scholarly journals Asymmetric effective connectivity between primate anterior cingulate and lateral prefrontal cortex revealed by electrical microstimulation

2018 ◽  
Author(s):  
Verónica Nácher ◽  
Seyed Alireza Hassani ◽  
Thilo Womelsdorf
Keyword(s):  
Prefrontal Cortex ◽  
Effective Connectivity ◽  
Anterior Cingulate ◽  
Inhibitory Neurons ◽  
Synaptic Connectivity ◽  
Reverse Direction ◽  
Neural Firing ◽  
Lateral Prefrontal Cortex ◽  
Electrical Microstimulation ◽  
Human Primate

AbstractThe anterior cingulate cortex (ACC) and lateral prefrontal cortex (IPFC) of the non-human primate show neural firing correlations and synchronize at theta and beta frequencies during the monitoring and shifting of attention. These functional interactions might be based on synaptic connectivity that is equally efficacious in both directions, but it might be that there are systematic asymmetries in connectivity consistent with reports of more effective inhibition within the ACC than IPFC, or with a preponderance of ACC projections synapsing onto inhibitory neurons in the IPFC. Here, we tested effective ACC-IPFC connectivity in awake monkeys and report systematic asymmetries in the temporal patterning and latencies of effective connectivity as measured using electrical microstimulation. We found that ACC stimulation triggered evoked fields (EFPs) were more likely to be multiphasic in the IPFC than in the reverse direction, with a large proportion of connections showing 2-4 inflection points resembling resonance in the 20-30 Hz beta frequency range. Stimulation of ACC → IPFC resulted, on average, in shorter-latency EFPs than IPFC → ACC. Overall, latencies and connectivity strength varied more than two-fold depending on the precise anterior-to-posterior location of the connections. These findings reveal systematic asymmetries in effective connectivity between ACC and IPFC in the awake non-human primate and document the spatial and temporal patchiness of effective synaptic connections. We speculate that measuring effective connectivity profiles will be essential for understanding how local synaptic efficacy and synaptic connectivity translates into functional neuronal interactions to support adaptive behaviors.

scholarly journals Muscarinic Acetylcholine Receptor Localization on Distinct Excitatory and Inhibitory Neurons Within the ACC and LPFC of the Rhesus Monkey

2022 ◽  
Vol 15 ◽  
Author(s):  
Alexandra Tsolias ◽  
Maria Medalla
Keyword(s):  
Prefrontal Cortex ◽  
Muscarinic Receptors ◽  
Calcium Binding ◽  
Pyramidal Neurons ◽  
Muscarinic Acetylcholine Receptor ◽  
Anterior Cingulate ◽  
Inhibitory Neurons ◽  
Receptor Localization ◽  
Cortical Inputs ◽  
Almost All

Acetylcholine (ACh) can act on pre- and post-synaptic muscarinic receptors (mAChR) in the cortex to influence a myriad of cognitive processes. Two functionally-distinct regions of the prefrontal cortex—the lateral prefrontal cortex (LPFC) and the anterior cingulate cortex (ACC)—are differentially innervated by ascending cholinergic pathways yet, the nature and organization of prefrontal-cholinergic circuitry in primates are not well understood. Using multi-channel immunohistochemical labeling and high-resolution microscopy, we found regional and laminar differences in the subcellular localization and the densities of excitatory and inhibitory subpopulations expressing m1 and m2 muscarinic receptors, the two predominant cortical mAChR subtypes, in the supragranular layers of LPFC and ACC in rhesus monkeys (Macaca mulatta). The subset of m1+/m2+ expressing SMI-32+ pyramidal neurons labeled in layer 3 (L3) was denser in LPFC than in ACC, while m1+/m2+ SMI-32+ neurons co-expressing the calcium-binding protein, calbindin (CB) was greater in ACC. Further, we found between-area differences in laminar m1+ dendritic expression, and m2+ presynaptic localization on cortico-cortical (VGLUT1+) and sub-cortical inputs (VGLUT2+), suggesting differential cholinergic modulation of top-down vs. bottom-up inputs in the two areas. While almost all inhibitory interneurons—identified by their expression of parvalbumin (PV+), CB+, and calretinin (CR+)—expressed m1+, the localization of m2+ differed by subtype and area. The ACC exhibited a greater proportion of m2+ inhibitory neurons compared to the LPFC and had a greater density of presynaptic m2+ localized on inhibitory (VGAT+) inputs targeting proximal somatodendritic compartments and axon initial segments of L3 pyramidal neurons. These data suggest a greater capacity for m2+-mediated cholinergic suppression of inhibition in the ACC compared to the LPFC. The anatomical localization of muscarinic receptors on ACC and LPFC micro-circuits shown here contributes to our understanding of diverse cholinergic neuromodulation of functionally-distinct prefrontal areas involved in goal-directed behavior, and how these interactions maybe disrupted in neuropsychiatric and neurological conditions.

scholarly journals Neural Correlates of True and False Recognition Memory for Socially Relevant Information in Schizophrenia

2020 ◽  
Vol 1 (1) ◽  
Author(s):  
Amy M Jimenez ◽  
Junghee Lee ◽  
Eric A Reavis ◽  
Jonathan K Wynn ◽  
Michael F Green
Keyword(s):  
Prefrontal Cortex ◽  
Recognition Memory ◽  
False Recognition ◽  
Cingulate Cortex ◽  
Posterior Cingulate Cortex ◽  
Anterior Cingulate ◽  
False Alarms ◽  
Neural Activation ◽  
Lateral Prefrontal Cortex ◽  
Socially Relevant

Abstract Individuals with schizophrenia (SZ) demonstrate poor recognition memory, even when information is socially relevant. The neural alterations associated with responses to old information that is accurately recognized (true recognition) vs new information inaccurately identified as old (false recognition) are not known. Twenty SZ patients and 16 healthy controls performed a recognition paradigm during functional magnetic resonance imaging (fMRI) using 78 learned target and 78 new distractor words (all socially relevant trait adjectives). Participants were asked to indicate whether they had seen the word before or not. Words were classified according to the subjects’ responses, as hits (true recognition), false alarms (false recognition), correct rejections, or misses and compared for blood-oxygen-level-dependent (BOLD) activation. During hits, patients with SZ and controls showed similar BOLD activation in expected areas of lateral prefrontal cortex, parietal cortex, and anterior cingulate cortex. During false alarms, controls activated many of the same regions as were activated during hits. In contrast, patients had reduced activation in lateral prefrontal cortex (Brodmann Area, BA, 9, 46), anterior cingulate/paracingulate (BA 24/32, 6), and posterior cingulate cortex (BA 23/31). These results indicate that, compared to controls, patients with SZ exhibit a lack of correspondence between behavior (ie, falsely identifying new items as old) and neural activation patterns (ie, overlap in activation of regions associated with true and false recognition). These findings shed light on the neural mechanisms associated with false recognition memory in SZ.

scholarly journals The Role of Intact Frontostriatal Circuits in Error Processing

2006 ◽  
Vol 18 (4) ◽  
pp. 651-664 ◽  
Author(s):  
Markus Ullsperger ◽  
D. Yves von Cramon
Keyword(s):  
Prefrontal Cortex ◽  
Basal Ganglia ◽  
Anterior Cingulate Cortex ◽  
Performance Monitoring ◽  
Brain Plasticity ◽  
Cingulate Cortex ◽  
Anterior Cingulate ◽  
Cortical Circuits ◽  
Lateral Prefrontal Cortex ◽  
Error Related Negativity

The basal ganglia have been suggested to play a key role in performance monitoring and resulting behavioral adjustments. It is assumed that the integration of prefrontal and motor cortico—striato—thalamo—cortical circuits provides contextual information to the motor anterior cingulate cortex regions to enable their function in performance monitoring. So far, direct evidence is missing, however. We addressed the involvement of frontostriatal circuits in performance monitoring by collecting event-related brain potentials (ERPs) and behavioral data in nine patients with focal basal ganglia lesions and seven patients with lateral prefrontal cortex lesions while they performed a flanker task. In both patient groups, the amplitude of the error-related negativity was reduced, diminishing the difference to the ERPs on correct responses. Despite these electrophysiological abnormalities, most of the patients were able to correct errors. Only in lateral prefrontal cortex patients whose lesions extended into the frontal white matter, disrupting the connections to the motor anterior cingulate cortex and the striatum, were error corrections severely impaired. In sum, the fronto—striato—thalamo—cortical circuits seem necessary for the generation of error-related negativity, even when brain plasticity has resulted in behavioral compensation of the damage. Thus, error-related ERPs in patients provide a sensitive measure of the integrity of the performance monitoring network.

scholarly journals Face selective patches in marmoset frontal cortex

2020 ◽  
Author(s):  
David J. Schaeffer ◽  
Janahan Selvanayagam ◽  
Kevin D. Johnston ◽  
Ravi S. Menon ◽  
Winrich A. Freiwald ◽  
...  
Keyword(s):  
Prefrontal Cortex ◽  
Frontal Cortex ◽  
Anterior Cingulate Cortex ◽  
Face Processing ◽  
New World ◽  
Anterior Cingulate ◽  
Old World ◽  
Lateral Prefrontal Cortex ◽  
Socially Relevant ◽  
High Level

AbstractPrimates have evolved the ability transmit important social information through facial expression. In humans and macaque monkeys, socially relevant face processing is accomplished via a distributed cortical and subcortical functional network that includes specialized patches in anterior cingulate cortex and lateral prefrontal cortex, regions usually associated with high-level cognition. It is unclear whether a similar network exists in New World primates, who diverged ~35 million years from Old World primates and have a less elaborated frontal cortex. The common marmoset (Callithrix jacchus) is a small New World primate that is ideally placed to address this question given the complex social repertoire inherent to this species (e.g., observational social learning; imitation; cooperative antiphonal calling). Here, we investigated the existence of a putative high-level face processing network in marmosets by employing ultra-high field (9.4 Tesla) task-based functional MRI (fMRI). We demonstrated that, like Old World primates, marmosets show differential activation in anterior cingulate cortex and lateral prefrontal cortex while they view socially relevant videos of marmoset faces. We corroborate the locations of these frontal regions by demonstrating both functional (via resting-state fMRI) and structural (via cellular-level tracing) connectivity between these regions and temporal lobe face patches. Given the evolutionary separation between macaques and marmosets, our results suggest this frontal network specialized for social face processing predates the separation between Platyrrhini and Catarrhine. These results give further credence to the marmoset as a viable preclinical modelling species for studying human social disorders.

scholarly journals Phase of Firing Coding of Learning Variables across Prefrontal Cortex, Anterior Cingulate Cortex and Striatum during Feature Learning

2019 ◽  
Author(s):  
Benjamin Voloh ◽  
Mariann Oemisch ◽  
Thilo Womelsdorf
Keyword(s):  
Prefrontal Cortex ◽  
Anterior Cingulate Cortex ◽  
Long Range ◽  
Cingulate Cortex ◽  
Temporal Coding ◽  
Anterior Cingulate ◽  
Prediction Errors ◽  
Lateral Prefrontal Cortex ◽  
Firing Rates ◽  
Reward Prediction

AbstractThe prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected the network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that neurons encoding current choice outcomes, outcome prediction errors, and outcome history in their firing rates also carried significant information in their phase-of-firing at a 10-25 Hz beta frequency at which they synchronized across lateral prefrontal cortex, anterior cingulate cortex and striatum. The phase-of-firing code exceeded information that could be obtained from firing rates alone, was strong for inter-areal connections, and multiplexed information at three different phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document the multiplexing of three different types of information in the phase-of-firing at an interareally shared beta oscillation frequency during goal-directed behavior.HighlightsLateral prefrontal cortex, anterior cingulate cortex and striatum show phase-of-firing encoding for outcome, outcome history and reward prediction errors.Neurons with phase-of-firing code synchronize long-range at 10-25 Hz.Spike phases encoding reward prediction errors deviate from preferred synchronization phases.Anterior cingulate cortex neurons show strongest long-range effects.

scholarly journals Specific Contributions of Ventromedial, Anterior Cingulate, and Lateral Prefrontal Cortex for Attentional Selection and Stimulus Valuation

PLoS Biology ◽  
2011 ◽  
Vol 9 (12) ◽  
pp. e1001224 ◽  
Author(s):  
Daniel Kaping ◽  
Martin Vinck ◽  
R. Matthew Hutchison ◽  
Stefan Everling ◽  
Thilo Womelsdorf
Keyword(s):  
Prefrontal Cortex ◽  
Attentional Selection ◽  
Anterior Cingulate ◽  
Lateral Prefrontal Cortex

scholarly journals Context-invariant neural dynamics underlying the encoding of Bayesian uncertainty, but not confidence

2019 ◽  
Author(s):  
Vincenzo G. Fiore ◽  
Xiaosi Gu
Keyword(s):  
Prefrontal Cortex ◽  
Medial Prefrontal Cortex ◽  
Effective Connectivity ◽  
Sensory Information ◽  
Anterior Insula ◽  
Anterior Cingulate ◽  
Neural Dynamics ◽  
Network Computing ◽  
Evidence Accumulation ◽  
Healthy Humans

AbstractBeliefs about action-outcomes contingencies are often updated in opaque environments where feedbacks might be inaccessible and agents might need to rely on other information for evidence accumulation. It remains unclear, however, whether and how the neural dynamics subserving confidence and uncertainty during belief updating might be context-dependent. Here, we applied a Bayesian model to estimate uncertainty and confidence in healthy humans (n=28) using two multi-option fMRI tasks, one with and one without feedbacks. We found that across both tasks, uncertainty was computed in the anterior insular, anterior cingulate, and dorsolateral prefrontal cortices, whereas confidence was encoded in anterior hippocampus, amygdala and medial prefrontal cortex. However, dynamic causal modelling (DCM) revealed a critical divergence between how effective connectivity in these networks was modulated by the available information. Specifically, there was directional influence from the anterior insula to other regions during uncertainty encoding, independent of outcome availability. Conversely, the network computing confidence was driven either by the anterior hippocampus when outcomes were not available, or by the medial prefrontal cortex and amygdala when feedbacks were immediately accessible. These findings indicate that confidence encoding might largely rely on evidence accumulation and therefore dynamically changes as a function of the available sensory information (i.e. symbolic sequences monitored by the hippocampus, and monetary feedbacks computed by amygdala and medial prefrontal cortex). In contrast, uncertainty could be triggered by any information that disputes existing beliefs (i.e. processed in the insula), independent of its content.Significance StatementOur choices are guided by our beliefs about action-outcome contingencies. In environments where only one action leads to a desired outcome, high estimated action-outcome probabilities result in confidence, whereas low probabilities distributed across multiple choices result in uncertainty. These estimations are continuously updated, sometimes based on feedbacks provided by the environment, but sometimes this update takes place in opaque environments where feedbacks are not readily available. Here, we show that uncertainty computations are driven by the anterior insula, independent of feedback availability. Conversely, confidence encoding dynamically adapts to the information available, as we found it was driven either by the anterior hippocampus, when feedback was absent, or by the medial prefrontal cortex and amygdala, otherwise.

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