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Grant Number: 5R01MH070836-02
Project Title: Neural Encoding of Emotion in the Primate Amygdala
PI Information: KATALIN M. GOTHARD,
[email protected]
Abstract: DESCRIPTION (provided by applicant): The neural
substrate of emotion encompasses a large brain circuit in which the
amygdala plays a key role. The long-term goal of the proposed research
is to determine how specific functions attributed to the amygdala are
carried out at the neural level. One of the functions of the amygdala is
to select from the environment stimuli with inherent emotional value and
respond to them adequately, e.g., withdraw or fight when threatened.
This process might rely on innately programmed and relatively inflexible
pathways to ensure enduring and reliable reactions in response to
objects and events of survival value. In parallel, the amygdala is
required to update the reinforcing value of many stimuli that gain or
lose emotional significance through learning and experience. Both
functions are used for social behavior. The intricacy of primate
societies requires that humans and monkeys respond reliably to facial
expressions and other signals with emotional significance but also to
adjust responses to social context or to the history of interactions
between individuals. The neural basis of these complex and diverse
functions are largely unknown. The central hypothesis of this proposal
is that the lateral, basal, and central amygdaloid nuclei carry out a
sequence of dissociable but complementary functions. The objective of
the proposed studies is to identify in the amygdala the neural signature
of stimulus differentiation, evaluation, and the initiation of emotional
responses. This will be achieved by relating autonomic, behavioral, and
neural ensemble responses to manipulations of the reinforcing value of
face and non-face stimuli. This approach will determine (1) whether
negative or positive stimuli are processed preferentially or
differentially in the amygdala, (2) whether facial expressions that
carry inherent positive or negative valence engage the same neuronal
processes as neutral objects paired with reward or punishment, (3)
whether neural activity in the amygdale predicts the autonomic and
somatic expressions of emotion. These studies will determine the neural
mechanism by which the amygdala evaluates stimuli of significance and
relays the results of this process to a complex brain circuits that
control emotional and social behavior. Understanding the neural
processes carried out at each level of this circuit holds promise for
more effective interventions in emotional disorders.
Thesaurus Terms:
amygdala, association learning, brain electrical activity, emotion, face
expression, neural information processing, neuroanatomy, reinforcer,
social behavior, visual stimulus
autonomic nervous system, brain imaging /visualization /scanning
Macaca mulatta, electrode
Institution: UNIVERSITY OF ARIZONA
PO BOX 3308
TUCSON, AZ 857223308
Fiscal Year: 2006
Department: PHYSIOLOGY
Project Start: 01-JAN-2005
Project End: 31-DEC-2009
ICD: NATIONAL INSTITUTE OF MENTAL HEALTH
IRG: COG
Neural Responses to Facial Expression and Face
Identity in the Monkey Amygdala
K. M. Gothard1, F. P. Battaglia2,
C. A. Erickson3, K. M. Spitler1
and D. G. Amaral4
1Department of Physiology,
College of Medicine, The University of Arizona, Tucson, Arizona;
2Graduate School of Neurosciences
Amsterdam, Faculty of Science, Swammerdam Institute for Life Sciences,
Center for Neuroscience, University of Amsterdam, Amsterdam, The
Netherlands; 3Helen Wills
Neuroscience Institute, University of California–Berkeley, Berkeley; and
4Department of Psychiatry and
Behavioral Sciences, The California National Primate Research Center and
The Music Intelligence Neural Development Institute, University of
California–Davis, Sacramento, California
Submitted 12 July 2006; accepted in final form 2 November 2006
J Neurophysiol 97: 1671-1683, 2007
Surgical procedures
All surgical procedures were carried out in compliance with National
Institutes of Health guidelines and were approved by the IACUC at the
University of Arizona. Two adult male rhesus monkeys (Macaca mulatta)
(monkeys S and H) were surgically prepared for multielectrode recordings
from the amygdala using a two-step surgical procedure. For both surgical
procedures the monkeys were preanesthetized with ketamine (10–15 mg/kg),
administered intramuscularly, and brought to surgical levels of
anesthesia with isoflurane (1–1.5%) supplemented with fentanyl (7–10 µg
• kg–1 • h–1). During the first procedure, monkeys were implanted with
three titanium tripod plates, custom-manufactured by Thomas Recording
(Giessen, Germany). Each tripod plate had an elevated center with a
threaded screw hole and three flat radial support arms emerging at 120°
intervals. The three support arms were 10 mm long, 2 mm wide, and were
perforated at the end to accommodate a 2-mm-diameter bone screw. The
arms were bent to match the curvature of the skull and affixed to the
bone with screws. Two plates were affixed posteriorly, 15 mm lateral
from midline and approximately 20 mm posterior from the interaural line.
The third plate was affixed straddling the midline 2 cm anterior to the
interaural line. The temporalis muscle and the scalp were closed over
the plates and the bone was allowed to heal and grow around the plates
(about 4–12 mo). Once substantial bone growth had occurred around the
screws and the arms of the plates (verified by CT scan), the second
procedure was undertaken in which the scalp above the plates was
perforated and small threaded head posts (3-mm-diameter shaft, 15-mm
length, 5-mm-diameter spherical head) were screwed into the center of
each of the tripod plates. The posts served as anchors for a removable
stainless steel ring that was secured in a rigid frame during
experiments. Such an arrangement distributed the torque generated by
head immobilization across the three head posts.
During the second surgical procedure, a recording chamber was secured
with bone screws and bone cement to the skull above the amygdala. The
chamber was placed at stereotaxic coordinates calculated from a
structural MRI carried out before surgery. Magnetic search coils were
also implanted in the left eye of one of monkey (S) following standard
procedures (Judge et al. 1980 ; Robinson 1963 ). After a 10-day recovery
period, monkeys were trained to tolerate head immobilization and to
fixate on objects presented on a computer monitor. When behavioral
training was complete, a 6- to 8-mm-diameter craniotomy was performed
within the chamber.
Behavioral training
The monkeys were trained to fixate on a white square that subtended 0.5
degree of visual angle (dva). The eye movements of monkey S were tracked
with a resolution of 0.25 dva and were digitized at 500 Hz using an
analog eye tracker (DNI, Newark, DE). Eye movements of monkey H were
monitored with the infrared eye tracker (Iscan, Burlington, MA) with a
resolution of 0.5 dva. Both eye trackers were connected to the CORTEX
experimental control system (NIMH-supported freeware from the website:
http://www.cortex.salk.edu) .
When the eyes were fixated for 150 ms at the white square, the fixation
icon was removed from the monitor and a stimulus image, subtending 12
dva, was displayed. The monkeys were allowed to freely scan the image,
with the requirement to maintain gaze within the boundaries of the
image. If this requirement was met for the entire duration of the
display (500 ms or 1 s) the monkeys received a 0.5- to 1-ml reward
droplet. The reward consisted of a paste of mashed granola, rice cereal,
and fruit juice or simple fruit juice mixed with applesauce. To
disambiguate the effect of the reward from the effect of the stimuli,
monkeys received a reward on only 50% of the trials, so that each image
was followed an equal number of times by reward or no reward. The
duration of the intertrial interval (ITI) was 1 s. When the monkey's
eyes moved outside the boundary of the image, the trial was terminated
by removing the image from the monitor. Error trials were not rewarded
and were followed by a 2-s time-out period. Error trials were excluded
from the analysis. To prevent habituation and blunting of the emotional
response to face stimuli, the sets of images used for training or used
during the period when we searched for neurons in the amygdala did not
contain monkey faces or images intended for presentation during
neurophysiological recordings.
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