Zachariah R Cross, Randolph F Helfrich, Andrew W Corcoran, Adam J O Dede, Mark J Kohler, Scott W Coussens, Lena Zou-Williams, Matthias Schlesewsky, M Gareth Gaskell, Robert T Knight, Ina Bornkessel-Schlesewsky
{"title":"Slow oscillation-spindle coupling predicts sequence-based language learning.","authors":"Zachariah R Cross, Randolph F Helfrich, Andrew W Corcoran, Adam J O Dede, Mark J Kohler, Scott W Coussens, Lena Zou-Williams, Matthias Schlesewsky, M Gareth Gaskell, Robert T Knight, Ina Bornkessel-Schlesewsky","doi":"10.1523/JNEUROSCI.2193-23.2024","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.2193-23.2024","url":null,"abstract":"<p><p>Sentence comprehension involves the rapid decoding of both semantic and grammatical information, a process fundamental to communication. As with other complex cognitive processes, language comprehension relies, in part, on long-term memory. However, the electrophysiological mechanisms underpinning the initial encoding and generalisation of higher-order linguistic knowledge remain elusive, particularly from a sleep-based consolidation perspective. One candidate mechanism that may support the consolidation of higher-order language is the temporal coordination of slow oscillations (SO) and sleep spindles during non-rapid eye movement sleep (NREM). To examine this hypothesis, we analysed electroencephalographic (EEG) data recorded from 35 participants (M<sub>age</sub> = 25.4, SD = 7.10; 16 males) during an artificial language learning task, contrasting performance between individuals who were given an 8hr nocturnal sleep period or an equivalent period of wake. We found that sleep relative to wake was associated with superior performance for rules that followed a sequence-based word order. Post-sleep sequence-based word order processing was further associated with less task-related theta desynchronisation, an electrophysiological signature of successful memory consolidation, as well as cognitive control and working memory. Frontal NREM SO-spindle coupling was also positively associated with behavioural sensitivity to sequence-based word order rules, as well as with task-related theta power. As such, theta activity during retrieval of previously learned information correlates with SO-spindle coupling, thus linking neural activity in the sleeping and waking brain. Taken together, this study presents converging behavioral and neurophysiological evidence for a role of NREM SO-spindle coupling and task-related theta activity as signatures of successful memory consolidation and retrieval in the context of higher-order language learning.<b>Significance statement</b> The endogenous temporal coordination of neural oscillations supports information processing during both wake and sleep states. Here we demonstrate that slow oscillation-spindle coupling during non-rapid eye movement sleep predicts the consolidation of complex grammatical rules and modulates task-related oscillatory dynamics previously implicated in sentence processing. We show that increases in theta power predict enhanced sensitivity to grammatical violations after a period of sleep and strong slow oscillation-spindle coupling modulates subsequent task-related theta activity to influence behaviour. Our findings reveal a complex interaction between both wake- and sleep-related oscillatory dynamics during the early stages of language learning beyond the single word level.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142689531","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}
Jessica Heeman, Brian J White, Stefan Van der Stigchel, Jan Theeuwes, Laurent Itti, Douglas P Munoz
{"title":"Saliency response in superior colliculus at the future saccade goal predicts fixation duration during free viewing of dynamic scenes.","authors":"Jessica Heeman, Brian J White, Stefan Van der Stigchel, Jan Theeuwes, Laurent Itti, Douglas P Munoz","doi":"10.1523/JNEUROSCI.0428-24.2024","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.0428-24.2024","url":null,"abstract":"<p><p>Eye movements in daily life occur in rapid succession and often without a predefined goal. Using a free viewing task, we examined how fixation duration prior to a saccade correlates to visual saliency and neuronal activity in the superior colliculus (SC) at the saccade goal. Rhesus monkeys (three male) watched videos of natural, dynamic, scenes while eye movements were tracked and, simultaneously, neurons were recorded in the superficial and intermediate layers of the superior colliculus (SCs and SCi respectively), a midbrain structure closely associated with gaze, attention, and saliency coding. Saccades that were directed into the neuron's receptive field (RF) were extrapolated from the data. To interpret the complex visual input, saliency at the RF location was computed during the pre-saccadic fixation period using a computational saliency model. We analyzed if visual saliency and neural activity at the saccade goal predicted pre-saccadic fixation duration. We report three major findings: 1) Saliency at the saccade goal inversely correlated with fixation duration, with motion and edge information being the strongest predictors. 2) SC visual saliency responses in both SCs and SCi were inversely related to fixation duration. 3) SCs neurons, and not SCi neurons, showed higher activation for two consecutive short fixations, suggestive of concurrent saccade processing during free viewing. These results reveal a close correspondence between visual saliency, SC processing, and the timing of saccade initiation during free viewing and are discussed in relation to their implication for understanding saccade initiation during real-world gaze behavior.<b>Significance statement</b> Contrary to traditional controlled stimuli/task studies, eye movements in day-to-day life are not discrete events but occur in (rapid) succession and often without a predefined goal. Therefore, the study of visual processing during free viewing of dynamic scenes is an essential step in understanding visual processing in its functional context. We present an investigation into saliency and visual responses in the superior colliculus (SC) during task-free viewing of dynamic videos and their correspondence to saccade initiation. In short, these results show the correspondence between fixation duration, pre-saccadic visual saliency at the saccade goal and SC processing and provide first evidence of a neural correlate of concurrent visual processing across a chain of saccades in the SC during free viewing.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142689524","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}
Mariana R Tavares, Willian O Dos Santos, Isadora C Furigo, Edward O List, John J Kopchick, Jose Donato
{"title":"Growth Hormone Receptor in Lateral Hypothalamic Neurons Is Required for Increased Food-Seeking Behavior during Food Restriction in Male Mice.","authors":"Mariana R Tavares, Willian O Dos Santos, Isadora C Furigo, Edward O List, John J Kopchick, Jose Donato","doi":"10.1523/JNEUROSCI.1761-23.2024","DOIUrl":"10.1523/JNEUROSCI.1761-23.2024","url":null,"abstract":"<p><p>Growth hormone (GH) action in the brain regulates neuroendocrine axes, energy and glucose homeostasis, and several neurological functions. The lateral hypothalamic area (LHA) contains numerous neurons that respond to a systemic GH injection by expressing the phosphorylated STAT5, a GH receptor (GHR) signaling marker. However, the potential role of GHR signaling in the LHA is unknown. In this study, we demonstrated that ∼70% of orexin- and leptin receptor (LepR)-expressing neurons in the LHA are responsive to GH. Male mice carrying inactivation of the <i>Ghr</i> gene in the LHA were generated via bilateral injections of an adeno-associated virus. In <i>ad libitum</i>-fed mice, GHR ablation in LHA neurons did not significantly change energy and glucose homeostasis. Subsequently, mice were subjected to 5 d of 40% food restriction. Food restriction decreased body weight, energy expenditure, and carbohydrate oxidation. These effects were similarly observed in control and LHA<sup>ΔGHR</sup> mice. While food-deprived control mice progressively increased ambulatory/exploratory activity and food-seeking behavior, LHA<sup>ΔGHR</sup> mice did not show hyperactivity induced by food restriction. GHR ablation in the LHA reduced the percentage of orexin neurons expressing c-Fos during food restriction. Additionally, an acute GH injection increased the expression of c-Fos in LHA<sup>ORX</sup> neurons. Inactivation of <i>Ghr</i> in LepR-expressing cells did not prevent hyperactivity in food-deprived mice, whereas whole-brain <i>Ghr</i> knock-out mice showed reduced ambulatory activity during food restriction. Our findings indicate that GHR signaling in the LHA regulates the activity of orexin neurons and is necessary to increase food-seeking behavior in food-deprived male mice.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580784/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142367203","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}
{"title":"Expression of Concern: L'Episcopo et al., \"Plasticity of Subventricular Zone Neuroprogenitors in MPTP (1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine) Mouse Model of Parkinson's Disease Involves Cross Talk between Inflammatory and Wnt/β-Catenin Signaling Pathways: Functional Consequences for Neuroprotection and Repair\".","authors":"","doi":"10.1523/JNEUROSCI.2033-24.2024","DOIUrl":"10.1523/JNEUROSCI.2033-24.2024","url":null,"abstract":"","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580761/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142631364","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}
Garret Lynn Kurteff, Alyssa M Field, Saman Asghar, Elizabeth C Tyler-Kabara, Dave Clarke, Howard L Weiner, Anne E Anderson, Andrew J Watrous, Robert J Buchanan, Pradeep N Modur, Liberty S Hamilton
{"title":"Spatiotemporal Mapping of Auditory Onsets during Speech Production.","authors":"Garret Lynn Kurteff, Alyssa M Field, Saman Asghar, Elizabeth C Tyler-Kabara, Dave Clarke, Howard L Weiner, Anne E Anderson, Andrew J Watrous, Robert J Buchanan, Pradeep N Modur, Liberty S Hamilton","doi":"10.1523/JNEUROSCI.1109-24.2024","DOIUrl":"10.1523/JNEUROSCI.1109-24.2024","url":null,"abstract":"<p><p>The human auditory cortex is organized according to the timing and spectral characteristics of speech sounds during speech perception. During listening, the posterior superior temporal gyrus is organized according to onset responses, which segment acoustic boundaries in speech, and sustained responses, which further process phonological content. When we speak, the auditory system is actively processing the sound of our own voice to detect and correct speech errors in real time. This manifests in neural recordings as suppression of auditory responses during speech production compared with perception, but whether this differentially affects the onset and sustained temporal profiles is not known. Here, we investigated this question using intracranial EEG recorded from seventeen pediatric, adolescent, and adult patients with medication-resistant epilepsy while they performed a reading/listening task. We identified onset and sustained responses to speech in the bilateral auditory cortex and observed a selective suppression of onset responses during speech production. We conclude that onset responses provide a temporal landmark during speech perception that is redundant with forward prediction during speech production and are therefore suppressed. Phonological feature tuning in these \"onset suppression\" electrodes remained stable between perception and production. Notably, auditory onset responses and phonological feature tuning were present in the posterior insula during both speech perception and production, suggesting an anatomically and functionally separate auditory processing zone that we believe to be involved in multisensory integration during speech perception and feedback control.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580786/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142512114","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}
{"title":"A Dynamic Link between Respiration and Arousal.","authors":"Daniel S Kluger, Joachim Gross, Christian Keitel","doi":"10.1523/JNEUROSCI.1173-24.2024","DOIUrl":"10.1523/JNEUROSCI.1173-24.2024","url":null,"abstract":"<p><p>Viewing brain function through the lens of other physiological processes has critically added to our understanding of human cognition. Further advances though may need a closer look at the interactions between these physiological processes themselves. Here we characterize the interplay of the highly periodic, and metabolically vital respiratory process and fluctuations in arousal neuromodulation, a process classically seen as nonperiodic. In the data from three experiments (<i>N</i> = 56 / 27 / 25 women and men), we tested for covariations in respiratory and pupil size (arousal) dynamics. After substantiating a robust coupling in the largest dataset, we further show that coupling strength decreases during task performance compared with rest and that it mirrors a decreased respiratory rate when participants take deeper breaths. Taken together, these findings suggest a stronger link between respiratory and arousal processes than previously thought. Moreover, these links imply a stronger coupling during periods of rest, and the effect of respiratory rate on the coupling suggests a driving role. As a consequence, studying the role of neuromodulatory arousal on cortical function may also need to consider respiratory influences.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580776/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142394784","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}
Akihiro Yamada, Mayank Gautam, Ayaka I Yamada, Jennifer Ling, Saurav Gupta, Hidemasa Furue, Wenqin Luo, Jianguo G Gu
{"title":"Acid-Sensing Ion Channels Drive the Generation of Tactile Impulses in Merkel Cell-Neurite Complexes of the Glabrous Skin of Rodent Hindpaws.","authors":"Akihiro Yamada, Mayank Gautam, Ayaka I Yamada, Jennifer Ling, Saurav Gupta, Hidemasa Furue, Wenqin Luo, Jianguo G Gu","doi":"10.1523/JNEUROSCI.0885-24.2024","DOIUrl":"10.1523/JNEUROSCI.0885-24.2024","url":null,"abstract":"<p><p>Merkel cell-neurite complexes (MNCs) are enriched in touch-sensitive areas, including whisker hair follicles and the glabrous skin of the rodent's paws, where tactile stimulation elicits slowly adapting type 1 (SA1) tactile impulses to encode for the sense of touch. Recently, we have shown with rodent whisker hair follicles that SA1 impulses are generated through fast excitatory synaptic transmission at MNCs and driven by acid-sensing ion channels (ASICs). However, it is currently unknown whether, besides whisker hair follicles, ASICs also play an essential role in generating SA1 impulses from MNCs of other body parts in mammals. In the present study, we attempted to address this question by using the skin-nerve preparations made from the hindpaw glabrous skin and tibial nerves of both male and female rodents and applying the pressure-clamped single-fiber recordings. We showed that SA1 impulses elicited by tactile stimulation to the rat hindpaw glabrous skin were largely diminished in the presence of amiloride and diminazene, two ASIC channel blockers. Furthermore, using the hindpaw glabrous skin and tibial nerve preparations made from the mice genetically deleted of ASIC3 channels (ASIC3<sup>-/-</sup>), we showed that the frequency of SA1 impulses was significantly lower in ASIC3<sup>-/-</sup> mice than in littermate wild-type ASIC3<sup>+/+</sup> mice, a result consistent with the pharmacological experiments with ASIC channel blockers. Our findings suggest that ASIC channels are essential for generating SA1 impulses to underlie the sense of touch in the glabrous skin of rodent hindpaws.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580779/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142394785","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}
{"title":"Probing Perceptual Uncertainty to Examine the Relationship between Curiosity and Confidence.","authors":"Jocelyn A Halim","doi":"10.1523/JNEUROSCI.1787-24.2024","DOIUrl":"10.1523/JNEUROSCI.1787-24.2024","url":null,"abstract":"","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"44 47","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580762/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142683276","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}
{"title":"Kernels of Motor Memory Formation: Temporal Generalization in Bimanual Adaptation.","authors":"Ian S Howard, Sae Franklin, David W Franklin","doi":"10.1523/JNEUROSCI.0359-24.2024","DOIUrl":"10.1523/JNEUROSCI.0359-24.2024","url":null,"abstract":"<p><p>In daily life, we coordinate both simultaneous and sequential bimanual movements to manipulate objects. Our ability to rapidly account for different object dynamics suggests there are neural mechanisms to quickly deal with them. Here we investigate how actions of one arm can serve as a contextual cue for the other arm and facilitate adaptation. Specifically, we examine the temporal characteristics that underlie motor memory formation and recall, by testing the contextual effects of prior, simultaneous, and post contralateral arm movements in both male and female human participants. To do so, we measure their temporal generalization in three bimanual interference tasks. Importantly, the timing context of the learned action plays a pivotal role in the temporal generalization. While motor memories trained with post adaptation contextual movements generalize broadly, motor memories trained with prior contextual movements exhibit limited generalization, and motor memories trained with simultaneous contextual movements do not generalize to prior or post contextual timings. This highlights temporal tuning in sensorimotor plasticity: different training conditions yield substantially different temporal generalization characteristics. Since these generalizations extend far beyond any variability in training times, we suggest that the observed differences may stem from inherent differences in the use of prior, current, and post adaptation contextual information in the generation of natural behavior. This would imply differences in the underlying neural circuitry involved in learning and executing the corresponding coordinated bimanual movements.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580777/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142367205","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}
{"title":"Erratum: Hurley et al., \"GluN3A and Excitatory Glycine Receptors in the Adult Hippocampus\".","authors":"","doi":"10.1523/JNEUROSCI.2031-24.2024","DOIUrl":"10.1523/JNEUROSCI.2031-24.2024","url":null,"abstract":"","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4,"publicationDate":"2024-11-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11580770/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142631362","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}