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• W3178102938 abstract "How the brain computes with sensory input to execute a delayed motor response remains elusive. In this issue of Neuron, Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar reveal a key cortical circuit that underlies sensorimotor transformation to execute a delayed motor output following a specific sensory input. How the brain computes with sensory input to execute a delayed motor response remains elusive. In this issue of Neuron, Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar reveal a key cortical circuit that underlies sensorimotor transformation to execute a delayed motor output following a specific sensory input. Imagine the 2018 NBA finals. Stephen Curry must draw a foul on the Cleveland Cavaliers defender, so the Golden State Warriors can prevail. One option is to fake a shot to get the defender in the air, then jump into the defender, pause, and take the shot. While this did not happen, imagine the shot went into the basket and Curry also drew the foul—2 points and a free throw! Strategy worked. We do not need to be an NBA superstar to purposefully delay motor execution. In fact, we do this every day. When we see an elevator full of passengers about to close, we withdraw our arm to push the button until after the elevator moves. The process to transform the sensory information (e.g., contact with the opponent player) to timed motor execution (e.g., shooting) involves your cortex. However, unraveling the neural mechanisms underlying this fundamental process poses challenges, as the mechanisms likely involve distributed neural activity across multiple cortical regions. In this issue of Neuron, Esmaeili et al. characterized the sequence of neuronal activity across cortical regions during a sensorimotor transformation task using an elegant combination of cortex-wide calcium imaging and single-unit recording (Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar). Further, they assessed the causal contribution of each region by using time-resolved optogenetic manipulations of neuronal activity in each region. The authors trained mice to lick a waterspout following a 1 s delay after a brief whisker deflection. An auditory tone signaled the onset of the response window. The delay epoch is key to the behavioral task because the neural activity during this period reflects the neural activity during the transformation between sensory input to motor response. During task performance, Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar mapped neuronal activity across 9 cortical regions using wide-field calcium imaging. To extract learning-induced changes in the sensory and motor circuits, calcium measurements were made within the same mice before and after whisker training. They also performed high-density single-unit recordings from 12 different brain regions, including areas outside the cortex, during task performance (see also Mayrhofer et al., 2019Mayrhofer J.M. El-Boustani S. Foustoukos G. Auffret M. Tamura K. Petersen C.C.H. Distinct Contributions of Whisker Sensory Cortex and Tongue-Jaw Motor Cortex in a Goal-Directed Sensorimotor Transformation.Neuron. 2019; 103: 1034-1043.e5Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar). Their detailed survey of neuronal dynamics provides a comprehensive view of brain-wide circuits that orchestrate the timely execution and suppression of a learned motor response. Whisker stimulation evoked rapid responses in canonical sensory areas like primary and secondary whisker somatosensory areas (wS1 and wS2, respectively). These sensory-evoked responses were robust in both novice and expert mice. The expert mice also exhibited striking learning-induced changes during the delay period following the whisker stimulation. Tongue-jaw motor area (tjM1) showed a transient suppression of activity only in expert mice. Suppressed tjM1 activity was more pronounced when mice successfully withheld licking until after the response cue presentation. Importantly, when Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar directly manipulated tjM1 activity using optogenetics, they could induce the corresponding behavioral response. Thus, the authors demonstrated that transient suppression of tjM1 activity directly contributed to the delayed licking or motor execution. In expert mice, this transient suppression of tjM1 activity preceded the sequential activation of motor cortical areas starting with primary and secondary whisker motor areas (wM1 and wM2), followed by anterolateral motor area (ALM) and then tjM1. The activity of these areas corresponded to different parts of the delay period. wM2 activity featured prominent learning-induced changes in expert mice. Its activity was significantly enhanced, whereas the activity of wM1 was reduced. The latency of wM2 activity became shorter after whisker training and increased shortly after whisker stimulation akin to the whisker-evoked response in sensory areas. wM1 showed opposite responses, showing increases at a later time point. These findings suggest a role for wM2 to route sensory information from the wS1-wS2 pathway to frontal areas (ALM and tjM1) during the delay period, which reveals a sensorimotor transformation circuit. Mice typically develop preparatory movements, such as whisking and jaw movements, during training in delayed-response tasks. Therefore, the prominent delay period activity in motor areas of expert mice could reflect preparatory movements as shown in prior reports (for example, Stringer et al., 2019Stringer C. Pachitariu M. Steinmetz N. Reddy C.B. Carandini M. Harris K.D. Spontaneous behaviors drive multidimensional, brainwide activity.Science. 2019; 364: 255Crossref PubMed Scopus (315) Google Scholar). To account for this possibility, Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar “regressed out” movement contributions to the delay period activity and found that the delay period activity in ALM remained even after accounting for preparatory movements, which confirms and extends prior findings (Guo et al., 2014Guo Z.V. Li N. Huber D. Ophir E. Gutnisky D. Ting J.T. Feng G. Svoboda K. Flow of cortical activity underlying a tactile decision in mice.Neuron. 2014; 81: 179-194Abstract Full Text Full Text PDF PubMed Scopus (322) Google Scholar; Li et al., 2015Li N. Chen T.W. Guo Z.V. Gerfen C.R. Svoboda K. A motor cortex circuit for motor planning and movement.Nature. 2015; 519: 51-56Crossref PubMed Scopus (257) Google Scholar). However, neural activity in other motor areas did not remain elevated during the delay period after accounting for preparatory movements. One question that could arise is whether delay period activity in motor areas outside ALM (for example, wM2) represents the animal’s movement unrelated to the learned task. If that were the case, inactivating these areas during the delay period should not impact behavioral performance. Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar also explored this possibility. They inactivated different brain regions at specific time windows and mapped the behavioral responses. Inactivation of wS2 during whisker stimulation elicited a pronounced decrease in the number of correct licks, consistent with previous studies (Kwon et al., 2016Kwon S.E. Yang H. Minamisawa G. O’Connor D.H. Sensory and decision-related activity propagate in a cortical feedback loop during touch perception.Nat. Neurosci. 2016; 19: 1243-1249Crossref PubMed Scopus (90) Google Scholar). Interestingly, inactivation during whisker stimulation impaired behavioral performance in every region tested, including wM1 and wM2. During the delay period, inactivating wM2, ALM, and tjM1 altered behavioral performance either by decreasing correct licks or by increasing incorrect licks. Inactivation surprisingly reduced preparatory movements during the delay period, indicating that preparatory movements facilitate task performance. Together, these results suggest that preparatory movements may represent a form of “motor memory,” like the stereotyped motor sequences observed in rats performing a complex motor task (Kawai et al., 2015Kawai R. Markman T. Poddar R. Ko R. Fantana A.L. Dhawale A.K. Kampff A.R. Ölveczky B.P. Motor cortex is required for learning but not for executing a motor skill.Neuron. 2015; 86: 800-812Abstract Full Text Full Text PDF PubMed Scopus (233) Google Scholar). Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar quantified the degree by which different brain regions contribute to the learned motor task using a metric comprising both the quantity of task-related activities and the behavioral impact upon optogenetic inactivation. Canonical sensory areas (wS1 and wS2) and frontal motor areas (ALM and tjM1) showed a large contribution to responding during whisker stimulation versus during the response window, respectively. wM2 showed significant activity throughout whisker stimulation, delay period, and response windows, consistent with its potential role in linking sensory information with motor planning and execution. Despite the high behavioral impact following inactivation, medial prefrontal cortex scored low in the overall involvement, as its activity did not correlate with the animal’s behavior. Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar identified cortical substrates for key processes during the delayed response task, suppression of premature responses and conversion of sensation into a learned motor output. Their study raises intriguing questions for future investigation. What is the circuit mechanism underlying the suppression and subsequent activation of tjM1? The onset of the delay period activity in wM2/ALM precedes and partially overlaps with the suppressed activity in tjM1, suggesting that wM2/ALM may directly suppress tjM1 via cortico-cortical pathway. A similar feedforward inhibition motif occurs in the M2→primary auditory cortex pathway implicated in corollary discharge signaling (Schneider et al., 2014Schneider D.M. Nelson A. Mooney R. A synaptic and circuit basis for corollary discharge in the auditory cortex.Nature. 2014; 513: 189-194Crossref PubMed Scopus (270) Google Scholar). Subcortical structures, such as cerebellum and thalamus, likely also contribute to modulating tjM1 activity. How these subcortical areas influence cortical activities probed in this study is a question for future investigation. Which brain structures map the sensory information to motor commands, and by what mechanisms? Esmaeili et al., 2021Esmaeili V. Tamura K. Muscinelli S.P. Modirshanechi A. Boscaglia M. Lee A.B. Oryshchuk A. Foustoukos G. Liu Y. Crochet S. et al.Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor response.Neuron. 2021; 109 (this issue): 2183-2201Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar suggest a role for the wS2→wM2 pathway in bridging the gap between sensation and the action. Does the activity propagating along this pathway encode sensory or motor information or both? wS2 neurons encode task-related activities, in addition to stimulus features (Kwon et al., 2016Kwon S.E. Yang H. Minamisawa G. O’Connor D.H. Sensory and decision-related activity propagate in a cortical feedback loop during touch perception.Nat. Neurosci. 2016; 19: 1243-1249Crossref PubMed Scopus (90) Google Scholar), and send projections to wM2 (Oh et al., 2014Oh S.W. Harris J.A. Ng L. Winslow B. Cain N. Mihalas S. Wang Q. Lau C. Kuan L. Henry A.M. et al.A mesoscale connectome of the mouse brain.Nature. 2014; 508: 207-214Crossref PubMed Scopus (1230) Google Scholar). Perhaps, wS2 transmits decision-related information to wM2. Alternatively, wS2 may transmit moment-by-moment sensory signals (Zuo and Diamond, 2019Zuo Y. Diamond M.E. Texture Identification by Bounded Integration of Sensory Cortical Signals.Curr. Biol. 2019; 29: 1425-1435.e5Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar), which are then integrated by wM2 neurons. Overall, this study represents a significant advance toward a greater understanding of cortical circuits underlying sensorimotor transformation. Rapid suppression and sustained activation of distinct cortical regions for a delayed sensory-triggered motor responseEsmaeili et al.NeuronJune 1, 2021In BriefEsmaeili, Tamura, et al. investigate cortical contributions to a task in which mice learn to respond to a brief whisker stimulus with delayed licking for reward. They find suppression of orofacial sensorimotor cortex inhibits premature licking, whereas excitation of secondary motor cortex maintains a lick plan during the delay period. Full-Text PDF Open Access" @default.
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• W3178102938 title "Delay tactics for action in the cortex" @default.
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