Medial Orbitofrontal Cortex, Dorsolateral Prefrontal Cortex, and Hippocampus Differentially Represent the Event Saliency

Jafarpour, Anna; Griffin, Sandon; Lin, Jack J.; Knight, Robert T.

doi:10.1162/jocn_a_01392

Cited by 28 publications

(40 citation statements)

References 82 publications

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“…This likely explains why we did not observe synchronization using the ISC method, which would require more consistent temporal synchronization from the majority of the participants. Moreover, these results are also consistent with previous work that has found that the vmPFC may be involved in assessing the saliency of a particular event (Jafarpour et al, 2019).…”

Section: Discussionsupporting

confidence: 92%

“…Stimulation paradigms have implicated the involvement of the vmPFC in the subjective experience of affect, olfaction, and gustation (Fox et al, 2018;Yih et al, 2019). Naturalistic designs, such as passive movie watching, can provide rich contextual information, which makes them well suited for studying social, cognitive, and affective processes (Hasson et al, 2020;Jolly and Chang, 2019;Sonkusare et al, 2019), but have been rarely used in intracranial EEG research (Honey et al, 2012;Jafarpour et al, 2019;Mukamel et al, 2005). The majority of work using naturalistic designs has instead focused on characterizing sensory processes in auditory cortex and found that power in high frequency bands, such as gamma ( ), positively correlate with the envelope of the auditory stimulus (Honey et al, 2012) and also with fluctuations in the BOLD response in auditory cortex of other participants viewing the same stimulus while undergoing fMRI (Mukamel et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Minimal functional alignment of ventromedial prefrontal cortex intracranial EEG signals during naturalistic viewing

Xie

Cheong

Manning

et al. 2021

Preprint

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The ventromedial prefrontal cortex (vmPFC) has been thought to play an important role in processing endogenous information such as generating subjective affective meaning. Unlike sensory cortex, which processes exogenous information about the external world similarly across individuals, prior work has posited that vmPFC activity may be idiosyncratic to each individual, even when exposed to the same external stimulus. In this study, we recorded local field potentials (LFPs) from intracranial stereo electrodes implanted in patients with intractable epilepsy while they watched an emotionally engaging television show episode and evaluated temporal synchronization of these signals across participants in auditory cortex and vmPFC. Overall, we observed markedly lower intersubject synchronization of signals recorded from electrodes implanted in vmPFC compared to auditory cortex. A subset of patients, however, appeared to share similar vmPFC states during the more emotionally salient scenes. This work suggests that the vmPFC is involved in processing affective responses to ongoing experience in a state-like manner, but the specific states and temporal sequences are idiosyncratic to each individual, even when viewing the same television episode.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Minimal functional alignment of ventromedial prefrontal cortex intracranial EEG signals during naturalistic viewing

Xie

Cheong

Manning

et al. 2021

Preprint

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“…Discussion SHIN (2020) ___________________________________________________________________________ Pastalkova et al, 2008). Lastly, salient or novel events are shown to engage hippocampal activity (Dolan and Fletcher, 1997;Jafarpour et al, 2019;Kumaran and Maguire, 2006;Ranganath and D'Esposito, 2001). Although we speculate that microstimulation evokes a similar sensation induced by natural stimuli, the initial high intensity of microstimulation might induce a novel sensation that animals had never experienced before.…”

Section: Shin (2020) ___________________________________________________________________________mentioning

confidence: 76%

Perirhinal input to neocortical layer 1 controls learning

Doron

Shin

Takahashi

et al. 2020

Science

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Declarative memory formation is believed to rely on interactions between the medial temporal lobe (MTL) and neocortex. However, the distributed nature of neocortical networks has hindered investigation on cellular targets and mechanisms of memory formation in the neocortex. The six-layered mammalian neocortex has an anatomical organization in which top-down inputs converge on its outermost layer, layer 1 (L1). We investigated this organization to examine how layer-specific MTL inputs modulate neocortical activity and memory formation. To this end, we first adapted a cortical-and hippocampal-dependent learning paradigm, in which animals were trained to associate direct cortical microstimulation and reward, and characterized learning behavior of rats and mice during this task. We next showed that neurons in the deep layers of the perirhinal cortex not only provide monosynaptic inputs to L1 of the primary somatosensory cortex (S1), where microstimulation was presented, but also actively reflect the behavioral outcome. Chemogenetic suppression of perirhinal inputs to L1 of S1 disrupted early memory formation but did not affect animals' performance after learning. The learning was followed by an emergence of a distinct subpopulation of layer 5 (L5) pyramidal neurons (~10%) characterized by high-frequency burst firing, which could be reduced by blocking perirhinal inputs to L1. Interestingly, similar proportion of apical dendrites (~10%) of L5 pyramidal neurons also displayed significantly enhanced calcium (Ca 2+ ) activity during memory retrieval in expert animals. Importantly, disrupting dendritic Ca 2+ activity impaired learning, suggesting that apical dendrites of L5 pyramidal neurons have a critical role in neocortical memory formation. Taken together, these results suggest that MTL inputs control learning via a perirhinal-mediated gating process in L1, manifested by elevated dendritic Ca 2+ activity and burst firing in L5 pyramidal neurons. The present study provides insights into cellular mechanisms of learning and memory representations in the neocortex. Zusammenfassung SHIN (2020) ___________________________________________________________________________ 2 Zusammenfassung Es wird angenommen, dass deklarative Gedächtnisbildung auf Wechselwirkungen zwischen dem medialen Temporallappens (MTL) und dem Neokortex beruht. Die Untersuchung der zellulären Ziele und Mechanismen von Gedächtnisbildung im Neokortex wird erschwert durch die über den Kortex verteilte Struktur neokortikaler Netzwerke. Der in sechs Schichten gegliederte Neokortex von Säugetieren besitzt eine anatomische Organisation, in der Top-Down-Inputs inseiner äußersten Schicht, Schicht 1 (L1), konvergieren. Wir haben diese Organisation untersucht, um zu verstehen, wie schichtspezifische MTL-Inputs die neokortikale Aktivität und die Gedächtnisbildung modulieren. Zu diesem Zweck haben wir ein Kortex-und Hippocampus-abhängiges Lernparadigma angepasst, in dem Tiere darauf trainiert wurden, direkte kortikale Mikrostimulation und Belohnung zu assoziieren, und...

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“…As described for improved auditory perception, the process of accentuation of auditory stimuli that leads to central neural gain may require the co-activation of the basal forebrain to amplify stimulus-induced responses at subcortical and cortical levels ( Figure 3 , BasF blue downward arrow and cross) ( Kilgard et al, 2002 ; Bajo et al, 2014 ; Kraus and White-Schwoch, 2015 ; Irvine, 2018a ). Also, the activation of the inferior frontal gyrus (IFG), as part of the prefrontal cortex (PFC) ( Figure 3 , IFG), is crucial to retaining temporal and spatial associations of auditory events during auditory perception ( Schonwiesner et al, 2007 ; Malmierca et al, 2014 ; Jafarpour et al, 2019 ). In general, the activation of PFC brain regions during perception is crucial to memorizing behaviorally relevant signals and increasing synaptic strength ( Kraus and White-Schwoch, 2015 ; Weinberger, 2015 ; Irvine, 2018b ).…”

Section: Altered Excitation and Inhibition After Acoustic Trauma And Age-related Hearing Loss Are Linked To Increased Central Neural Gainmentioning

confidence: 99%

Disturbed Balance of Inhibitory Signaling Links Hearing Loss and Cognition

Knipper

Singer

Schwabe

et al. 2022

Front. Neural Circuits

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Neuronal hyperexcitability in the central auditory pathway linked to reduced inhibitory activity is associated with numerous forms of hearing loss, including noise damage, age-dependent hearing loss, and deafness, as well as tinnitus or auditory processing deficits in autism spectrum disorder (ASD). In most cases, the reduced central inhibitory activity and the accompanying hyperexcitability are interpreted as an active compensatory response to the absence of synaptic activity, linked to increased central neural gain control (increased output activity relative to reduced input). We here suggest that hyperexcitability also could be related to an immaturity or impairment of tonic inhibitory strength that typically develops in an activity-dependent process in the ascending auditory pathway with auditory experience. In these cases, high-SR auditory nerve fibers, which are critical for the shortest latencies and lowest sound thresholds, may have either not matured (possibly in congenital deafness or autism) or are dysfunctional (possibly after sudden, stressful auditory trauma or age-dependent hearing loss linked with cognitive decline). Fast auditory processing deficits can occur despite maintained basal hearing. In that case, tonic inhibitory strength is reduced in ascending auditory nuclei, and fast inhibitory parvalbumin positive interneuron (PV-IN) dendrites are diminished in auditory and frontal brain regions. This leads to deficits in central neural gain control linked to hippocampal LTP/LTD deficiencies, cognitive deficits, and unbalanced extra-hypothalamic stress control. Under these conditions, a diminished inhibitory strength may weaken local neuronal coupling to homeostatic vascular responses required for the metabolic support of auditory adjustment processes. We emphasize the need to distinguish these two states of excitatory/inhibitory imbalance in hearing disorders: (i) Under conditions of preserved fast auditory processing and sustained tonic inhibitory strength, an excitatory/inhibitory imbalance following auditory deprivation can maintain precise hearing through a memory linked, transient disinhibition that leads to enhanced spiking fidelity (central neural gain⇑) (ii) Under conditions of critically diminished fast auditory processing and reduced tonic inhibitory strength, hyperexcitability can be part of an increased synchronization over a broader frequency range, linked to reduced spiking reliability (central neural gain⇓). This latter stage mutually reinforces diminished metabolic support for auditory adjustment processes, increasing the risks for canonical dementia syndromes.

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Medial Orbitofrontal Cortex, Dorsolateral Prefrontal Cortex, and Hippocampus Differentially Represent the Event Saliency

Cited by 28 publications

References 82 publications

Minimal functional alignment of ventromedial prefrontal cortex intracranial EEG signals during naturalistic viewing

Minimal functional alignment of ventromedial prefrontal cortex intracranial EEG signals during naturalistic viewing

Perirhinal input to neocortical layer 1 controls learning

Disturbed Balance of Inhibitory Signaling Links Hearing Loss and Cognition

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