Relation of ordinal position signals to the expectation of reward and passage of time in four areas of the macaque frontal cortex

Neurons in several areas of the monkey frontal cortex exhibit rank selectivity, firing differentially as a function of the stage attained during the performance of a serial order task. The activity of these neurons is commonly thought to represent ordinal position within the trial. However, they might also be sensitive to factors correlated with ordinal position including time elapsed during the trial (which is greater for each successive stage) and the degree of anticipation of reward (which probably increases at each successive stage). To compare the influences of these factors, we monitored neuronal activity in the supplementary motor area (SMA), presupplementary motor area (pre-SMA), supplementary eye field (SEF), and dorsolateral prefrontal cortex during the performance of a serial order task (requiring a series of saccades in three specified directions), a variable reward task (in which a cue displayed early in the trial indicated whether the reward received at the end of the trial would be large or small), and a long delay task (in which the monkey had simply to maintain fixation during a period of time approximating the duration of an average trial in the serial order task). We found that rank signals were partially correlated with sensitivity to elapsed time and anticipated reward. The connection to elapsed time was strongest in the pre-SMA. The connection to anticipated reward was most pronounced in the SMA and SEF. However, critically, these factors could not fully explain rank selectivity in any of the areas tested.

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Rank Signals in Four Areas of Macaque Frontal Cortex During Selection of Actions and Objects in Serial Order

Journal of Neurophysiology ◽

10.1152/jn.00639.2009 ◽

2010 ◽

Vol 104 (1) ◽

pp. 141-159 ◽

Cited By ~ 30

Author(s):

Tamara K. Berdyyeva ◽

Carl R. Olson

Keyword(s):

Frontal Cortex ◽

Serial Order ◽

The Other ◽

Motor Area ◽

Moderate Degree ◽

Task Context ◽

Supplementary Eye Field ◽

Dorsolateral Prefrontal ◽

Eye Field ◽

Selection Of

Neurons in several areas of monkey frontal cortex exhibit ordinal position (rank) selectivity during the performance of serial order tasks. It has been unclear whether rank selectivity or the dependence of rank selectivity on task context varies across the areas of frontal cortex. To resolve this issue, we recorded from neurons in the supplementary motor area (SMA), presupplementary motor area (pre-SMA), supplementary eye field (SEF), and dorsolateral prefrontal cortex (dlPFC) as monkeys performed two oculomotor tasks, one requiring the selection of three actions in sequence and the other requiring the selection of three objects in sequence. We found that neurons representing all ranks were present in all areas. Only to a moderate degree did the prevalence and nature of rank selectivity vary from area to area. The two most prominent inter-area differences involved a lower prevalence of rank selectivity in the dlPFC than in the other areas and a higher proportion of neurons preferring late ranks in the SMA and SEF than in the other areas. Neurons in all four areas are rank generalists in the sense of favoring the same rank in both the serial action task and the serial object task.

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Intracortical microstimulation of supplementary eye field impairs ability of monkeys to make serially ordered saccades

Journal of Neurophysiology ◽

10.1152/jn.00503.2013 ◽

2014 ◽

Vol 111 (8) ◽

pp. 1529-1540 ◽

Cited By ~ 4

Author(s):

Tamara K. Berdyyeva ◽

Carl R. Olson

Keyword(s):

Serial Order ◽

Macaque Monkey ◽

Ordinal Position ◽

Neural Representation ◽

Intracortical Microstimulation ◽

Supplementary Eye Field ◽

Eye Field ◽

Fixed Order ◽

Later Phase

Neurons in the supplementary eye field (SEF) of the macaque monkey exhibit rank selectivity, firing differentially as a function of the phase attained during the performance of a task requiring the execution of saccades to a series of objects in fixed order. The activity of these neurons is commonly thought to represent ordinal position in the service of serial-order performance. However, there is little evidence causally linking neuronal activity in the SEF to sequential behavior. To explore the role of the SEF in serial-order performance, we delivered intracortical microstimulation while monkeys performed a task requiring them to make saccades to three objects in a fixed order on each trial. Microstimulation, considered on average across all SEF sites and all phases of the trial, affected saccadic kinematics. In particular, it prolonged the reaction time, increased the peak velocity, and slightly increased the amplitude of saccades. In addition, it interfered with the monkeys' ability to select the target appropriate to a given phase of the trial. The pattern of the errors was such as would be expected if microstimulation shifted the neural representation of ordinal position toward a later phase of the trial.

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The Saccadic System

The Neurology of Eye Movements ◽

10.1093/med/9780199969289.003.0004 ◽

2015 ◽

pp. 169-288 ◽

Cited By ~ 3

Author(s):

R. John Leigh ◽

David S. Zee

Keyword(s):

Posterior Parietal Cortex ◽

Laboratory Evaluation ◽

Frontal Eye Field ◽

Supplementary Eye Field ◽

System P ◽

Dorsolateral Prefrontal ◽

Substrate Properties ◽

Eye Field ◽

Posterior Parietal ◽

Parietal Eye

This chapter reviews the behavioral properties of rapid eye movements, ranging from quick phases of nystagmus to cognitively controlled saccades, and their neural substrate. Properties of various types of saccades are described, including express saccades, memory-guided saccades, antisaccades, and saccades during visual search and reading. Current concepts of regions important for the generation of saccades are reviewed, integrating results of functional imaging and electrophysiology, including brainstem burst neurons and omnipause neurons, the superior colliculus, frontal eye field, supplementary eye field, dorsolateral prefrontal cortex, cingulate cortex, posterior parietal cortex, parietal eye field, thalamus, pulvinar, caudate, substantia nigra pars reticulata, subthalamic nucleus, cerebellar dorsal vermis, and fastigial nucleus. Saccade adaptation to novel visual demands is discussed, and the interaction between saccades and eyelid movements (blinks). Mathematical models of saccades are discussed. Clinical and laboratory evaluation of saccades and the pathophysiology of saccadic disorders, from slow saccades to opsoclonus, are reviewed.

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Monkey Supplementary Eye Field Neurons Signal the Ordinal Position of Both Actions and Objects

Journal of Neuroscience ◽

10.1523/jneurosci.4803-08.2009 ◽

2009 ◽

Vol 29 (3) ◽

pp. 591-599 ◽

Cited By ~ 16

Author(s):

T. K. Berdyyeva ◽

C. R. Olson

Keyword(s):

Ordinal Position ◽

Supplementary Eye Field ◽

Eye Field

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Inactivation of medial frontal cortex changes risk preference

10.1101/390021 ◽

2018 ◽

Cited By ~ 1

Author(s):

Xiaomo Chen ◽

Veit Stuphorn

Keyword(s):

Frontal Cortex ◽

Risk Preference ◽

Medial Frontal Cortex ◽

Supplementary Eye Field ◽

Decisions Under Risk ◽

High Reward ◽

Neural Processes ◽

Eye Field ◽

Increased Sensitivity ◽

Cortical Regions

SummaryHumans and other animals need to make decisions under varying degrees of uncertainty. These decisions are strongly influenced by an individual’s risk preference, however the neuronal circuitry by which risk preference shapes choice is still unclear [1]. Supplementary eye field (SEF), an oculomotor area within primate medial frontal cortex, is thought to be an essential part of the neuronal circuit underlying oculomotor decision-making, including decisions under risk [2–5]. Consistent with this view, risk-related action value and monitoring signals have been observed in SEF [6–8]. However, such activity has also been observed in other frontal areas, including orbitofrontal [9–11], cingulate [12–14], and dorsal lateral frontal cortex [15]. It is thus unknown whether the activity in SEF causally contributes to risky decisions, or if it is merely a reflection of neural processes in other cortical regions. Here, we tested a causal role of SEF in risky oculomotor choices. We found that SEF inactivation strongly reduced the frequency of risky choices. This reduction was largely due to a reduced attraction to reward uncertainty and high reward gain, but not due to changes in the subjective estimation of reward probability or average expected reward. Moreover, SEF inactivation also led to increased sensitivity to differences between expected and actual reward during free choice. Nevertheless, it did not affect adjustments of decisions based on reward history.

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Distribution of Eye- and Arm-Movement-Related Neuronal Activity in the SEF and in the SMA and Pre-SMA of Monkeys

Journal of Neurophysiology ◽

10.1152/jn.00867.2001 ◽

2002 ◽

Vol 87 (4) ◽

pp. 2158-2166 ◽

Cited By ~ 68

Author(s):

Naotaka Fujii ◽

Hajime Mushiake ◽

Jun Tanji

Keyword(s):

Neuronal Activity ◽

Supplementary Motor Area ◽

Motor Behavior ◽

Visual Target ◽

Arm Movement ◽

Context Dependency ◽

Motor Area ◽

Motor Tasks ◽

Supplementary Eye Field ◽

Eye Field

We analyzed neuronal activity in the supplementary eye field (SEF), supplementary motor area (SMA), and presupplementary motor area (pre-SMA) during the performance of three motor tasks: capturing a visual target with a saccade, reaching one arm to a target while gazing at a visual fixation point, or capturing a target with a saccade and arm-reach together. Our data demonstrated that each area was involved in controlling the arm and eye movements in a different manner. Saccade-related neurons were found mainly in the SEF. In contrast, arm-movement-related neurons were found primarily in the SMA and pre-SMA. In addition, we found that the activity of both arm-movement- and saccade-related neurons differed depending on the presence or absence of an accompanying saccade or arm movement. Such context dependency was found in all three areas. We also discovered that activity preceding eye or arm movement alone, and eye and arm movement combined, appeared more often in the pre-SMA and SEF, suggesting their involvement in effector-independent aspects of motor behavior. Subsequent analysis revealed that the laterality of arm representation differed in the three areas: it was predominantly contralateral in the SMA but largely bilateral in the pre-SMA and SEF.

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Erratum to “Prefrontal cortical cells projecting to the supplementary eye field and presupplementary motor area in the monkey”

Neuroscience Research ◽

10.1016/j.neures.2005.09.008 ◽

2005 ◽

Vol 53 (3) ◽

pp. 349-351 ◽

Cited By ~ 1

Author(s):

Yan Wang ◽

Masaki Isoda ◽

Yoshiya Matsuzaka ◽

Keisetsu Shima ◽

Jun Tanji

Keyword(s):

Motor Area ◽

Cortical Cells ◽

Prefrontal Cortical ◽

Supplementary Eye Field ◽

Eye Field

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The Effects of Microstimulation of the Dorsomedial Frontal Cortex on Saccade Latency

Journal of Neurophysiology ◽

10.1152/jn.00119.2007 ◽

2008 ◽

Vol 99 (4) ◽

pp. 1857-1870 ◽

Cited By ~ 17

Author(s):

Shun-nan Yang ◽

Stephen J. Heinen ◽

Marcus Missal

Keyword(s):

Frontal Cortex ◽

Target Selection ◽

Saccade Latency ◽

Saccade Target ◽

Electrical Microstimulation ◽

Supplementary Eye Field ◽

Dorsomedial Frontal Cortex ◽

Eye Field ◽

Movement Field ◽

Contralateral Movement

Neural regions in the dorsomedial frontal cortex (DMFC), including the supplementary eye field (SEF) and the presupplementary motor area (pre-SMA), are likely candidates for generating top-down control of saccade target selection. To investigate this, we applied electrical microstimulation to these structures while saccades were being planned to visual targets. Stimulation administered to superficial and lateral DMFC sites that were within or close to the SEF delayed ipsilateral and facilitated contralateral saccades. Facilitation was limited to saccades made toward targets in a narrow, contralateral movement field that had endpoints consistent with the goal of evoked saccades. Facilitation occurred with current delivered before target onset and delay with current applied after this time. Stimulation at deeper, medial sites that encompassed the pre-SMA resulted in mostly bilateral delay. The amount of delay at these sites was usually greater for ipsilateral saccades and increased with current amplitude. Changes in saccade latency were not accompanied by altered endpoint, trajectory, or peak velocity. The spatial specificity of SEF stimulation in inducing latency changes suggests that the SEF participates in selecting saccade goals. The less specific delay with pre-SMA stimulation suggests that it is involved in postponing visually guided saccades, thus likely permitting other oculomotor structures to select saccade goals.

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