task, sitting in front of a computer screen. The monkey would look at a point on the screen which would change from filled in to open at the same time which a colored point of "opposite" color appears on the screen. The monkey would be rewarded for looking at a new spot—"for making a single saccade"—within 2000 ms and then fixating on the spot for 500 ms. Varied tasks such as these are used and data is analyzed to determine the SEF's role in saccade initiation, visual saliency, etc. [2] [3]

See also

Related Research Articles

Visual cortex Region of the brain that processes visual information

The visual cortex of the brain is the area of the cerebral cortex that processes visual information. It is located in the occipital lobe. Sensory input originating from the eyes travels through the lateral geniculate nucleus in the thalamus and then reaches the visual cortex. The area of the visual cortex that receives the sensory input from the lateral geniculate nucleus is the primary visual cortex, also known as visual area 1 (V1), Brodmann area 17, or the striate cortex. The extrastriate areas consist of visual areas 2, 3, 4, and 5.

Saccade Eye movement

A saccade is a quick, simultaneous movement of both eyes between two or more phases of fixation in the same direction. In contrast, in smooth pursuit movements, the eyes move smoothly instead of in jumps. The phenomenon can be associated with a shift in frequency of an emitted signal or a movement of a body part or device. Controlled cortically by the frontal eye fields (FEF), or subcortically by the superior colliculus, saccades serve as a mechanism for fixation, rapid eye movement, and the fast phase of optokinetic nystagmus. The word appears to have been coined in the 1880s by French ophthalmologist Émile Javal, who used a mirror on one side of a page to observe eye movement in silent reading, and found that it involves a succession of discontinuous individual movements.

Superior colliculus

The superior colliculus is a structure lying on the roof of the mammalian midbrain. In non-mammalian vertebrates, the homologous structure is known as the optic tectum, or optic lobe. The adjective form tectal is commonly used for both structures.

Motor cortex Region of the cerebral cortex

The motor cortex is the region of the cerebral cortex involved in the planning, control, and execution of voluntary movements. Classically, the motor cortex is an area of the frontal lobe located in the posterior precentral gyrus immediately anterior to the central sulcus.

The pars reticulata (SNpr) is a portion of the substantia nigra and is located lateral to the pars compacta. Most of the neurons that project out of the pars reticulata are inhibitory GABAergic neurons.

Microsaccades are a kind of fixational eye movement. They are small, jerk-like, involuntary eye movements, similar to miniature versions of voluntary saccades. They typically occur during prolonged visual fixation, not only in humans, but also in animals with foveal vision. Microsaccade amplitudes vary from 2 to 120 arcminutes. The first empirical evidence for their existence was provided by Robert Darwin, the father of Charles Darwin.

Smooth pursuit Type of eye movement used for closely following a moving object

In the scientific study of vision, smooth pursuit describes a type of eye movement in which the eyes remain fixated on a moving object. It is one of two ways that visual animals can voluntarily shift gaze, the other being saccadic eye movements. Pursuit differs from the vestibulo-ocular reflex, which only occurs during movements of the head and serves to stabilize gaze on a stationary object. Most people are unable to initiate pursuit without a moving visual signal. The pursuit of targets moving with velocities of greater than 30°/s tends to require catch-up saccades. Smooth pursuit is asymmetric: most humans and primates tend to be better at horizontal than vertical smooth pursuit, as defined by their ability to pursue smoothly without making catch-up saccades. Most humans are also better at downward than upward pursuit. Pursuit is modified by ongoing visual feedback.

Frontal eye fields Region of the frontal cortex of the brain

The frontal eye fields (FEF) are a region located in the frontal cortex, more specifically in Brodmann area 8 or BA8, of the primate brain. In humans, it can be more accurately said to lie in a region around the intersection of the middle frontal gyrus with the precentral gyrus, consisting of a frontal and parietal portion. The FEF is responsible for saccadic eye movements for the purpose of visual field perception and awareness, as well as for voluntary eye movement. The FEF communicates with extraocular muscles indirectly via the paramedian pontine reticular formation. Destruction of the FEF causes deviation of the eyes to the ipsilateral side.

Premotor cortex

The premotor cortex is an area of the motor cortex lying within the frontal lobe of the brain just anterior to the primary motor cortex. It occupies part of Brodmann's area 6. It has been studied mainly in primates, including monkeys and humans. The functions of the premotor cortex are diverse and not fully understood. It projects directly to the spinal cord and therefore may play a role in the direct control of behavior, with a relative emphasis on the trunk muscles of the body. It may also play a role in planning movement, in the spatial guidance of movement, in the sensory guidance of movement, in understanding the actions of others, and in using abstract rules to perform specific tasks. Different subregions of the premotor cortex have different properties and presumably emphasize different functions. Nerve signals generated in the premotor cortex cause much more complex patterns of movement than the discrete patterns generated in the primary motor cortex.

Supplementary motor area Midline region in front of the motor cortex of the brain

The supplementary motor area (SMA) is a part of the cerebral cortex of primates that contributes to the control of movement. It is located on the midline surface of the hemisphere just in front of the primary motor cortex leg representation. In monkeys the SMA contains a rough map of the body. In humans the body map is not apparent. Neurons in the SMA project directly to the spinal cord and may play a role in the direct control of movement. Possible functions attributed to the SMA include the postural stabilization of the body, the coordination of both sides of the body such as during bimanual action, the control of movements that are internally generated rather than triggered by sensory events, and the control of sequences of movements. All of these proposed functions remain hypotheses. The precise role or roles of the SMA is not yet known.

Premovement neuronal activity in neurophysiological literature refers to neuronal modulations that alter the rate at which neurons fire before a subject produces movement. Through experimentation with multiple animals, predominantly monkeys, it has been shown that several regions of the brain are particularly active and involved in initiation and preparation of movement. Two specific membrane potentials, the bereitschaftspotential, or the BP, and contingent negative variation, or the CNV, play a pivotal role in premovement neuronal activity. Both have been shown to be directly involved in planning and initiating movement. Multiple factors are involved with premovement neuronal activity including motor preparation, inhibition of motor response, programming of the target of movement, closed-looped and open-looped tasks, instructed delay periods, short-lead and long-lead changes, and mirror motor neurons.

Medial dorsal nucleus

The medial dorsal nucleus is a large nucleus in the thalamus.

Posterior parietal cortex

The posterior parietal cortex plays an important role in planned movements, spatial reasoning, and attention.

The lateral intraparietal cortex is found in the intraparietal sulcus of the brain. This area is most likely involved in eye movement, as electrical stimulation evokes saccades of the eyes. It is also thought to contribute to working memory associated with guiding eye movement, examined using a delayed saccade task described below:

  1. A subject focuses on a fixation point at the center of a computer screen.
  2. A target is presented at a peripheral location on the screen.
  3. The target is removed and followed by a variable-length delay period.
  4. The initial focus point in the middle of the screen is removed.
  5. The subject's task is to make a saccade to the location of the target.
Vivien Casagrande American ophthalmologist

Vivien Alice Casagrande was a professor in the Department of Cell and Developmental Biology at the Vanderbilt University Medical Center.

The anti-saccade (AS) task is a gross estimation of injury or dysfunction of the frontal lobe, by assessing the brain’s ability to inhibit the reflexive saccade. Saccadic eye movement is primarily controlled by the frontal cortex.

Doug Crawford Canadian neuroscientist

John Douglas (Doug) Crawford is a Canadian neuroscientist and the scientific director of the Vision: Science to Applications(VISTA) program. He is a professor at York University where he holds the Canada Research Chair in Visuomotor Neuroscience and the title of Distinguished Research Professor in Neuroscience.

Peter Schiller (neuroscientist) Neuroscientist

Peter H. Schiller is a professor emeritus of Neuroscience in the Department of Brain and Cognitive Sciences at the Massachusetts Institute of Technology (MIT). He is well known for his work on the behavioral, neurophysiological and pharmacological studies of the primate visual and oculomotor systems.

Michael E. Goldberg, also known as Mickey Goldberg, is an American neuroscientist and David Mahoney Professor at Columbia University. He is known for his work on the mechanisms of the mammalian eye in relation to brain activity. He served as president of the Society for Neuroscience from 2009 to 2010.

The corollary discharge theory (CD) of motion perception helps understand how the mind can detect motion through the visual system, even though the body is not moving. When a signal is sent from the motor cortex of the brain to the eye muscles, a copy of that signal is sent through the brain as well. The brain does this in order to distinguish real movements in the visual world from our own body and eye movement. The original signal and copy signal are then believed to be compared somewhere in the brain. Such a structure has not yet been identified, but it is believed to be the Medial Superior Temporal Area (MST). The original signal and copy need to be compared in order to determine if the change in vision was caused by eye movement or movement in the world. If the two signals cancel then no motion is perceived, but if they do not cancel then the residual signal is perceived as motion in the real world. Without a corollary discharge signal, the world would seem to spin around every time the eyes moved. It is important to note that corollary discharge and efference copy are sometimes used synonymously, they were originally coined for much different applications, with corollary discharge being used in a much broader sense.

References

  1. 1 2 3 4 Schlag J, Schlag-Rey M.(1987) Evidence for a supplementary eye field. J Neurophysiol. 57(1):179-200.
  2. 1 2 3 4 5 6 7 Purcell, B. A., Weigand, P. K., & Schall, J. D. (2012). Supplementary Eye Field during Visual Search: Salience, Cognitive Control, and Performance Monitoring. Journal of Neuroscience, 32(30), 10273-10285. doi: Doi 10.1523/Jneurosci.6386-11.2012
  3. 1 2 3 4 5 Stuphorn V, Brown JW, Schall JD. Role of Supplementary Eye Field in Saccade Initiation: Executive, Not Direct, Control. J Neurophysiol. Feb 2010;103(2):801-816
  4. ↑ Emeric, E. E., Leslie, M., Pouget, P., & Schall, J. D. (2010). Performance monitoring local field potentials in the medial frontal cortex of primates: supplementary eye field. Journal of neurophysiology, 104(3), 1523-1537.
  5. ↑ Olson CR, Gettner SN. (1995) Object-centered direction selectivity in the macaque supplementary eye field. Science. 269(5226):985-8.
  6. ↑ Chen LL, Wise SP. (1995) Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol. 73(3):1101-21.
  7. ↑ Stuphorn V, Schall JD. (2006) Executive control of countermanding saccades by the supplementary eye field. Nat Neurosci. 9(7):925-31.
  8. ↑ Husain, M., Parton, A., Hodgson, T. L., Mort, D., & Rees, G. (2002). Self-control during response conflict by human supplementary eye field. Nature neuroscience, 6(2), 117-118.
  9. 1 2 3 Ferrier, D. (1874). Experiments on the Brain of Monkeys.--No. I. Proceedings of the Royal Society of London (1854-1905). 23: 409-430.
  10. 1 2 3 Rockland, K. S., Kaas, J. H., & Peters, A. (Eds.). (1997). Cerebral Cortex: Volume 12: Extrastriate Cortex in Primates (Vol. 12, pp. 584-585). Springer.
  11. 1 2 Penfield, W. (1950). The supplementary motor area in the cerebral cortex of man. European Archives of Psychiatry and Clinical Neuroscience, 185(6), 670-674.
  12. ↑ Penfield, W. and Welch, K (1951). "The supplementary motor area of the cerebral cortex: A clinical and experimental study". Am. Med. Ass. Arch. Neurol. Psychiat. 66: 289–317.
  13. ↑ Melamed, E., & Larsen, B. (1979). Cortical activation pattern during saccadic eye movements in humans: localization by focal cerebral blood flow increases. Annals of neurology, 5(1), 79-88.
  14. ↑ Fried, I., Katz, A., McCarthy, G., Sass, K. J., Williamson, P., Spencer, S. S., & Spencer, D. D. (1991). Functional organization of human supplementary motor cortex studied by electrical stimulation. The Journal of Neuroscience, 11(11), 3656-3666.
  15. ↑ Lim, S. H., Dinner, D. S., Pillay, P. K., Lüders, H., Morris, H. H., Klem, G., ... & Awad, I. A. (1994). Functional anatomy of the human supplementary sensorimotor area: results of extraoperative electrical stimulation. Electroencephalography and clinical Neurophysiology, 91(3), 179-193.
  16. ↑ Müller-Forell, W. S. (Ed.). (2002). Imaging of orbital and visual pathway pathology. Springer.
  17. ↑ Luppino, G., Rozzi, S., Calzavara, R., & Matelli, M. (2003). Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey (Fig. 3). European Journal of Neuroscience, 17(3), 559-578.
  18. ↑ Schall, J. D. (1991). Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. Journal of Neurophysiology, 66(2), 530-558.
  19. ↑ Amiez, C., & Petrides, M. (2009). Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Progress in Neurobiology, 89(2), 220-230.
  20. 1 2 Stuphorn, V., Taylor, T. L., & Schall, J. D. (2000). Performance monitoring by the supplementary eye field. Nature, 408(6814), 857-860.
  21. ↑ So, N., & Stuphorn, V. (2012). Supplementary eye field encodes reward prediction error. The Journal of Neuroscience, 32(9), 2950-2963.
  22. ↑ Gottlieb, J. P., Kusunoki, M., & Goldberg, M. E. (1998). The representation of visual salience in monkey parietal cortex. Nature, 391(6666), 481-484.
  23. ↑ Breitmeyer, B. G., & Ganz, L. (1976). Implications of sustained and transient channels for theories of visual pattern masking, saccadic suppression, and information processing. Psychological Review, 83(1), 1.
  24. 1 2 Schall, J. D. (2001). Neural basis of deciding, choosing and acting. Nature Reviews Neuroscience, 2(1), 33-42.
  25. ↑ Harel, J., Koch, C., & Perona, P. (2006). Graph-based visual saliency. In Advances in neural information processing systems (pp. 545-552).
  26. 1 2 Schall, J. D., & Thompson, K. G. (1999). Neural selection and control of visually guided eye movements. Annual Review of Neuroscience, 22(1), 241-259.
  27. ↑ Edelman, G. M. (1987). Neural Darwinism: The theory of neuronal group selection. Basic Books.
  28. ↑ Morris, J. S., Friston, K. J., & Dolan, R. J. (1997). Neural responses to salient visual stimuli. Proceedings of the Royal Society of London. Series B: Biological Sciences, 264(1382), 769-775.
  29. ↑ Elazary, L., & Itti, L. (2008). Interesting objects are visually salient. Journal of Vision, 8(3).
  30. ↑ Gaymard, B., Ploner, C. J., Rivaud, S., Vermersch, A. I., & Pierrot-Deseilligny, C. (1998). Cortical control of saccades. Experimental Brain Research, 123(1-2), 159-163.
  31. ↑ Grosbras, M. H., Leonards, U., Lobel, E., Poline, J. B., LeBihan, D., & Berthoz, A. (2001). Human cortical networks for new and familiar sequences of saccades. Cerebral Cortex, 11(10), 936-945.
  32. ↑ Shook, B. L., Schlag-Rey, M., & Schlag, J. (1990). Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. Journal of Comparative Neurology, 301(4), 618-642.
  33. ↑ Thompson, K. G., Bichot, N. P., & Schall, J. D. (1997). Dissociation of visual discrimination from saccade programming in macaque frontal eye field. Journal of neurophysiology, 77(2), 1046-1050.
  34. ↑ Sato, T., Murthy, A., Thompson, K. G., & Schall, J. D. (2001). Search efficiency but not response interference affects visual selection in frontal eye field. Neuron, 30(2), 583-591.
  35. ↑ Yang, S. N., Hwang, H., Ford, J., & Heinen, S. (2010). Supplementary eye field activity reflects a decision rule governing smooth pursuit but not the decision. Journal of neurophysiology, 103(5), 2458-2469.
  36. ↑ Coe, B., Tomihara, K., Matsuzawa, M., & Hikosaka, O. (2002). Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. The Journal of Neuroscience, 22(12), 5081-5090.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.