Similar neural activity during fear and disgust in the rat basolateral amygdala

12Citations
Citations of this article
64Readers
Mendeley users who have this article in their library.

Abstract

Much research has focused on how the amygdala processes individual affects, yet little is known about how multiple types of positive and negative affects are encoded relative to one another at the single-cell level. In particular, it is unclear whether different negative affects, such as fear and disgust, are encoded more similarly than negative and positive affects, such as fear and pleasure. Here we test the hypothesis that the basolateral nucleus of the amygdala (BLA), a region known to be important for learned fear and other affects, encodes affective valence by comparing neuronal activity in the BLA during a conditioned fear stimulus (fear CS) with activity during intraoral delivery of an aversive fluid that induces a disgust response and a rewarding fluid that induces a hedonic response. Consistent with the hypothesis, neuronal activity during the fear CS and aversive fluid infusion, but not during the fear CS and rewarding fluid infusion, was more similar than expected by chance. We also found that the greater similarity in activity during the fear- and disgust-eliciting stimuli was specific to a subpopulation of cells and a limited window of time. Our results suggest that a subpopulation of BLA neurons encodes affective valence during learned fear, and furthermore, within this subpopulation, different negative affects are encoded more similarly than negative and positive affects in a time-specific manner.

Figures

  • Figure 1. Experimental design and methods. (A) Experimental design. If the BLA encodes emotional valence during learned fear, then neuronal activity should be more similar during the fear CS and aversive fluid infusion (valence-congruent comparison) than during the fear CS and rewarding fluid infusion (valence-incongruent comparison). (B) Methods. Neuronal activity during the 5 second fear CS was compared to neuronal activity during the first 10 seconds of the rewarding and aversive intraoral fluid infusions. doi:10.1371/journal.pone.0027797.g001
  • Figure 2. Blood pressure and behavior during the recording sessions. (A) Change in blood pressure during fear CS, rewarding fluid infusion, and aversive fluid infusion (n = 39 sessions). (B) Mean of individual types of aversive taste reactivity responses during rewarding and aversive fluid infusions. (n = 45 sessions). (C) Mean of individual types of positive hedonic taste reactivity responses during rewarding and aversive fluid infusions. (n = 45 sessions). (D) Change in aversive taste reactivity responses shown in (B) (n = 45 sessions). (E) Change in positive hedonic taste reactivity responses shown in (C) (n = 45 sessions). Values represent mean +/2 standard error of the mean. doi:10.1371/journal.pone.0027797.g002
  • Figure 3. Neuronal activity during affective stimuli. (A) Design of aligned versus shuffled comparisons. If neuronal activity is similar during the affective stimuli, then the difference in the aligned condition should be less than the difference in the shuffled condition. If neuronal activity is different during the affective stimuli, then the difference in the aligned condition should be greater than the difference in the shuffled condition. (B) Valence-congruent comparison. Activity during fear CS and aversive fluid infusion is more similar than expected by chance (n = 84 cells). (C) Valence-incongruent comparison. Activity during fear CS and rewarding fluid infusion is not more similar than expected by chance (n = 84 cells). (D) Non-SD cells. Valence-congruent comparison of activity is more similar than valence-incongruent comparison (n = 62 cells). (E) SD cells. No significant difference between valence-congruent and valence-incongruent comparison of activity (n = 22 cells). Values represent mean +/2 standard error of the mean. * P,.01, ** P,.0001. doi:10.1371/journal.pone.0027797.g003
  • Figure 4. Population plots and examples of SD and non-SD cells. (A) Population plot of changes in neuronal activity during the fear CS and aversive fluid infusion. (B) Population plot of changes in neuronal activity during the fear CS and rewarding fluid infusion. (C)–(F) depict average activity to each of the stimuli for one cell. Red is fear CS, blue is rewarding fluid infusion, and green is aversive fluid infusion. (C) Example perievent time histogram of an SD cell which had an increase in activity during the fear CS. Mean and standard deviation of firing rates for baseline periods before fear CS, rewarding fluid infusion, and aversive fluid infusion, respectively: 2.062.3; 2.062.1; 1.661.7; (D) Example perievent time histogram of an SD cell which had a decrease in activity during the fear CS. Mean and standard deviation of firing rates for baseline periods before fear CS, rewarding fluid infusion, and aversive fluid infusion, respectively: 2.161.5; 0.360.7; 0.560.6; (E) Example perievent time histogram of a non-SD cell which had an increase in activity during the fear CS. Mean and standard deviation of firing rates for baseline periods before fear CS, rewarding fluid infusion, and aversive fluid infusion, respectively: 7.463.3; 5.763.5; 5.762.8; (F) Example of a non-SD cell which had a decrease in activity during the fear CS. Mean and standard deviation of firing rates for baseline periods before fear CS, rewarding fluid infusion, and aversive fluid infusion, respectively: 0.360.6; 0.160.5; 0.260.4. doi:10.1371/journal.pone.0027797.g004
  • Figure 5. Timing of valence-specific and valence-nonspecific neuronal activity. (A) Valence-congruent comparison (n = 84 cells). Activity during fear CS and aversive fluid infusion is more similar than expected by chance in many time bins. (B) Valence-incongruent comparison (n = 84 cells). Activity during fear CS and rewarding fluid infusion is more similar than expected by chance in a smaller number of time bins towards the onset of the rewarding fluid infusion. (C) All fear-CS responsive cells (SD and non-SD cells; n = 84). Valence-congruent comparison of activity is more similar than valence-incongruent comparison in a small time window. (D) Non-SD cells (n = 62). Valence-congruent comparison of activity is more similar than valence-incongruent comparison, except towards onset of fear CS and fluid infusions. Scale bar is Z units. * P,.05, ** P,.01, *** P,.001. doi:10.1371/journal.pone.0027797.g005

Cited by Powered by Scopus

Get full text
Get full text

Hebbian and neuromodulatory mechanisms interact to trigger associative memory formation

136Citations
433Readers

Register to see more suggestions

Mendeley helps you to discover research relevant for your work.

Already have an account?

Cite

CITATION STYLE

APA

Shabel, S. J., Schairer, W., Donahue, R. J., Powell, V., & Janak, P. H. (2011). Similar neural activity during fear and disgust in the rat basolateral amygdala. PLoS ONE, 6(12). https://doi.org/10.1371/journal.pone.0027797

Readers over time

‘11‘12‘13‘14‘15‘16‘17‘18‘19‘20‘21‘22‘23‘2505101520

Readers' Seniority

Tooltip

PhD / Post grad / Masters / Doc 26

55%

Researcher 15

32%

Professor / Associate Prof. 5

11%

Lecturer / Post doc 1

2%

Readers' Discipline

Tooltip

Agricultural and Biological Sciences 26

52%

Neuroscience 16

32%

Psychology 6

12%

Medicine and Dentistry 2

4%

Save time finding and organizing research with Mendeley

Sign up for free
0