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Pathways for Contextual Memory: The Primate Hippocampal Pathway to Anterior Cingulate Cortex.

ABSTRACT: The anterior cingulate cortex (ACC) is one of the few prefrontal areas that receives robust direct hippocampal terminations. This pathway may enable current context and past experience to influence goal-directed actions and emotional regulation by prefrontal cortices. We investigated the still ill-understood organization of the pathway from anterior hippocampus to ACC (A24a, A25, A32) to identify laminar termination patterns and their postsynaptic excitatory and inhibitory targets from system to synapse in rhesus monkeys. The densest hippocampal terminations targeted posterior A25, a region that is involved in affective and autonomic regulation. Hippocampal terminations innervated mostly excitatory neurons (~90%), suggesting strong excitatory effects. Among the smaller fraction of inhibitory targets, hippocampal terminations in A25 preferentially innervated calretinin neurons, a pattern that differs markedly from rodents. Further, hippocampal terminations innervated spines with D1 receptors, particularly in the deep layers of A25, where D1 receptors are enriched in comparison with the upper layers. The proximity of hippocampal terminations to D1 receptors may enable dopamine to enhance information transfer from the hippocampus to A25 and contribute to dopaminergic influence downstream on goal-directed action and emotional control by prefrontal cortices, in processes that may be disrupted by excessive dopamine release during uncontrollable stress.

SUBMITTER: Wang J

PROVIDER: S-EPMC7869091 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The lateral prefrontal cortex (LPFC) and anterior cingulate cortex (ACC) of the primate play distinctive roles in the mediation of complex cognitive tasks. Compared with the LPFC, integration of information by the ACC can span longer timescales and requires stronger engagement of inhibitory processes. Here, we reveal the synaptic mechanism likely to underlie these differences using in vitro patch-clamp recordings of synaptic events and multiscale imaging of synaptic markers in rhesus monkeys. Although excitatory synaptic signaling does not differ, the level of synaptic inhibition is much higher in ACC than LPFC layer 3 pyramidal neurons, with a significantly higher frequency (∼6×) and longer duration of inhibitory synaptic currents. The number of inhibitory synapses and the ratio of cholecystokinin to parvalbumin-positive inhibitory inputs are also significantly higher in ACC compared with LPFC neurons. Therefore, inhibition is functionally and structurally more robust and diverse in ACC than in LPFC, resulting in a lower excitatory: inhibitory ratio and a greater dynamic range for signal integration and network oscillation by the ACC. These differences in inhibitory circuitry likely underlie the distinctive network dynamics in ACC and LPC during normal and pathological brain states.SIGNIFICANCE STATEMENT The lateral prefrontal cortex (LPFC) and anterior cingulate cortex (ACC) play temporally distinct roles during the execution of cognitive tasks (rapid working memory during ongoing tasks and long-term memory to guide future action, respectively). Compared with LPFC-mediated tasks, ACC-mediated tasks can span longer timescales and require stronger engagement of inhibition. This study shows that inhibitory signaling is much more robust and diverse in the ACC than in the LPFC. Therefore, there is a lower excitatory: inhibitory synaptic ratio and a greater dynamic range for signal integration and oscillatory behavior in the ACC. These significant differences in inhibitory synaptic transmission form an important basis for the differential timing of cognitive processing by the LPFC and ACC in normal and pathological brain states.

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Pathways for Contextual Memory: The Primate Hippocampal Pathway to Anterior Cingulate Cortex.

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