Neurons in the Nonhuman Primate Amygdala and Dorsal Anterior Cingulate Cortex Signal Aversive Memory Formation under Sedation

Background Anesthetics aim to prevent memory of unpleasant experiences. The amygdala and dorsal anterior cingulate cortex participate in forging emotional and valence-driven memory formation. It was hypothesized that this circuitry maintains its role under sedation. Methods Two nonhuman primates underwent aversive tone–odor conditioning under sedative states induced by ketamine or midazolam (1 to 8 and 0.1 to 0.8 mg/kg, respectively). The primary outcome was behavioral and neural evidence suggesting memory formation. This study simultaneously measured conditioned inspiratory changes and changes in firing rate of single neurons in the amygdala and the dorsal anterior cingulate cortex in response to an expected aversive olfactory stimulus appearing during acquisition and tested their retention after recovery. Results Aversive memory formation occurred in 26 of 59 sessions under anesthetics (16 of 29 and 10 of 30, 5 of 30 and 21 of 29 for midazolam and ketamine at low and high doses, respectively). Single-neuron responses in the amygdala and dorsal anterior cingulate cortex were positively correlated between acquisition and retention (amygdala, n = 101, r = 0.51, P < 0.001; dorsal anterior cingulate cortex, n = 121, r = 0.32, P < 0.001). Neural responses during acquisition under anesthetics were stronger in sessions exhibiting memory formation than those that did not (amygdala median response ratio, 0.52 versus 0.33, n = 101, P = 0.021; dorsal anterior cingulate cortex median response ratio, 0.48 versus 0.32, n = 121, P = 0.012). The change in firing rate of amygdala neurons during acquisition was correlated with the size of stimuli-conditioned inspiratory response during retention (n = 101, r = 0.22 P = 0.026). Thus, amygdala and dorsal anterior cingulate cortex responses during acquisition under anesthetics predicted retention. Respiratory unconditioned responses to the aversive odor anesthetics did not differ from saline controls. Conclusions These results suggest that the amygdala–dorsal anterior cingulate cortex circuit maintains its role in acquisition and maintenance of aversive memories in nonhuman primates under sedation with ketamine and midazolam and that the stimulus valence is sufficient to drive memory formation. Editor’s Perspective What We Already Know about This Topic What This Article Tells Us That Is New

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Ramping ensemble activity in dorsal anterior cingulate neurons during persistent commitment to a decision

Journal of Neurophysiology ◽

10.1152/jn.00711.2015 ◽

2015 ◽

Vol 114 (4) ◽

pp. 2439-2449 ◽

Cited By ~ 58

Author(s):

Tommy C. Blanchard ◽

Caleb E. Strait ◽

Benjamin Y. Hayden

Keyword(s):

Firing Rate ◽

Anterior Cingulate Cortex ◽

Cingulate Cortex ◽

Reward Processing ◽

Self Control ◽

Anterior Cingulate ◽

Dorsal Anterior Cingulate Cortex ◽

Neural Processes ◽

Reward Amount ◽

Ensemble Activity

We frequently need to commit to a choice to achieve our goals; however, the neural processes that keep us motivated in pursuit of delayed goals remain obscure. We examined ensemble responses of neurons in macaque dorsal anterior cingulate cortex (dACC), an area previously implicated in self-control and persistence, in a task that requires commitment to a choice to obtain a reward. After reward receipt, dACC neurons signaled reward amount with characteristic ensemble firing rate patterns; during the delay in anticipation of the reward, ensemble activity smoothly and gradually came to resemble the postreward pattern. On the subset of risky trials, in which a reward was anticipated with 50% certainty, ramping ensemble activity evolved to the pattern associated with the anticipated reward (and not with the anticipated loss) and then, on loss trials, took on an inverted form anticorrelated with the form associated with a win. These findings enrich our knowledge of reward processing in dACC and may have broader implications for our understanding of persistence and self-control.

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Dorsal anterior cingulate cortex intrinsic functional connectivity linked to electrocortical measures of error-monitoring

10.1101/2020.10.21.348649 ◽

2020 ◽

Author(s):

Hayley Gilbertson ◽

Lin Fang ◽

Jeremy A. Andrzejewski ◽

Joshua M. Carlson

Keyword(s):

Functional Connectivity ◽

Anterior Cingulate Cortex ◽

Flanker Task ◽

Monitoring Network ◽

Cingulate Cortex ◽

Event Related Potential ◽

Anterior Cingulate ◽

Functional Coupling ◽

Error Monitoring ◽

Dorsal Anterior Cingulate Cortex

AbstractThe error-related negativity (ERN) is a response-locked event-related potential, occurring approximately 50 ms following an erroneous response at frontocentral electrode sites. Source localization and functional magnetic resonance imaging (fMRI) research indicate that the ERN is likely generated by activity in the dorsal anterior cingulate cortex (dACC). The dACC is thought to be a part of a broader network of brain regions that collectively comprise an error-monitoring network. However, little is known about how intrinsic connectivity within the dACC-based error-monitoring network contributes to variability in ERN amplitude. The purpose of this study was to assess the relationship between dACC functional connectivity and ERN amplitude. In a sample of 53 highly trait-anxious individuals, the ERN was elicited in a flanker task and functional connectivity was assessed in a 10-minute resting-state fMRI scan. Results suggest that the strength of dACC seeded functional connectivity with the supplementary motor area is correlated with the ΔERN (i.e., incorrect – correct responses) amplitude such that greater ΔERN amplitude was accompanied by greater functional coupling between these regions. In addition to the dACC, exploratory analyses found that functional connectivity in the caudate, cerebellum, and a number of regions in the error-monitoring network were linked to variability in ΔERN amplitude. In sum, ERN amplitude appears to be related to the strength of functional connectivity between error-monitoring and motor control regions of the brain.

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Altered resting-state dorsal anterior cingulate cortex functional connectivity in patients with post-traumatic stress disorder

Australian & New Zealand Journal of Psychiatry ◽

10.1177/0004867418812674 ◽

2018 ◽

Vol 53 (1) ◽

pp. 68-79 ◽

Cited By ~ 6

Author(s):

Hui Juan Chen ◽

Li Zhang ◽

Jun Ke ◽

Rongfeng Qi ◽

Qiang Xu ◽

...

Keyword(s):

Functional Connectivity ◽

Anterior Cingulate Cortex ◽

Post Traumatic Stress Disorder ◽

Traumatic Stress ◽

Stress Disorder ◽

Cingulate Cortex ◽

Anterior Cingulate ◽

Post Traumatic Stress ◽

Dorsal Anterior Cingulate Cortex ◽

Post Traumatic

Objective: The brain functional alterations at regional and network levels in post-traumatic stress disorder patients are still unclear. This study explored brain functional alterations at regional and network levels in post-traumatic stress disorder patients with resting-state functional magnetic resonance imaging and evaluated the relationship between brain function and clinical indices in post-traumatic stress disorder. Methods: Amplitude of low-frequency fluctuation and seed-based functional connectivity analyses were conducted among typhoon survivors with ( n = 27) and without post-traumatic stress disorder ( n = 33) and healthy controls ( n = 30) to assess the spontaneous brain activity and network-level brain function. Pearson correlation analyses were performed to examine the association of brain function with clinical symptom and social support. Results: Both the post-traumatic stress disorder group and the trauma-exposed control group showed decreased amplitude of low-frequency fluctuation in the dorsal anterior cingulate cortex relative to the healthy control group. The post-traumatic stress disorder group showed increased dorsal anterior cingulate cortex functional connectivity with the right paracentral lobule and bilateral precentral gyrus/postcentral gyrus relative to both control groups. Both traumatized groups exhibited decreased dorsal anterior cingulate cortex functional connectivity with the right hippocampus and left cerebellum relative to the healthy control group. More decreased dorsal anterior cingulate cortex functional connectivity with the right hippocampus was found in the post-traumatic stress disorder group. The Checklist-Civilian Version score positively correlated with functional connectivity between the dorsal anterior cingulate cortex and the right paracentral lobule as well as between the dorsal anterior cingulate cortex and the right precentral gyrus/postcentral gyrus. The social support was associated with functional connectivity between the dorsal anterior cingulate cortex and the bilateral precentral gyrus/postcentral gyrus as well as the dorsal anterior cingulate cortex and the left middle frontal gyrus. Conclusion: Trauma exposure may result in aberrant local and network-level functional connectivity in individuals with or without post-traumatic stress disorder. Altered amplitude of low-frequency fluctuation in the dorsal anterior cingulate cortex may be a predisposing risk factor for post-traumatic stress disorder development following trauma exposure. More prominent decreased dorsal anterior cingulate cortex functional connectivity with the right hippocampus might be specific in the post-traumatic stress disorder group. Improvement of social support might possibly be significant for post-traumatic stress disorder patients.

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