{"title":"Erratum: van Geen et al., \"Lesions to Different Regions of the Frontal Cortex Have Dissociable Effects on Voluntary Persistence in Humans\".","authors":"","doi":"10.1523/JNEUROSCI.1544-25.2025","DOIUrl":"10.1523/JNEUROSCI.1544-25.2025","url":null,"abstract":"","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-09-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12410034/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144976781","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Monami Nishio, Monica E Ellwood-Lowe, Mackenzie Woodburn, Cassidy L McDermott, Anne T Park, Ursula A Tooley, Austin L Boroshok, Joanes Grandjean, Allyson P Mackey
{"title":"The development of neural inhibition across species: insights from the Hurst exponent.","authors":"Monami Nishio, Monica E Ellwood-Lowe, Mackenzie Woodburn, Cassidy L McDermott, Anne T Park, Ursula A Tooley, Austin L Boroshok, Joanes Grandjean, Allyson P Mackey","doi":"10.1523/JNEUROSCI.0025-25.2025","DOIUrl":"10.1523/JNEUROSCI.0025-25.2025","url":null,"abstract":"<p><p>The maturation of inhibitory neurons is crucial for regulating plasticity in developing brains. Previous work has suggested that the Hurst exponent, the measure of autocorrelation in time series, reflects inhibition, but empirical data supporting this link is sparse. Here, we demonstrate significant spatial correlations between the Hurst exponent and ex vivo parvalbumin inhibitory mRNA expression in human children and adults, as well as between the Hurst exponent and parvalbumin-positive cell counts in mice, across both sexes. We further identified developmental plateaus in inhibition, as indicated by both parvalbumin inhibitory mRNA expression and the Hurst exponent, occurring prior to adolescence in humans and rats. In sum, this work suggests that the Hurst exponent can be used to study the development of inhibition in vivo, and to understand inhibitory development across species.<b>Significance Statement</b> Understanding the spatial and temporal progression of developmental plasticity is crucial for identifying periods of vulnerability and opportunity in the human brain. This study supports the Hurst exponent as a promising in vivo marker for inhibition, showing significant spatial correlations with parvalbumin RNA expression and cell counts across species. Findings indicate a plateau in inhibition by late childhood in humans and prior to puberty in rats, suggesting the Hurst exponent's translational potential for exploring inhibitory development mechanisms in both humans and animals.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144976934","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Erratum: van Geen et al., \"Lesions to Different Regions of the Frontal Cortex Have Dissociable Effects on Voluntary Persistence in Humans\".","authors":"","doi":"10.1523/jneurosci.1544-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.1544-25.2025","url":null,"abstract":"","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"24 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960086","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Maeve R Boylan,Anna-Lena Tebbe,Jamie Newland,Jessica Sanches Braga Figueira,Andreas Keil,Lisa S Scott
{"title":"Competitive cortical prioritization emerges for trained objects across the first year of life.","authors":"Maeve R Boylan,Anna-Lena Tebbe,Jamie Newland,Jessica Sanches Braga Figueira,Andreas Keil,Lisa S Scott","doi":"10.1523/jneurosci.2314-24.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.2314-24.2025","url":null,"abstract":"Learning to detect and recognize a broad range of visual objects is a crucial developmental task during the first year of life. However, many of the neurophysiological changes underlying the emergence of this cognitive ability remain poorly understood. The current study tested the hypothesis that training infants to recognize novel objects leads to selectively enhanced visuocortical responses and a competitive advantage that prioritizes the processing of trained relative to untrained objects. A cross-sectional sample of parent-infant dyads at 6-, 9-, and 12-months of age read books in which novel objects were associated with different types of labels. The next day, EEG was recorded while infants (N = 51, 24 females and 26 males, 1 unknown) were concurrently presented with trained objects (i.e., from the book) and untrained objects (i.e., novel objects not in the book). Trained and untrained objects flickered at distinct frequencies (5 Hz, 6 Hz) to evoke frequency-tagged steady-state visual evoked potentials (ssVEPs). Analyses of the visuocortical response showed training-related competition effects that increased with age. Specifically, responses to trained stimuli increased while responses to untrained stimuli decreased with age. At 6 months, infants showed no visuocortical bias for trained objects, but by 9 and 12 months, visuocortical responses favored trained objects. This pattern suggests that competitive neural interactions between trained and untrained stimuli may support the development of object recognition and that experience with objects guides attentional prioritization in the infant brain.Significance Statement The present investigation suggests that as infants age, experience with images of objects impacts the selective prioritization of visuocortical resources. Here, learned objects receive increasing attentional priority over a novel object with age. These competitive visuocortical interactions support the development of object recognition throughout the first year of life.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"43 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960087","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Network Activity Shapes Inhibitory Synaptic Development in the Mouse Hippocampus.","authors":"Erin M Johnson-Venkatesh, Hisashi Umemori","doi":"10.1523/JNEUROSCI.1182-24.2025","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.1182-24.2025","url":null,"abstract":"<p><p>The proper development of excitatory/inhibitory balance is critical for brain function, as any imbalance has been associated with myriad neuropsychiatric disorders. How this balance evolves during synaptic development remains unclear. To address this question, we examine how manipulations of SIRPα, a cell-adhesion molecule that organizes excitatory synaptic development in the hippocampus, affect inhibitory synaptogenesis to maintain excitatory/inhibitory balance, using mice of either sex. SIRPα primarily localizes to excitatory synapses. Overexpression or inactivation of SIRPα in a single neuron in hippocampal cultures affects excitatory, but not inhibitory synapses formed onto the SIRPα-manipulated neuron, indicating that SIRPα is an excitatory, but not inhibitory, synapse organizer. Despite this, bath application of SIRPα's ectodomain increases inhibitory synapses in culture, and global inactivation of SIRPα <i>in-vitro</i> and <i>in-vivo</i> during critical periods functionally decreases both excitatory and inhibitory synapses in the hippocampus. By using various conditional KO mice, we found that SIRPα from pyramidal neurons, but not from inhibitory interneurons, astrocytes, or microglia is necessary for proper inhibitory synapse development. Interestingly, inactivation of SIRPα from most pyramidal neurons is necessary to impact inhibitory synaptic development, suggesting that inhibitory synaptogenesis in the hippocampus is driven by the strength of excitation in the pyramidal-neuron network, and not by a change in excitatory input to a single cell. Consistently, the effect of SIRPα's ectodomain on inhibitory, but not excitatory synaptogenesis is blocked by global neural activity inhibition. We propose that the development of inhibitory synapses in the hippocampus is regulated by network-level excitatory activity to evolve excitatory/inhibitory balance.<b>Significance Statement</b> How excitatory/inhibitory (E/I) balance evolves during development is still unknown. We manipulated an excitatory synapse organizing cell-adhesion molecule, SIRPα, in the hippocampus and examined how inhibitory synaptogenesis is affected to maintain E/I balance. Global inactivation of SIRPα during a critical period functionally decreases both excitatory and inhibitory synapses. Using many mouse mutants and manipulations, we identified that inactivation of SIRPα from most pyramidal neurons is necessary to impact inhibitory synaptogenesis and that the effect of SIRPα on inhibitory synaptogenesis is blocked by global neural activity inhibition. Therefore, we propose that inhibitory synaptogenesis is regulated by the excitatory drive at the network level and not at the single-cell level. Our work reveals a fundamental mechanism that develops E/I balance.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144976846","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Monami Nishio,Monica E Ellwood-Lowe,Mackenzie Woodburn,Cassidy L McDermott,Anne T Park,Ursula A Tooley,Austin L Boroshok,Joanes Grandjean,Allyson P Mackey
{"title":"The development of neural inhibition across species: insights from the Hurst exponent.","authors":"Monami Nishio,Monica E Ellwood-Lowe,Mackenzie Woodburn,Cassidy L McDermott,Anne T Park,Ursula A Tooley,Austin L Boroshok,Joanes Grandjean,Allyson P Mackey","doi":"10.1523/jneurosci.0025-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.0025-25.2025","url":null,"abstract":"The maturation of inhibitory neurons is crucial for regulating plasticity in developing brains. Previous work has suggested that the Hurst exponent, the measure of autocorrelation in time series, reflects inhibition, but empirical data supporting this link is sparse. Here, we demonstrate significant spatial correlations between the Hurst exponent and ex vivo parvalbumin inhibitory mRNA expression in human children and adults, as well as between the Hurst exponent and parvalbumin-positive cell counts in mice, across both sexes. We further identified developmental plateaus in inhibition, as indicated by both parvalbumin inhibitory mRNA expression and the Hurst exponent, occurring prior to adolescence in humans and rats. In sum, this work suggests that the Hurst exponent can be used to study the development of inhibition in vivo, and to understand inhibitory development across species.Significance Statement Understanding the spatial and temporal progression of developmental plasticity is crucial for identifying periods of vulnerability and opportunity in the human brain. This study supports the Hurst exponent as a promising in vivo marker for inhibition, showing significant spatial correlations with parvalbumin RNA expression and cell counts across species. Findings indicate a plateau in inhibition by late childhood in humans and prior to puberty in rats, suggesting the Hurst exponent's translational potential for exploring inhibitory development mechanisms in both humans and animals.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"32 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960085","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Network Activity Shapes Inhibitory Synaptic Development in the Mouse Hippocampus.","authors":"Erin M Johnson-Venkatesh,Hisashi Umemori","doi":"10.1523/jneurosci.1182-24.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.1182-24.2025","url":null,"abstract":"The proper development of excitatory/inhibitory balance is critical for brain function, as any imbalance has been associated with myriad neuropsychiatric disorders. How this balance evolves during synaptic development remains unclear. To address this question, we examine how manipulations of SIRPα, a cell-adhesion molecule that organizes excitatory synaptic development in the hippocampus, affect inhibitory synaptogenesis to maintain excitatory/inhibitory balance, using mice of either sex. SIRPα primarily localizes to excitatory synapses. Overexpression or inactivation of SIRPα in a single neuron in hippocampal cultures affects excitatory, but not inhibitory synapses formed onto the SIRPα-manipulated neuron, indicating that SIRPα is an excitatory, but not inhibitory, synapse organizer. Despite this, bath application of SIRPα's ectodomain increases inhibitory synapses in culture, and global inactivation of SIRPα in-vitro and in-vivo during critical periods functionally decreases both excitatory and inhibitory synapses in the hippocampus. By using various conditional KO mice, we found that SIRPα from pyramidal neurons, but not from inhibitory interneurons, astrocytes, or microglia is necessary for proper inhibitory synapse development. Interestingly, inactivation of SIRPα from most pyramidal neurons is necessary to impact inhibitory synaptic development, suggesting that inhibitory synaptogenesis in the hippocampus is driven by the strength of excitation in the pyramidal-neuron network, and not by a change in excitatory input to a single cell. Consistently, the effect of SIRPα's ectodomain on inhibitory, but not excitatory synaptogenesis is blocked by global neural activity inhibition. We propose that the development of inhibitory synapses in the hippocampus is regulated by network-level excitatory activity to evolve excitatory/inhibitory balance.Significance Statement How excitatory/inhibitory (E/I) balance evolves during development is still unknown. We manipulated an excitatory synapse organizing cell-adhesion molecule, SIRPα, in the hippocampus and examined how inhibitory synaptogenesis is affected to maintain E/I balance. Global inactivation of SIRPα during a critical period functionally decreases both excitatory and inhibitory synapses. Using many mouse mutants and manipulations, we identified that inactivation of SIRPα from most pyramidal neurons is necessary to impact inhibitory synaptogenesis and that the effect of SIRPα on inhibitory synaptogenesis is blocked by global neural activity inhibition. Therefore, we propose that inhibitory synaptogenesis is regulated by the excitatory drive at the network level and not at the single-cell level. Our work reveals a fundamental mechanism that develops E/I balance.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"7 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-09-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960296","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nathan J Stevenson,Kartik Iyer,Anton Tokariev,James A Roberts,Sampsa Vanhatalo
{"title":"Maturation of neuronal activity in the human cortex exhibits robust spatial gradients across the birth transition.","authors":"Nathan J Stevenson,Kartik Iyer,Anton Tokariev,James A Roberts,Sampsa Vanhatalo","doi":"10.1523/jneurosci.0610-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.0610-25.2025","url":null,"abstract":"Early structural and molecular development of the human cortex is extensively studied, but little is known about the development of neuronal activity across cortical regions. We used dense array electroencephalography recordings and a machine-learning-based measure, functional brain age (FBA), to study spatiotemporally resolved maturation of cortical activity across the birth transition in human infants (male and female). We found clear spatial FBA gradients indicating more mature frontal cortical activity relative to other brain regions (geometric axis), as well as more mature activity in association cortices relative to sensory cortices (hierarchical axis). The frontal advance was explained by more mature bursting characteristics, a hallmark of early endogenous neuronal activity. The findings jointly support an advanced maturation of neuronal ensemble activity in cortical regions that are preparing to host synergistic, large-scale network interactions, a key global characteristic of mature brain function.Significance Statement Orderly brain organization from late pregnancy to early infancy is of paramount importance for optimal lifelong health. These complex processes are driven by brain activity, but surprisingly little is known about maturation of this activity across brain regions. We used high-density electroencephalography recordings and machine learning-based measures of brain age to study regionally specific maturation in the developing brain. We showed that frontal and central regions are more mature than other brain regions with these differences largely driven by characteristics of bursts of brain activity. While challenging common ideas about delayed frontal development, our findings suggest that the early maturation in bursts of activity in frontal regions reflects its upcoming roles in the large-scale organization of the brain.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"20 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960060","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Nathan J Stevenson, Kartik Iyer, Anton Tokariev, James A Roberts, Sampsa Vanhatalo
{"title":"Maturation of neuronal activity in the human cortex exhibits robust spatial gradients across the birth transition.","authors":"Nathan J Stevenson, Kartik Iyer, Anton Tokariev, James A Roberts, Sampsa Vanhatalo","doi":"10.1523/JNEUROSCI.0610-25.2025","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.0610-25.2025","url":null,"abstract":"<p><p>Early structural and molecular development of the human cortex is extensively studied, but little is known about the development of neuronal activity across cortical regions. We used dense array electroencephalography recordings and a machine-learning-based measure, functional brain age (FBA), to study spatiotemporally resolved maturation of cortical activity across the birth transition in human infants (male and female). We found clear spatial FBA gradients indicating more mature frontal cortical activity relative to other brain regions (geometric axis), as well as more mature activity in association cortices relative to sensory cortices (hierarchical axis). The frontal advance was explained by more mature bursting characteristics, a hallmark of early endogenous neuronal activity. The findings jointly support an advanced maturation of neuronal ensemble activity in cortical regions that are preparing to host synergistic, large-scale network interactions, a key global characteristic of mature brain function.<b>Significance Statement</b> Orderly brain organization from late pregnancy to early infancy is of paramount importance for optimal lifelong health. These complex processes are driven by brain activity, but surprisingly little is known about maturation of this activity across brain regions. We used high-density electroencephalography recordings and machine learning-based measures of brain age to study regionally specific maturation in the developing brain. We showed that frontal and central regions are more mature than other brain regions with these differences largely driven by characteristics of bursts of brain activity. While challenging common ideas about delayed frontal development, our findings suggest that the early maturation in bursts of activity in frontal regions reflects its upcoming roles in the large-scale organization of the brain.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144976838","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Beyond divisive normalization: Scalable feed-forward networks for multisensory integration across reference frames.","authors":"Arefeh Farahmandi,Parisa Abedi Khoozani,Gunnar Blohm","doi":"10.1523/jneurosci.0104-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.0104-25.2025","url":null,"abstract":"The integration of multiple sensory inputs is essential for human perception and action in uncertain environments. This process includes reference frame transformations as different sensory signals are encoded in different coordinate systems. Studies have shown multisensory integration in humans is consistent with Bayesian optimal inference. However, neural mechanisms underlying this process are still debated. Different population coding models have been proposed to implement probabilistic inference. This includes a recent suggestion that explicit divisive normalization accounts for empirical principles of multisensory integration. However, whether and how divisive operations are implemented in the brain is not well understood. Indeed, all existing models suffer from the curse of dimensionality and thus fail to scale to real-world problems. Here, we propose an alternative model for multisensory integration that approximates Bayesian inference: a multilayer-feedforward neural network of multisensory integration (MSI) across different reference frames trained on the analytical Bayesian solution. This model displays all empirical principles of multisensory integration and produces similar behavior to that reported in Ventral Intraparietal (VIP) neurons in the brain. The model achieved this without a neatly organized and regular connectivity structure between contributing neurons, such as required by explicit divisive normalization. Overall, we show that simple feedforward networks of purely additive units can approximate optimal inference across different reference frames through parallel computing principles. This suggests that it is not necessary for the brain to use explicit divisive normalization to achieve multisensory integration.Significance Statement This research presents an alternative model to divisive normalization models of multisensory integration in the brain. Our study demonstrates that a feed-forward neural network can achieve optimal multisensory integration across different reference frames without explicitly implementing divisive operations, challenging the long-held assumption that such operations are necessary for multisensory integration. The model displays all the empirical principles of multisensory integration, producing similar behavior to that reported in Ventral Intraparietal (VIP) neurons in the brain. This work offers profound insights into the putative neural computations underlying multisensory processing.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"24 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-08-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144960067","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}