Parallel processing of working memory and temporal information by distinct types of cortical projection neurons

Bae, Jung Won; Jeong, Huijeong; Yoon, Young Ju; Bae, Chan Mee; Lee, Hyeonsu; Paik, Se-Bum; Jung, Min Whan

doi:10.1038/s41467-021-24565-z

Cited by 15 publications

(8 citation statements)

References 71 publications

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“…It seems that IT neurons are strongly engaged in preparatory stages of various tasks as they are more active in sensory regions during sensory sampling phases ( Musall et al, 2021 ; Mohan et al, 2022 ). This trend is consistent in other areas such as mPFC where they retain goal specific responses prior to action initiation ( Bae et al, 2021 ) and preparatory movement activities in motor structures ( Currie et al, 2021 ; Heindorf and Keller, 2022 ). Inhibiting the IT neurons during sampling periods only weakly affects the behavioral outcome, suggesting a minor role in regulating behavioral output.…”

Section: Behaviorsupporting

confidence: 83%

“…In recent years, there has been a surge of evidence of the distinct functional roles of IT and ET neurons in cognitive behavior ( Li et al, 2015 ; Takahashi et al, 2020 ; Bae et al, 2021 ; Currie et al, 2021 ; Musall et al, 2021 ; Heindorf and Keller, 2022 ; Mohan et al, 2022 ; Park et al, 2022 ). With recent development of combining whole-brain imaging with newly developed mouse lines, it is now possible to record brain-wide activity of IT neurons (including both L5 and L2/3 IT neurons) and L5 ET neurons.…”

Section: Behaviormentioning

confidence: 99%

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Neocortical layer 5 subclasses: From cellular properties to roles in behavior

Moberg

2022

Front. Synaptic Neurosci.

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Layer 5 (L5) serves as the main output layer of cortical structures, where long-range projecting pyramidal neurons broadcast the columnar output to other cortical and extracortical regions of the brain. L5 pyramidal neurons are grouped into two subclasses based on their projection targets; while intratelencephalic (IT) neurons project to cortical areas and the striatum, extratelencephalic (ET) neurons project to subcortical areas such as the thalamus, midbrain, and brainstem. Each L5 subclass possesses distinct morphological and electrophysiological properties and is incorporated into a unique synaptic network. Thanks to recent advances in genetic tools and methodologies, it has now become possible to distinguish between the two subclasses in the living brain. There is increasing evidence indicating that each subclass plays a unique role in sensory processing, decision-making, and learning. This review first summarizes the anatomical and physiological properties as well as the neuromodulation of IT and ET neurons in the rodent neocortex, and then reviews recent literature on their roles in sensory processing and rodent behavior. Our ultimate goal is to provide a comprehensive understanding of the role of each subclass in cortical function by examining their operational regimes based on their cellular properties.

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Section: Behaviorsupporting

confidence: 83%

Section: Behaviormentioning

confidence: 99%

Neocortical layer 5 subclasses: From cellular properties to roles in behavior

Moberg

2022

Front. Synaptic Neurosci.

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“…In this study, we found that the frontal lobe regions (including the ORBmid.L, ORBinf.R, and MFG.L) in MCI reverters showed increased ALFF and fALFF, while the cerebellum_9_R showed decreased ALFF and fALFF. The frontal lobe is thought to be involved in many high-level cognitive functions ( Bae et al, 2021 ; Wang Y. et al, 2021 ). Increased frontal cortex connectivity is considered to be associated with increased cognitive control, higher IQ, and higher cognitive performance in young individuals.…”

Section: Discussionmentioning

confidence: 99%

“…This suggests a reduced and increased, respectively, significance of these regions in the whole-brain. ITG.L and SFGmed.L regions are involved in memory tasks ( Sidhu et al, 2013 ; Bae et al, 2021 ), and the cerebellum, INS.L, and INS.R are more related to motor and attentional processes ( Wagner and Luo, 2020 ; Song et al, 2021 ). Previous studies have suggested that patients with AD may use other neurological resources to compensate for the loss of cognitive function in the early stages of the disease ( Grady et al, 2003 ).…”

Section: Discussionmentioning

confidence: 99%

Intrinsic Brain Activity Alterations in Patients With Mild Cognitive Impairment-to-Normal Reversion: A Resting-State Functional Magnetic Resonance Imaging Study From Voxel to Whole-Brain Level

Wang

et al. 2022

Front. Aging Neurosci.

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Mild cognitive impairment (MCI) reversion refers to patients with MCI who revert from MCI to a normal cognitive state. Exploring the underlying neuromechanism of MCI reverters may contribute to providing new insights into the pathogenesis of Alzheimer’s disease and developing therapeutic interventions. Information on patients with MCI and healthy controls (HCs) was collected from the Alzheimer’s Disease Neuroimaging Initiative database. We redefined MCI reverters as patients with MCI whose logical memory scores changed from MCI to normal levels using the logical memory criteria. We explored intrinsic brain activity alterations in MCI reverters from voxel, regional, and whole-brain levels by comparing resting-state functional magnetic resonance imaging metrics of the amplitude of low-frequency of fluctuation (ALFF), the fractional amplitude of low-frequency fluctuation (fALFF), percent amplitude of fluctuation (PerAF), regional homogeneity (ReHo), and degree centrality (DC) between MCI reverters and HCs. Finally, partial correlation analyses were conducted between cognitive scale scores and resting-state functional magnetic resonance imaging metrics of brain regions, revealing significant group differences. Thirty-two patients with MCI from the Alzheimer’s Disease Neuroimaging Initiative database were identified as reverters. Thirty-seven age-, sex-, and education-matched healthy individuals were also enrolled. At the voxel level, compared with the HCs, MCI reverters had increased ALFF, fALFF, and PerAF in the frontal gyrus (including the bilateral orbital inferior frontal gyrus and left middle frontal gyrus), increased PerAF in the left fusiform gyrus, and decreased ALFF and fALFF in the right inferior cerebellum. Regarding regional and whole-brain levels, MCI reverters showed increased ReHo in the left fusiform gyrus and right median cingulate and paracingulate gyri; increased DC in the left inferior temporal gyrus and left medial superior frontal; decreased DC in the right inferior cerebellum and bilateral insular gyrus relative to HCs. Furthermore, significant correlations were found between cognitive performance and neuroimaging changes. These findings suggest that MCI reverters show significant intrinsic brain activity changes compared with HCs, potentially related to the cognitive reversion of patients with MCI. These results enhance our understanding of the underlying neuromechanism of MCI reverters and may contribute to further exploration of Alzheimer’s disease.

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“…Since at least 10 sniffing trials were required for each group, neurons with less than 10 sniffing trials for any of left and right sidedness or social and object targets were removed from analysis. We have modified an open source code ( Bae et al, 2021 ), which uses MATLAB ‘fitcsvm’ function for SVM decoding.…”

Section: Methodsmentioning

confidence: 99%

Suppressed prefrontal neuronal firing variability and impaired social representation in IRSp53-mutant mice

Kim

Shin

Jeong

et al. 2022

eLife

Self Cite

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Social deficit is a major feature of neuropsychiatric disorders, including autism spectrum disorders, schizophrenia, and attention-deficit/hyperactivity disorder, but its neural mechanisms remain unclear. Here, we examined neuronal discharge characteristics in the medial prefrontal cortex (mPFC) of IRSp53/Baiap2-mutant mice, which show social deficits, during social approach. We found a decrease in the proportion of IRSp53-mutant excitatory mPFC neurons encoding social information, but not that encoding non-social information. In addition, the firing activity of IRSp53-mutant neurons was less differential between social and non-social targets. IRSp53-mutant excitatory mPFC neurons displayed an increase in baseline neuronal firing, but decreases in the variability and dynamic range of firing as well as burst firing during social and non-social target approaches compared to wild-type controls. Treatment of memantine, an NMDA receptor antagonist that rescues social deficit in IRSp53-mutant mice, alleviates the reduced burst firing of IRSp53-mutant pyramidal mPFC neurons. These results suggest that suppressed neuronal activity dynamics and burst firing may underlie impaired cortical encoding of social information and social behaviors in IRSp53-mutant mice.

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Parallel processing of working memory and temporal information by distinct types of cortical projection neurons

Cited by 15 publications

References 71 publications

Neocortical layer 5 subclasses: From cellular properties to roles in behavior

Neocortical layer 5 subclasses: From cellular properties to roles in behavior

Intrinsic Brain Activity Alterations in Patients With Mild Cognitive Impairment-to-Normal Reversion: A Resting-State Functional Magnetic Resonance Imaging Study From Voxel to Whole-Brain Level

Suppressed prefrontal neuronal firing variability and impaired social representation in IRSp53-mutant mice

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