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Exp Brain Res (2015) 233:459–476
DOI 10.1007/s00221-014-4127-2
RESEARCH ARTICLE
A mechanism for decision rule discrimination by supplementary
eye field neurons
Supriya Ray · Stephen J. Heinen
Received: 13 August 2014 / Accepted: 11 October 2014 / Published online: 5 November 2014
© Springer-Verlag Berlin Heidelberg 2014
of either the decision to pursue or the decision to continue
fixation accounts for the observed neural phenomena.
Keywords Abstract rule · Accumulator model ·
Decision making · Primates · Smooth pursuit ·
Supplementary eye field
Introduction
While most studies of action selection have focused on how
concrete rules (e.g., ‘red means stop’; ‘green means go’)
guide a one-to-one mapping between a sensory stimulus
and a motor response, less is known about how abstract
rules connect many sensory inputs to a specific motor
output, or a specific sensory input to many motor outputs
(Bunge 2004; Cisek and Kalaska 2010). For example, for
the rule ‘if a pedestrian is on the crosswalk then stop, but
if the pedestrian is on the sidewalk then go,’ pedestrians
of different physical characteristics may result in a single
action, and a particular pedestrian may result in different
actions depending on where they are standing. The prefron-
tal and premotor cortices in human and non-human pri-
mates have been shown to be involved in encoding abstract
rules (White and Wise 1999; Asaad et al. 2000; Wallis et al.
2001; Bunge et al. 2003; Wallis and Miller 2003; Muham-
mad et al. 2006; Bengtsson et al. 2009; Badre et al. 2010),
which allow an arbitrary sensory motor association for limb
and eye movements to be made (Mitz et al. 1991; Asaad
et al. 1998).
The supplementary eye field (SEF) in the medial frontal
cortex of primates (Schlag and Schlag-Rey 1987) plays a
key role in conditional stimulus–response mapping for sac-
cadic (Chen and Wise 1995, 1996) and smooth pursuit eye
movements (Kim et al. 2005; Shichinohe et al. 2009). SEF
Abstract A decision to select an action from alternatives
is often guided by rules that flexibly map sensory inputs to
motor outputs when certain conditions are satisfied. How-
ever, the neural mechanisms underlying rule-based deci-
sion making remain poorly understood. Two complemen-
tary types of neurons in the supplementary eye field (SEF)
of macaques have been identified that modulate activity
differentially to interpret rules in an ocular go–nogo task,
which stipulates that the animal either visually pursue a
moving object if it intersects a visible zone (‘go’), or main-
tain fixation if it does not (‘nogo’). These neurons discrimi-
nate between go and nogo rule-states by increasing activity
to signal their preferred (agonist) rule-state and decreasing
activity to signal their non-preferred (antagonist) rule-state.
In the current study, we found that SEF neurons decrease
activity in anticipation of the antagonist rule-state, and
do so more rapidly when the rule-state is easier to pre-
dict. This rapid decrease in activity could underlie a pro-
cess of elimination in which trajectories that do not invoke
the preferred rule-state receive no further computational
resources. Furthermore, discrimination between difficult
and easy trials in the antagonist rule-state occurs prior to
when discrimination within the agonist rule-state occurs. A
winner-take-all like model that incorporates a pair of mutu-
ally inhibited integrators to accumulate evidence in favor
S. Ray · S. J. Heinen
The Smith-Kettlewell Eye Research Institute, San Francisco,
CA, USA
S. Ray (*)
Centre of Behavioural and Cognitive Sciences, University
of Allahabad, Senate Hall Campus, Allahabad 211002,
Uttar Pradesh, India
e-mail: sray@cbcs.ac.in