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Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making.

Amemori K, Graybiel AM - Nat. Neurosci. (2012)

Bottom Line: In healthy individuals, the pACC is involved in cost-benefit evaluation.We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value.This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.

View Article: PubMed Central - PubMed

Affiliation: McGovern Institute for Brain Research, and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

ABSTRACT
The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.

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Distributions of pACC units classified by the correlation analyses. Distributions and numbers (indicated by size of circles) of units whose activity showed significantly positive (red, pos-type) or negative (blue, neg-type) correlations (Pearson's correlation coefficients, P < 0.05) with offered amount of reward (Rew, a), offered strength of airpuff (Ave, b), expected utility (Eutil, c), approach or avoidance decision (Cho, d), amount of chosen reward (Cho*Rew, e), strength of chosen airpuff (Cho*Ave, f), conflict in decision (Conf, g), and reaction time (RT, h). Total numbers of correlated units are indicated (n). For each distribution, we tested whether the neg-type or the pos-type populations of units in the ventral bank cortex significantly outnumbered the counterpart (blue shading, Fisher's exact test, P < 0.05) or not (blue rectangle).
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Figure 5: Distributions of pACC units classified by the correlation analyses. Distributions and numbers (indicated by size of circles) of units whose activity showed significantly positive (red, pos-type) or negative (blue, neg-type) correlations (Pearson's correlation coefficients, P < 0.05) with offered amount of reward (Rew, a), offered strength of airpuff (Ave, b), expected utility (Eutil, c), approach or avoidance decision (Cho, d), amount of chosen reward (Cho*Rew, e), strength of chosen airpuff (Cho*Ave, f), conflict in decision (Conf, g), and reaction time (RT, h). Total numbers of correlated units are indicated (n). For each distribution, we tested whether the neg-type or the pos-type populations of units in the ventral bank cortex significantly outnumbered the counterpart (blue shading, Fisher's exact test, P < 0.05) or not (blue rectangle).

Mentions: To determine whether this biased distribution toward negatively correlated units in the ventral bank region was produced by units with one primary behavioral correlate, or instead, by units with activity correlated with multiple behavioral variables, we performed a series of correlation analyses between unit activity and each behavioral variable used in the regression analyses. For each variable, we tested whether there was a predominance of ventral bank units with activity either positively or negatively correlated with the given variable. Fig. 5 shows the distributions of units with significant correlations (Pearson's correlation coefficients, P < 0.05). The results were striking. Negatively correlated units predominated positive ones in the ventral bank (Fisher's exact test, P < 0.05) for offered reward (Rew, Fig. 5a), for expected utility (Eutil, Fig. 5c), and for chosen reward amount (Cho*Rew, Fig. 5e). For conflict in decision (Conf, Fig. 5g) and for reaction time (RT, Fig. 5h), positively correlated units dominated negative ones. And for decision (Cho, Fig. 5d), units coding avoidance (Cho=0) dominated units coding approach (Cho=1). Thus, except for offered and chosen airpuff strength (Ave, Fig. 5b and Cho*Ave, Fig. 5f), units responding to multiple different variables (low Rew, low Eutil, low Cho*Rew; high Conf and high RT; Cho=0) predominated over their counterparts in the ventral bank region. These variables corresponded to the "motivationally negative" variables that activated N-type units.


Localized microstimulation of primate pregenual cingulate cortex induces negative decision-making.

Amemori K, Graybiel AM - Nat. Neurosci. (2012)

Distributions of pACC units classified by the correlation analyses. Distributions and numbers (indicated by size of circles) of units whose activity showed significantly positive (red, pos-type) or negative (blue, neg-type) correlations (Pearson's correlation coefficients, P < 0.05) with offered amount of reward (Rew, a), offered strength of airpuff (Ave, b), expected utility (Eutil, c), approach or avoidance decision (Cho, d), amount of chosen reward (Cho*Rew, e), strength of chosen airpuff (Cho*Ave, f), conflict in decision (Conf, g), and reaction time (RT, h). Total numbers of correlated units are indicated (n). For each distribution, we tested whether the neg-type or the pos-type populations of units in the ventral bank cortex significantly outnumbered the counterpart (blue shading, Fisher's exact test, P < 0.05) or not (blue rectangle).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3369110&req=5

Figure 5: Distributions of pACC units classified by the correlation analyses. Distributions and numbers (indicated by size of circles) of units whose activity showed significantly positive (red, pos-type) or negative (blue, neg-type) correlations (Pearson's correlation coefficients, P < 0.05) with offered amount of reward (Rew, a), offered strength of airpuff (Ave, b), expected utility (Eutil, c), approach or avoidance decision (Cho, d), amount of chosen reward (Cho*Rew, e), strength of chosen airpuff (Cho*Ave, f), conflict in decision (Conf, g), and reaction time (RT, h). Total numbers of correlated units are indicated (n). For each distribution, we tested whether the neg-type or the pos-type populations of units in the ventral bank cortex significantly outnumbered the counterpart (blue shading, Fisher's exact test, P < 0.05) or not (blue rectangle).
Mentions: To determine whether this biased distribution toward negatively correlated units in the ventral bank region was produced by units with one primary behavioral correlate, or instead, by units with activity correlated with multiple behavioral variables, we performed a series of correlation analyses between unit activity and each behavioral variable used in the regression analyses. For each variable, we tested whether there was a predominance of ventral bank units with activity either positively or negatively correlated with the given variable. Fig. 5 shows the distributions of units with significant correlations (Pearson's correlation coefficients, P < 0.05). The results were striking. Negatively correlated units predominated positive ones in the ventral bank (Fisher's exact test, P < 0.05) for offered reward (Rew, Fig. 5a), for expected utility (Eutil, Fig. 5c), and for chosen reward amount (Cho*Rew, Fig. 5e). For conflict in decision (Conf, Fig. 5g) and for reaction time (RT, Fig. 5h), positively correlated units dominated negative ones. And for decision (Cho, Fig. 5d), units coding avoidance (Cho=0) dominated units coding approach (Cho=1). Thus, except for offered and chosen airpuff strength (Ave, Fig. 5b and Cho*Ave, Fig. 5f), units responding to multiple different variables (low Rew, low Eutil, low Cho*Rew; high Conf and high RT; Cho=0) predominated over their counterparts in the ventral bank region. These variables corresponded to the "motivationally negative" variables that activated N-type units.

Bottom Line: In healthy individuals, the pACC is involved in cost-benefit evaluation.We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value.This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.

View Article: PubMed Central - PubMed

Affiliation: McGovern Institute for Brain Research, and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA.

ABSTRACT
The pregenual anterior cingulate cortex (pACC) has been implicated in human anxiety disorders and depression, but the circuit-level mechanisms underlying these disorders are unclear. In healthy individuals, the pACC is involved in cost-benefit evaluation. We developed a macaque version of an approach-avoidance decision task used to evaluate anxiety and depression in humans and, with multi-electrode recording and cortical microstimulation, we probed pACC function as monkeys performed this task. We found that the macaque pACC has an opponent process-like organization of neurons representing motivationally positive and negative subjective value. Spatial distribution of these two neuronal populations overlapped in the pACC, except in one subzone, where neurons with negative coding were more numerous. Notably, microstimulation in this subzone, but not elsewhere in the pACC, increased negative decision-making, and this negative biasing was blocked by anti-anxiety drug treatment. This cortical zone could be critical for regulating negative emotional valence and anxiety in decision-making.

Show MeSH
Related in: MedlinePlus