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2015 ; 35
(38
): 12994-3005
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Amygdala Signaling during Foraging in a Hazardous Environment
#MMPMID26400931
Amir A
; Lee SC
; Headley DB
; Herzallah MM
; Pare D
J Neurosci
2015[Sep]; 35
(38
): 12994-3005
PMID26400931
show ga
We recorded basolateral amygdala (BL) neurons in a seminaturalistic foraging
task. Rats had to leave their nest to retrieve food in an elongated arena
inhabited by a mechanical predator. There were marked trial-to-trial variations
in behavior. After poking their head into the foraging arena and waiting there
for a while, rats either retreated to their nest or initiated foraging. Before
initiating foraging, rats waited longer on trials that followed failed than
successful trials indicating that prior experience influenced behavior. Upon
foraging initiation, most principal cells (Type-1) reduced their firing rate,
while in a minority (Type-2) it increased. When rats aborted foraging, Type-1
cells increased their firing rates, whereas in Type-2 cells it did not change.
Surprisingly, the opposite activity profiles of Type-1 and Type-2 units were also
seen in control tasks devoid of explicit threats or rewards. The common correlate
of BL activity across these tasks was movement velocity, although an influence of
position was also observed. Thus depending on whether rats initiated movement or
not, the activity of BL neurons decreased or increased, regardless of whether
threat or rewards were present. Therefore, BL activity not only encodes threats
or rewards, but is closely related to behavioral output. We propose that higher
order cortical areas determine task-related changes in BL activity as a function
of reward/threat expectations and internal states. Because Type-1 and Type-2
cells likely form differential connections with the central amygdala (controlling
freezing), this process would determine whether movement aimed at attaining food
or exploration is suppressed or facilitated. Significance statement: For decades,
amygdala research has been dominated by pavlovian and operant conditioning
paradigms. This work has led to the view that amygdala neurons signal threats or
rewards, in turn causing defensive or approach behaviors. However, the artificial
circumstances of conditioning studies bear little resemblance to normal life. In
natural conditions, subjects are simultaneously presented with potential threats
and rewards, forcing them to engage in a form of risk assessment. We examined
this process using a seminaturalistic foraging task. In constant conditions of
threats and rewards, amygdala activity could be high or low, depending on the
rats' decisions on a given trial. Therefore, amygdala activity does not only
encode threats or rewards but is also closely related to behavioral output.
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