Journal of Neuroscience最新文献

{"title":"Spontaneous alpha-band lateralization extends persistence of visual information in iconic memory by modulating cortical excitability.","authors":"Paul Justin Connor Smith, Niko A Busch","doi":"10.1523/JNEUROSCI.2117-24.2025","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.2117-24.2025","url":null,"abstract":"<p><p>Pre-stimulus alpha oscillations in the visual cortex modulate neuronal excitability, influencing sensory processing and decision-making. While this relationship has been demonstrated mostly in detection tasks with low-visibility stimuli, interpretations of such effects can be ambiguous due to biases, making it difficult to clearly distinguish between perception-related and decision-related effects. In this study, we investigated how spontaneous fluctuations in pre-stimulus alpha power affect iconic memory, a high-capacity, ultra-short visual memory store. Data from 49 healthy adults (34 female and 15 male) was analyzed. We employed a partial report task, where a brief display of six stimuli was followed by a report cue indicating the target stimulus. In this paradigm, accuracy at short stimulus-cue onset asynchronies (SOAs) is typically high, reflecting the initial availability of sensory information, but it rapidly declines at intermediate SOAs due to the decay of the iconic memory trace, stabilizing at a low asymptote at long SOAs, representing the limited capacity of short-term memory. Crucially, performance in this task is constrained by the temporal persistence of sensory information, not by low visibility or response bias. We found that strong pre-stimulus alpha power enhanced performance by amplifying initial stimulus availability without affecting the speed of iconic decay. This effect partially reflects stronger pre-stimulus alpha power in the hemisphere ipsilateral to the to-be-reported target, likely suppressing neuronal excitability of neurons coding irrelevant stimuli. Our findings underscore the role of alpha oscillations in modulating neuronal excitability and visual perception, independent of decision-making strategies implicated in prior studies.<b>Significance statement</b> Pre-stimulus alpha oscillations in the visual cortex are known to influence visual perception, but the exact mechanism has been debated. Our study reveals that spontaneous fluctuations in pre-stimulus alpha power, particularly alpha lateralization, enhance iconic memory - a brief, high capacity visual memory system - by suppressing neuronal excitability at irrelevant spatial locations. This suppression improves the availability and temporal persistence of visual information and highlights a novel link between alpha oscillations and iconic memory. These findings extend our understanding of how pre-stimulus alpha power modulates neuronal excitability by showcasing its influence in a paradigm that is unaffected by low visibility and decision-making strategies.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145304085","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":"Intrinsic Neural Timescales Relate to Event-Related Activity - Key Role for Intracolumnar Connections.","authors":"Yasir Çatal, Kaan Keskin, Angelika Wolman, Andrea Buccellato, Georg Northoff","doi":"10.1523/JNEUROSCI.0896-25.2025","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.0896-25.2025","url":null,"abstract":"<p><p>The relationship of the brain's intrinsic neural timescales (INTs) during the resting state with event-related activity in response to external stimuli remains poorly understood. Here, we bridge this gap by combining computational modeling with human magnetoencephalography (MEG, resting state: N=64, 45 female; task state: N=58, 41 female) data to investigate the relation of intrinsic neuronal timescales (INT) with task-related activity, e.g., event-related fields (ERFs). Using the Jansen-Rit model, we first show that intracolumnar (and thus intra-regional) excitatory and inhibitory connections (rather than inter-regional feedback, feedforward and lateral connections between the columns of different regions) strongly influence both resting state INTs and task-related ERFs. Secondly, our results demonstrate a positive relationship between the magnitude of event-related fields (mERFs) and INTs, observed in both model simulations and empirical MEG data collected during an emotional face recognition task. Thirdly, modeling shows that the positive relationship of mERF and INT depends on intracolumnar connections through observing that the correlation between them disappears for fixed values of intracolumnar connections. Together, these findings highlight the importance of intracolumnar connections as a shared biological mechanism underlying both the resting-state's INTs and the task-state's event-related activity including their interplay.<b>Significance Statement</b> Intrinsic neural timescales (INTs) reflect the temporal persistence of neural activity and are increasingly recognized as a fundamental property of brain dynamics. How INTs relate to event-related neural responses remains poorly understood. Bridging this gap would give us a wider perspective on rest-task relationship in the brain. In this study, we combine modeling and magnetoencephalography (MEG) data to investigate this relationship. Modeling shows that intracolumnar connectivity simultaneously modulates both resting-state INTs and task-state event-related activity, leading to a positive correlation. The positive correlation is confirmed in MEG data. By bridging the gap between resting-state dynamics and task-state event-related responses, our work advances the understanding of how spontaneous and stimulus-driven brain processes are fundamentally intertwined.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145304107","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":"10.1523/JNEUROSCI.1182-24.2025","url":null,"abstract":"<p><p>The proper development of excitatory/inhibitory (E/I) 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 signal-regulatory protein α (SIRPα), a cell adhesion molecule that organizes excitatory synaptogenesis in the hippocampus, affect inhibitory synaptogenesis to maintain E/I 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 during critical periods functionally decreases both excitatory and inhibitory synapses in the hippocampus. By using various conditional knock-out mice, we found that SIRPα from pyramidal neurons, but not from 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 E/I balance.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12528841/pdf/","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":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"Competition between Tool and Hand Motion Impairs Movement Planning in Limb Apraxia.","authors":"Simon Thibault, John B Yates, Laurel J Buxbaum, Aaron L Wong","doi":"10.1523/JNEUROSCI.0692-25.2025","DOIUrl":"10.1523/JNEUROSCI.0692-25.2025","url":null,"abstract":"<p><p>Tool use is a complex motor planning problem. Prior research suggests that planning to use tools involves resolving competition between different tool-related action representations. We therefore reasoned that competition may also be exacerbated with tools for which the motions of the tool and the hand are incongruent (e.g., pinching the fingers to open a clothespin). If this hypothesis is correct, we should observe marked deficits in planning the use of incongruent as compared with congruent tools in individuals with limb apraxia following left hemisphere stroke (LCVA), a disorder associated with abnormal action competition. We asked 34 individuals with chronic LCVA (14 females) and 16 matched neurotypical controls (8 females) to use novel tools in which the correspondence between the motions of the hand and tool-tip were either congruent or incongruent. Individuals with LCVA also completed background assessments to quantify apraxia severity. We observed increased planning time for incongruent as compared with congruent tools as a function of apraxia severity. Further analysis revealed that this impairment predominantly occurred early in the task when the tools were first introduced. Lesion-symptom mapping analyses revealed that lesions to posterior temporal and inferior parietal areas were associated with impaired planning for incongruent tools. A second experiment on the same individuals with LCVA revealed that the ability to gesture the use of conventional tools was impaired for tools rated as more incongruent by a normative sample. These findings suggest that tool-hand incongruence evokes action competition and influences the tool-use difficulties experienced by people with apraxia.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12528837/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145031062","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":"Large-Scale Color Biases in the Retinotopic Functional Architecture Are Region Specific and Shared across Human Brains.","authors":"Michael M Bannert, Andreas Bartels","doi":"10.1523/JNEUROSCI.2717-20.2025","DOIUrl":"10.1523/JNEUROSCI.2717-20.2025","url":null,"abstract":"<p><p>Despite the functional specialization in visual cortex, there is growing evidence that the processing of chromatic and spatial visual features is intertwined. While past studies focused on visual field biases in retina and behavior, large-scale dependencies between coding of color and retinotopic space are largely unexplored in the cortex. Using a sample of male and female volunteers, we asked whether spatial color biases are shared across different human observers and whether they are idiosyncratic for distinct areas. We tested this by predicting the color a person was seeing using a linear classifier that has never been trained on chromatic responses from that same brain, solely by taking into account: (1) the chromatic responses in other individuals' brains and (2) commonalities between the spatial coding in brains used for training and the test brain. We were able to predict the color (and luminance) of stimuli seen by an observer based on other subjects' activity patterns in areas V1-V3, hV4, and LO1. In addition, we found that different colors elicited systematic, large-scale retinotopic biases that were idiosyncratic for distinct areas and common across brains. The area-specific spatial color codes and their conservation across individuals suggest functional or evolutionary organization pressures that remain to be elucidated.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12528842/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145024646","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":"Trigeminal motor nucleus regulates microstructure of feeding behavior without affecting total food intake.","authors":"Alison Maun Yeng Kok,Yi-Fei Li,Hua Huang,Nan Wang,Yufei Gao,Yu Fu","doi":"10.1523/jneurosci.0337-24.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.0337-24.2025","url":null,"abstract":"Feeding is critical for animal survival and is tightly regulated by designated neural circuits. Several brain regions have been implicated in feeding regulation, including hypothalamus, amygdala, parabrachial nucleus and others. However, how these feeding regulation neurons communicate with the executors of feeding behavior, the trigeminal motor (MoV) neurons that directly control mastication muscles, is unclear. Despite its clear involvement in feeding, MoV is rarely considered as a part of the feeding neural network in literature reviews, indicating an incomplete conceptual framework of feeding regulation. Here, by using Isl1 and ChAT as neuronal markers, we genetically targeted MoV neurons to reveal its connections with other brain regions and investigated their function in feeding in mice of either sex. Notably, we identified direct connection of MoV neurons with forebrain regions including amygdala and BNST, while hypothalamic feeding regulation neurons do not represent as a major direct regulator of MoV neurons. Functionally, although complete silencing of MoV neurons renders the mice incapable of eating, acute inhibition or activation of MoV neurons only changed microstructure of feeding behavior without influencing total food intake, suggesting that MoV neurons mainly function as the executor of feeding but are not involved in appetite regulation. Moreover, activating the GABAergic input neurons of MoV neurons generated similar effect as activating the MoV neurons, because MoV neurons are depolarised by GABA transmission. Together, we established the role of MoV neurons in feeding regulation and advanced the understanding of hindbrain feeding regulation network.Significance Statement Despite the extensive research of hypothalamic feeding regulation neural circuits, the nucleus that controls chewing, trigeminal motor nucleus (MoV), has rarely been considered in literature reviews as part of the feeding circuits, representing a major gap of knowledge in feeding regulation. In this manuscript, we mapped the inputs of MoV neurons using rabies virus method and revealed surprising direct connections with forebrain regions including amygdala. We also examined the functional impact of manipulating MoV neurons, or MoV-projecting CeA neurons, in feeding behavior and confirmed that MoV neurons only fine-tune the microstructure of feeding behavior without influencing total food consumption, suggesting that appetite is controlled by upstream feeding regulation neurons in hypothalamus or other brain regions.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"1 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296128","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":"Intrinsic dendritic integration features of prefrontal layer 5 pyramidal cell subclasses.","authors":"Selin Schamiloglu,Rebecca L Clarkson,Natalia S Stone,Alayna T Liptak,Kevin J Bender","doi":"10.1523/jneurosci.1080-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.1080-25.2025","url":null,"abstract":"Prefrontal cortex (PFC) is an associative center in the brain and integrates various inputs to support cognition. Layer 5 pyramidal cells are themselves associative centers, as their dendrites span all cortical layers and sample multiple input streams. Backpropagating action potentials (bAPs) are an important mechanism for integrating synaptic inputs arriving at distinct dendritic locations. bAPs originating in the axon initial segment can depolarize the apical dendrite, activate voltage-gated currents that underlie dendritic processing and synaptic plasticity, and influence the integration of synaptic inputs arriving onto apical dendrites. How effectively bAPs depolarize apical dendrites depends on cell type, dendritic morphology, and the dendrite's passive and active properties. Here, we found that in a unique subclass of PFC layer 5 pyramidal cell defined by D3 dopamine receptor (D3R) expression, dendritic calcium responses to bAP stimuli were far greater for a burst of APs than expected from a linear sum of single AP-evoked events in mice of either sex. D3R-expressing neurons electrophysiologically resemble intratelencephalic, D1R-expressing pyramidal neurons but morphologically resemble pyramidal tract, D2R-expressing pyramidal neurons. In both D1R- and D2R-expressing cells, burst-evoked dendritic calcium events largely reflected a linear sum of individual AP responses. In D1R neurons, this was partially due to large conductance calcium-activated potassium (BK) channels, while in D2R neurons, both BK and hyperpolarization-activated cyclic nucleotide-gated channels contributed. These data demonstrate that the intrinsic dendritic excitability of PFC layer 5 pyramidal cells widely differs and suggest that nonlinear dendritic excitability in D3R-expressing neurons uniquely positions these cells within PFC circuits.Significance Statement Layer 5 pyramidal cells associate inputs from diverse information streams to shape behavior. Backpropagating action potentials (bAPs) enable the integration of synaptic inputs that arrive coincidentally on the basal and apical dendrites, but the extent to which bAPs depolarize the apical dendrites can vary across cell types and dendritic morphologies. In prefrontal cortex, layer 5 pyramidal cells can be distinguished based on expression of the D1, D2, or D3 dopamine receptor expression. Here, we examined intrinsic dendritic excitability across D1R, D2R and D3R-expressing neurons and found that bAP-associated dendritic calcium transients vary considerably across these three intermingled neuronal subtypes, suggesting that these pyramidal cell classes have unique roles in prefrontal cortex processing.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"1 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-10-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145296129","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":"Hippocampal ripples during offline periods predict human motor sequence learning.","authors":"Pin-Chun Chen, Jenny Stritzelberger, Katrin Walther, Hajo Hamer, Bernhard P Staresina","doi":"10.1523/JNEUROSCI.1502-25.2025","DOIUrl":"https://doi.org/10.1523/JNEUROSCI.1502-25.2025","url":null,"abstract":"<p><p>High-frequency bursts in the hippocampus, known as ripples (80-120 Hz in humans), have been shown to support episodic memory processes. However, converging recent evidence in rodent models and human neuroimaging suggests that the hippocampus may be involved in a wider range of memory domains, including motor sequence learning (MSL). Nevertheless, no direct link between hippocampal ripples and MSL has been established yet. Here, we recorded intracranial electroencephalography (iEEG) from the hippocampus in 20 epilepsy patients (11 males and 9 females) during an MSL task in which participants showed steady improvement across nine 30-second <i>typing</i> blocks interspersed with 30-second <i>rest</i> ('offline') periods. We first demonstrated that ripple rates strongly increased during <i>rest</i> relative to <i>typing</i> blocks. Importantly, ripple rates during rest periods tracked behavioural improvements, both across learning blocks and across participants. These findings suggest that hippocampal ripples during rest periods play a role in facilitating motor sequence learning.<b>Significance Statement</b> This study provides the first direct evidence that hippocampal ripples, brief high-frequency oscillations previously linked to episodic memory, also play a role in human motor sequence learning. By recording intracranial EEG from epilepsy patients during a motor learning task, we found that ripple rates increased during rest periods between typing blocks and closely tracked behavioural improvements in performance. These findings suggest that hippocampal ripples during offline periods may facilitate consolidation of newly acquired motor skills, extending the functional significance of ripples beyond episodic memory.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145294267","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":"Selective attention shapes neural representations of complex auditory scenes: The Roles of Object Identity and Scene Composition.","authors":"Patrik Wikman,Ilkka Muukkonen,Jaakko Kauramäki,Ville Laaksonen,Onnipekka Varis,Christopher Petkov,Josef Rauschecker","doi":"10.1523/jneurosci.0506-25.2025","DOIUrl":"https://doi.org/10.1523/jneurosci.0506-25.2025","url":null,"abstract":"Everyday auditory scenes contain overlapping sound objects, requiring attention to isolate relevant objects from irrelevant background objects. This study examined how selective attention shapes neural representations of complex sound scenes in the auditory cortex (AC). Using functional magnetic resonance imaging, we recorded brain activity from participants (12 males, 8 females) as they attended to a designated object in scenes comprising three overlapping sounds. Scenes were constructed in two manners: one where each object belonged to a different category (speech, animal, instrument) and another where all objects were from the same category. Attending to speech enhanced activations in lateral AC subfields, while attention to animal and instrument sounds preferentially modulated medial AC subfields, supporting models where attention modulates feature-selective neural gain in AC. Remarkably, however, spatial pattern analysis revealed that the attended object dominated the AC activation patterns of the entire scene in a manner depending on both object type and scene composition: When scene objects belonged to different categories, attention effects were dominated by category-level processing. In contrast, when all scene objects shared the same category, dominance shifted to exemplar level processing in fields processing acoustic features. Thus, attention seems to dynamically prioritize the features offering maximal contrast within a given context, emphasizing object-specific patterns in feature-similar scenes and category-level patterns in feature-diverse scenes. Our results support models where top-down signals not only modulate gain but also affect scene decomposition and analysis - influencing stream segregation and gating of higher-level processing in a contextual manner, adapting to specific auditory environments.Significance statement Selective attention is essential for filtering behaviorally relevant sounds from complex auditory environments, yet the underlying neural mechanisms remain obscure. We combined fMRI with spatial activation pattern analysis to determine how the auditory cortex attentionally filters different types of sounds (speech, animal, instrument) in complex scenes composed of three sounds, either from different or the same categories. Attentional filtering depended both on the object type and on scene composition. Our data suggest that in the auditory cortex attentional filtering operates on category-level features in multi-category scenes, while exemplar-level features prevail in same-category scenes. Thus, top-down attention not only modulates neural gain but also affects scene decomposition and gating of higher-level processing in a contextual manner, adapting to specific auditory environments.","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":"23 1","pages":""},"PeriodicalIF":5.3,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145288480","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":"Superior colliculus projections drive dopamine neuron activity and movement but not value.","authors":"Carli L Poisson, Izzabella K Green, Gretchen M Stemmler, Julianna Prohofsky, Amy R Wolff, Cassandra Herubin, Madelyn Blake, Benjamin T Saunders","doi":"10.1523/JNEUROSCI.0291-25.2025","DOIUrl":"10.1523/JNEUROSCI.0291-25.2025","url":null,"abstract":"<p><p>To navigate dynamic environments, animals must rapidly integrate sensory information and respond appropriately to gather rewards and avoid threats. It is well established that dopamine (DA) neurons in the ventral tegmental area (VTA) and substantia nigra (SNc) are key for creating associations between environmental stimuli (i.e., cues) and the outcomes they predict. Critically, it remains unclear how sensory information is integrated into dopamine pathways. The superior colliculus (SC) receives direct visual input and is positioned as a relay for dopamine neuron augmentation. We characterized the anatomy and functional impact of SC projections to the VTA/SNc in male and female rats. First, we show that neurons in the deep layers of SC synapse densely throughout the ventral midbrain, interfacing with projections to the striatum and ventral pallidum, and these SC projections excite dopamine and GABA neurons in the VTA/SNc in vivo. Despite this, cues predicting SC→VTA/SNc neuron activation did not reliably evoke behavior in an optogenetic Pavlovian conditioning paradigm, and activation of SC→VTA/SNc neurons did not support primary reinforcement or produce place preference/avoidance. Instead, we find that stimulation of SC→VTA/SNc neurons evokes head turning. Focusing optogenetic activation solely onto dopamine neurons that receive input from the SC was sufficient to invigorate turning, but not reinforcement. Turning intensity increased with repeated stimulations, suggesting that this circuit may underlie sensorimotor learning for exploration and attentional switching. Together, our results show that collicular neurons contribute to cue-guided behaviors by controlling pose adjustments through interaction with dopamine neurons that preferentially engage movement instead of reward.<b>Significance Statement</b> In dynamic environments, animals must rapidly integrate sensory information and respond appropriately to survive. Dopamine (DA) neurons are key for creating associations between environmental cues through learning, but it remains unclear how relevant sensory information is integrated into DA pathways to guide this process. The superior colliculus (SC) is positioned for rapid sensory augmentation of dopamine neurons. Using a combination of approaches, we find that SC neurons projecting to the ventral midbrain activate dopamine neurons and drive postural changes without creating conditioned behavior or valence. Our results highlight a brain circuit that is important for guiding movement to redirect attention, via interaction with classic learning systems, and suggest distinct subpopulations of dopamine neurons preferentially engage movement instead of reward.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145294270","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}