NEURONAL RESPONSES TO A DELAYED-RESPONSE
DELAYED-REWARD GO/NOGO TASK IN THE MONKEY
POSTERIOR INSULAR CORTEX
T. ASAHI,
a,d
T. UWANO,
b,e
S. EIFUKU,
b
R. TAMURA,
b,e
S. ENDO,
d
T. ONO
a,e
AND H. NISHIJO
c,e
*
a
Molecular and Integrative Emotional Neuroscience, Graduate School
of Medicine, University of Toyama, Toyama 930-0194, Japan
b
Integrative Neuroscience, Graduate School of Medicine, University of
Toyama, Toyama 930-0194, Japan
c
System Emotional Science, Graduate School of Medicine, University
of Toyama, Sugitani 2630, Toyama 930-0194, Japan
d
Department of Neurosurgery, Graduate School of Medicine, Univer-
sity of Toyama, Toyama 930-0194, Japan
e
Core Research for Evolutional Science and Technology, Japan Sci-
ence and Technology Agency, Saitama 332-0012, Japan
Abstract—Anatomical connections of the insular cortex
suggest its involvement in cognition, emotion, memory,
and behavioral manifestation. However, there have been
few neurophysiological studies on the insular cortex in
primates, in relation to such higher cognitive functions. In
the present study, neural activity was recorded from the
monkey insular cortex during performance of a delayed-
response delayed-reward go/nogo task. In this task, visual
stimuli indicating go or nogo responses associated with
reward (reward trials) and with no reward (no-reward trials)
were presented after eye fixation. In the reward trials, the
monkey was required to release a button during presenta-
tion of the 2nd visual stimuli after a delay period (delay 1).
Then, a juice reward was delivered after another delay
(delay 2). The results indicated that the neurons respond-
ing in each epoch of the task were topographically local-
ized within the insular cortex, consistent with the previous
anatomical studies indicating topographical distributions
of afferent inputs from other subcortical and cortical sen-
sory areas. Furthermore, some insular neurons 1) nonspe-
cifically responded to the visual cues and during fixation;
2) responded to the visual cues predicting reward and
during the delay period before reward delivery; 3) re-
sponded differentially in go/nogo trials during the delay 2;
and 4) responded around button manipulation. The ob-
served patterns of insular-neuron responses and the cor-
respondence of their topographical localization to those in
previous anatomical studies suggest that the insular cor-
tex is involved in attention- and reward-related functions
and might monitor and integrate activities of other brain
regions during cognition and behavioral manifestation.
© 2006 IBRO. Published by Elsevier Ltd. All rights
reserved.
Key words: insular cortex, neural responses, go/nogo, de-
layed task, reward, monkey.
A previous neuroanatomical study has suggested that the
orbital-insular-temporopolar region is an integrated cortical
region that is part of a paralimbic circuit (Mesulam and
Mufson, 1982). The insular cortex, especially its posterior
part, is in a unique position to receive information of all
sensory modalities: gustation, olfaction, audition, somes-
thesis and vision (Mesulam and Mufson, 1982). The pos-
terior insula has intimate connections to somatosensory
(Friedman et al., 1986) and auditory association areas
(Hurst, 1959). The gustatory (Ogawa, 1994) and olfactory
(Pribriam et al., 1950; Augustine, 1985) inputs terminate in
the anterior division of the insula. Intra-insular connections
occur predominantly from the anterior to the posterior sec-
tors. The insular cortex also receives visual inputs from the
superior temporal sulcus (Mesulam and Mufson, 1982;
Seltzer and Pandya, 1991).
Consistent with the above anatomical studies, several
neurophysiological studies have reported various sensory
and complex responses in the primate insular cortex in
association with gustatory (Yaxley et al., 1990; Ogawa,
1994), somatosensory (Shneider et al., 1993), cardiovas-
cular (Zhang et al., 1999), and vestibular (Grusser et al.,
1990) functions. Recent noninvasive imaging studies in
humans have demonstrated a role of the insular cortex in
complex sensory-motor functions; the insular cortex was
implicated in visceral sensory (gustatory, esophageal move-
ment), somatosensory (tactile, pain), autonomic (vomiting,
cardiovascular function), motor association, and vestibular
functions (Augustine, 1996).
The insular cortex also has intimate anatomical con-
nections with the brain regions implicated in higher brain
functions (emotion, cognition, memory, attention, etc.),
such as the amygdala (Mufson et al., 1981; Amaral and
Price, 1984; Friedman et al., 1986), entorhinal cortex (In-
sausti et al., 1987), striatum (Chikama et al., 1997), tem-
poropolar (Mesulam and Mufson, 1982; Markowitsch et al.,
1985), orbitofrontal (Mesulam and Mufson, 1982; More-
craft et al., 1992), cingulate (Mesulam and Mufson, 1982),
and perirhinal and parahippocampal cortices (Suzuki and
Amaral, 1994). In addition, a posterior part of the insular
cortex receives afferent inputs from the cortices related to
reward expectancy, e.g. the orbitofrontal cortex (Tremblay
*Correspondence to: H. Nishijo, System Emotional Science, Graduate
School of Medicine, University of Toyama, Sugitani 2630, Toyama
930-0194, Japan. Tel: +81-76-434-7215; fax: +81-76-434-5012.
E-mail address: nishijo@med.u-toyama.ac.jp (H. Nishijo).
Abbreviations: BP, button press; BR, button release; CCD, charge-
coupled device; DR-DRW, delayed-response delayed-reward go/
nogo; D1, first delay; D2, second delay; EMGs, electromyograms; FIX,
fixation period; GNG-D, go/nogo differential; Ia, agranular insula; Id,
dysgranular insula; Ig, granular insula; ITI, inter-trial interval; N-D,
non-differential; RNR-D, reward/no-reward differential; RW, reward
period; SB, start beep; S1, first visual stimulation; S2, second visual
stimulation; S2E, end of the second visual stimulation.
Neuroscience 143 (2006) 627– 639
0306-4522/06$30.00+0.00 © 2006 IBRO. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuroscience.2006.08.008
627