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Neuronal representation of locomotion during motivated behavior in the mouse anterior cingulate cortex

Sachuriga 富山大学

2022.09.28

概要

〔目的〕When we engage in a continuous and/or repetitive reward-seeking activity that involves movement, we make unconscious decisions based on our past experiences and potential outcomes to value the effort. In many mammals, such a reward-seeking activity involves overground locomotion (e.g., walking and running). The anterior cingulate cortex (ACC) has been implicated in motor planning, motor control, sensory processing, emotion, motivation, and evaluation of outcome value. Behavioral studies reported that ACC lesions causes akinetic mutism, impairments in movement initiation, and deficits in self-paced motor tasks. These findings suggest that the ACC integrates sensory and motivated (reward) information to initiate and maintain locomotion. However, it is unclear how ACC neurons dynamically represent motivated locomotor behavior in a self-paced task. The current study examined how information of locomotion and reward outcomes is temporally represented by individual and ensemble ACC neurons in mice in a self-paced and reward-based locomotor task.

〔方法〕Seven male C57BL/6J mice were used for the experiment. To record neural signals during performance of the task, a single array with four tetrodes was implanted in the left ACC under anesthesia, and an aluminum frame was cemented on the exposed skull for the animal to be attached to the behavioral apparatus. Then, the mice were trained to perform the self-paced and reward-based locomotor task consisting of repeated runs on a spherical treadmill to obtain a reward. The mouse had to initiate a run and then stop (preparatory run). When the mouse stopped, a white square on the monitor was presented for 2 s as a visual cue, a time window where the animal had to restart running (reward run). After running for more than 1 s, sucrose water was dispensed as a reward, and a white rectangle was presented for 4 s as visual feedback. If the mouse did not restart or complete the 1 s reward run, they were not rewarded (non-reward trial) and had a 3 s time out (the cue cannot be triggered during this period). During performance of the task, activities of ACC neurons were recorded and then isolated into single neurons for further analysis. In individual neurons, peri-event histograms (PETHs) around the task events were created and analyzed by a repeated one-way ANOVA. Ensemble activity of ACC neurons was also analyzed by a demixed principal component analysis (dPCA). After recording, the mice were perfused, and electrode locations were histologically identified.

〔結果〕The 343 neurons were recorded from the ACC during the task performance. Of 343 ACC neurons, activity of 81 neurons (23.6%, 81/343) was significantly modulated around the timing of the reward delivery (Type 1 neurons). Thirty-six neurons (10.0%, 36/343) significantly increased firing rates when the mouse spontaneously started to run (Type 2 neurons). Twenty-six neurons (7.6%, 26/343) significantly decreased firing rates when the mice began to spontaneously run (Type 3 neurons). Furthermore, by applying a dPCA, the ACC population activity was decomposed into components representing locomotion and the previous (retrospective)/future (prospective) reward outcome.

〔総括〕The main finding of this study is that the ACC activity mainly represents locomotion during motivated reward-based behavior, which requires repetitive running. Activity patterns of the individual ACC neurons suggest that Types 2 and 3 encode the proactive locomotor and inactive elements of the task, respectively. At the populational level, the first component of the dPCA represented the time course of locomotion that was independent of reward outcomes. These findings indicate that the ACC mainly encodes the timing of locomotion, specifically the initiation, maintenance and termination of the movement in the self-paced task. Furthermore, ensemble activity of the ACC neurons represented prospective and retrospective reward outcome. These findings suggest that the ACC encodes the reward information to affect motor behavior (locomotion). In conclusion, the present results provide a neurophysiological basis of a self-paced motivated locomotor behavior: ACC neurons encode reward information required for decision of initiation and maintenance of locomotor behavior and also encode actual locomotion.

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参考文献

Allman, J. M., Hakeem, A., Erwin, J. M., Nimchinsky, E., and Hof, P. (2006). The Anterior Cingulate Cortex: The Evolution of an Interface between Emotion and Cognition. Annals of the New York Academy of Sciences 935, 107–117. doi:10.1111/j.1749-6632.2001.tb03476.x.

Bryden, D. W., Johnson, E. E., Tobia, S. C., Kashtelyan, V., and Roesch, M. R. (2011). Attention for Learning Signals in Anterior Cingulate Cortex. J. Neurosci. 31, 18266–18274. doi:10.1523/JNEUROSCI.4715-11.2011.

Bush, G., Luu, P., and Posner, M. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. (Regul. Ed.) 4, 215–222. doi:10.1016/s1364-6613(00)01483-2.

Carr, D. B., and Sesack, S. R. (2000). Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20, 3864–3873.

Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B., and Uchida, N. (2012). Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85–88. doi:10.1038/nature10754.

Cowen, S. L., Davis, G. A., and Nitz, D. A. (2012). Anterior cingulate neurons in the rat map anticipated effort and reward to their associated action sequences. Journal of Neurophysiology 107, 2393–2407. doi:10.1152/jn.01012.2011.

Dalley, J. W., Everitt, B. J., and Robbins, T. W. (2011). Impulsivity, Compulsivity, and Top-Down Cognitive Control. Neuron 69, 680–694. doi:10.1016/j.neuron.2011.01.020.

Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995). Contributions of anterior cingulate cortex to behaviour. Brain 118, 279–306. doi:10.1093/brain/118.1.279.

Drew, T., and Marigold, D. S. (2015). Taking the next step: cortical contributions to the control of locomotion. Current Opinion in Neurobiology 33, 25–33. doi:10.1016/j.conb.2015.01.011.

Dum, R. P., and Strick, P. L. (1991). The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11, 667–689. doi:10.1523/JNEUROSCI.11-03-00667.1991.

Elston, T. W., and Bilkey, D. K. (2017). Anterior Cingulate Cortex Modulation of the Ventral Tegmental Area in an Effort Task. Cell Reports 19, 2220–2230. doi:10.1016/j.celrep.2017.05.062.

Engelhard, B., Finkelstein, J., Cox, J., Fleming, W., Jang, H. J., Ornelas, S., et al. (2019). Specialized coding of sensory, motor and cognitive variables in VTA dopamine neurons. Nature 570, 509–513. doi:10.1038/s41586-019-1261-9.

Euston, D. R., and McNaughton, B. L. (2006). Apparent encoding of sequential context in rat medial prefrontal cortex is accounted for by behavioral variability. J. Neurosci. 26, 13143–13155. doi:10.1523/JNEUROSCI.3803-06.2006.

Ferreira-Pinto, M. J., Ruder, L., Capelli, P., and Arber, S. (2018). Connecting Circuits for Supraspinal Control of Locomotion. Neuron 100, 361–374. doi:10.1016/j.neuron.2018.09.015.

Franklin, K., and Paxinos, G. (2008). The Mouse Brain in Stereotaxic Coordinates, Compact - 3rd Edition. New York: Academic Press

Fujisawa, S., Amarasingham, A., Harrison, M. T., and Buzsáki, G. (2008). Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 11, 823–833. doi:10.1038/nn.2134.

Fuster (2015). The Prefrontal Cortex - 5th Edition. New York: Academic Press

Galvin, C., and Ninan, I. (2014). Regulation of the Mouse Medial Prefrontal Cortical Synapses by Endogenous Estradiol. Neuropsychopharmacology 39, 2086–2094. doi:10.1038/npp.2014.56.

Gabbott, P. L. A., Warner, T. A., Jays, P. R. L., Salway, P., and Busby, S. J. (2005). Prefrontal cortex in the rat: Projections to subcortical autonomic, motor, and limbic centers. Journal of Comparative Neurology 492, 145–177. doi:10.1002/cne.20738.

Grillner, S., and El Manira, A. (2019). Current Principles of Motor Control, with Special Reference to Vertebrate Locomotion. Physiological Reviews 100, 271–320. doi:10.1152/physrev.00015.2019.

Han, W., Tellez, L. A., Rangel, M. J., Motta, S. C., Zhang, X., Perez, I. O., et al. (2017). Integrated Control of Predatory Hunting by the Central Nucleus of the Amygdala. Cell 168, 311- 324.e18. doi:10.1016/j.cell.2016.12.027.

Hayden, B. Y., and Platt, M. L. (2010). Neurons in Anterior Cingulate Cortex Multiplex Information about Reward and Action. J. Neurosci. 30, 3339–3346. doi:10.1523/JNEUROSCI.4874- 09.2010.

Hoover, W. B., and Vertes, R. P. (2007). Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212, 149–179. doi:10.1007/s00429-007-0150- 4.

Hu, F., Kamigaki, T., Zhang, Z., Zhang, S., Dan, U., and Dan, Y. (2019). Prefrontal Corticotectal Neurons Enhance Visual Processing through the Superior Colliculus and Pulvinar Thalamus. Neuron 104, 1141-1152.e4. doi:10.1016/j.neuron.2019.09.019.

Ito, S., Stuphorn, V., Brown, J. W., and Schall, J. D. (2003). Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120–122. doi:10.1126/science.1087847.

Jhang, J., Lee, H., Kang, M. S., Lee, H.-S., Park, H., and Han, J.-H. (2018). Anterior cingulate cortex and its input to the basolateral amygdala control innate fear response. Nature Communications 9, 2744. doi:10.1038/s41467-018-05090-y.

Jung, M. W., Qin, Y., McNaughton, B. L., and Barnes, C. A. (1998). Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8, 437–450. doi:10.1093/cercor/8.5.437.

Kawai, T., Yamada, H., Sato, N., Takada, M., and Matsumoto, M. (2015). Roles of the Lateral Habenula and Anterior Cingulate Cortex in Negative Outcome Monitoring and Behavioral Adjustment in Nonhuman Primates. Neuron 88, 792–804. doi:10.1016/j.neuron.2015.09.030.

Kennerley, S. W., Dahmubed, A. F., Lara, A. H., and Wallis, J. D. (2009). Neurons in the frontal lobe encode the value of multiple decision variables. J Cogn Neurosci 21, 1162–1178. doi:10.1162/jocn.2009.21100.

Khalighinejad, N., Alessandro Bongioanni, Verhagen, L., Folloni, D., Attali, D., Aubry, J.-F., et al. (2020). A Basal Forebrain-Cingulate Circuit in Macaques Decides It Is Time to Act. Neuron 105, 370-384.e8. doi:10.1016/j.neuron.2019.10.030.

Kim, H., Ährlund-Richter, S., Wang, X., Deisseroth, K., and Carlén, M. (2016). Prefrontal Parvalbumin Neurons in Control of Attention. Cell 164, 208–218. doi:10.1016/j.cell.2015.11.038.

Kobak, D., Brendel, W., Constantinidis, C., Feierstein, C. E., Kepecs, A., Mainen, Z. F., et al. (2016). Demixed principal component analysis of neural population data. eLife 5, e10989. doi:10.7554/eLife.10989.

Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., and Kepecs, A. (2013). Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498, 363–366. doi:10.1038/nature12176.

Leinweber, M., Ward, D. R., Sobczak, J. M., Attinger, A., and Keller, G. B. (2017). A Sensorimotor Circuit in Mouse Cortex for Visual Flow Predictions. Neuron 95, 1420-1432.e5. doi:10.1016/j.neuron.2017.08.036.

Ma, L., Hyman, J. M., Phillips, A. G., and Seamans, J. K. (2014). Tracking Progress toward a Goal in Corticostriatal Ensembles. J. Neurosci. 34, 2244–2253. doi:10.1523/JNEUROSCI.3834- 13.2014.

Matsumoto, J., Urakawa, S., Hori, E., de Araujo, M. F. P., Sakuma, Y., Ono, T., et al. (2012). Neuronal responses in the nucleus accumbens shell during sexual behavior in male rats. J. Neurosci. 32, 1672–1686. doi:10.1523/JNEUROSCI.5140-11.2012.

Matsumoto, K., Suzuki, W., and Tanaka, K. (2003). Neuronal correlates of goal-based motor selection in the prefrontal cortex. Science 301, 229–232. doi:10.1126/science.1084204.

Mesulam, M.-M. (1981). A cortical network for directed attention and unilateral neglect. Annals of Neurology 10, 309–325. doi:10.1002/ana.410100402.

Murakami, M., Shteingart, H., Loewenstein, Y., and Mainen, Z. F. (2017). Distinct Sources of Deterministic and Stochastic Components of Action Timing Decisions in Rodent Frontal Cortex. Neuron 94, 908-919.e7. doi:10.1016/j.neuron.2017.04.040.

Narayanan, N. S., and Laubach, M. (2006). Top-Down Control of Motor Cortex Ensembles by Dorsomedial Prefrontal Cortex. Neuron 52, 921–931. doi:10.1016/j.neuron.2006.10.021.

Niell, C. M., and Stryker, M. P. (2010). Modulation of Visual Responses by Behavioral State in Mouse Visual Cortex. Neuron 65, 472–479. doi:10.1016/j.neuron.2010.01.033.

Picard, N., and Strick, P. L. (1996). Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex 6, 342–353. doi:10.1093/cercor/6.3.342.

Quilodran, R., Rothé, M., and Procyk, E. (2008). Behavioral Shifts and Action Valuation in the Anterior Cingulate Cortex. Neuron 57, 314–325. doi:10.1016/j.neuron.2007.11.031.

Reppucci, C. J., and Petrovich, G. D. (2016). Organization of connections between the amygdala, medial prefrontal cortex, and lateral hypothalamus: a single and double retrograde tracing study in rats. Brain Struct Funct 221, 2937–2962. doi:10.1007/s00429-015-1081-0.

Rolls, E. T. (2019). The cingulate cortex and limbic systems for emotion, action, and memory. Brain Struct Funct 224, 3001–3018. doi:10.1007/s00429-019-01945-2.

Rossi-Pool, R., Zainos, A., Alvarez, M., Zizumbo, J., Vergara, J., and Romo, R. (2017). Decoding a Decision Process in the Neuronal Population of Dorsal Premotor Cortex. Neuron 96, 1432- 1446.e7. doi:10.1016/j.neuron.2017.11.023.

Rushworth, M. F. S., and Behrens, T. E. J. (2008). Choice, uncertainty and value in prefrontal and cingulate cortex. Nature Neuroscience 11, 389–397. doi:10.1038/nn2066.

Sachuriga, Nishimaru, H., Takamura, Y., Matsumoto, J., Ferreira Pereira de Araújo, M., Ono, T., Nishijo, H. (2021). Neuronal Representation of Locomotion During Motivated Behavior in the Mouse Anterior Cingulate Cortex. Front. Syst. Neurosci. 15, 655110.

Schultz, W., Dayan, P., and Montague, P. R. (1997). A Neural Substrate of Prediction and Reward. Science 275, 1593–1599. doi:10.1126/science.275.5306.1593.

Shima, K., and Tanji, J. (1998). Role for Cingulate Motor Area Cells in Voluntary Movement Selection Based on Reward. Science 282, 1335–1338. doi:10.1126/science.282.5392.1335.

Stark, E., Eichler, R., Roux, L., Fujisawa, S., Rotstein, H. G., and Buzsáki, G. (2013). Inhibition- Induced Theta Resonance in Cortical Circuits. Neuron 80, 1263–1276. doi:10.1016/j.neuron.2013.09.033.

Stuber, G. D., and Wise, R. A. (2016). Lateral hypothalamic circuits for feeding and reward. Nature Neuroscience 19, 198–205. doi:10.1038/nn.4220.

Sul, J. H., Kim, H., Huh, N., Lee, D., and Jung, M. W. (2010). Distinct Roles of Rodent Orbitofrontal and Medial Prefrontal Cortex in Decision Making. Neuron 66, 449–460. doi:10.1016/j.neuron.2010.03.033.

Thaler, D., Chen, Y. C., Nixon, P. D., Stern, C. E., and Passingham, R. E. (1995). The functions of the medial premotor cortex. I. Simple learned movements. Exp Brain Res 102, 445–460. doi:10.1007/bf00230649.

The cingulate cortex and limbic systems for emotion, action, and memory | SpringerLink Available at: https://link.springer.com/article/10.1007/s00429-019-01945-2 [Accessed June 30, 2020].

Totah, N. K. B., Kim, Y. B., Homayoun, H., and Moghaddam, B. (2009). Anterior Cingulate Neurons Represent Errors and Preparatory Attention within the Same Behavioral Sequence. J. Neurosci. 29, 6418–6426. doi:10.1523/JNEUROSCI.1142-09.2009.

Williams, S. M., and Goldman-Rakic, P. S. (1993). Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cereb. Cortex 3, 199–222. doi:10.1093/cercor/3.3.199.

Zhang, S., Xu, M., Kamigaki, T., Do, J. P. H., Chang, W.-C., Jenvay, S., et al. (2014). Long-range and local circuits for top-down modulation of visual cortex processing. Science 345, 660–665.

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