Rui M. Costa, PhD

Rui M. Costa, PhD

Research Interest

Behavioral and Systems Neuroscience: Non-human Models
Synapses and Circuits

Animals have a distinctive ability to behave, i.e. to move and interact with their surroundings, which permits them to shift between environments and also to change their environment.

Did you ever stop to think why animals move? What type of nervous system organization permits the generation of movement? How can actions be planned to achieve particular goals? To what extent they reflect the interaction with the environment or inherited programs? Do similar movements always represent similar actions? How do sequences of actions emerge? And how do certain actions become compulsive?

Our goal is to understand the circuit mechanisms underlying the generation of self-paced actions, and the reinforcement and refinement of actions into complex action repertoires based on the consequences of their execution. Understanding this adaptive process, how actions are learned through trial and feedback, requires mechanistic insight into how actions are initiated, how they can be selected/initiated again, and how feedback can refine their execution and organization. We use genetic, electrophysiological, optical, and behavioral approaches to gain this mechanistic insight and understand basal ganglia function in motor learning and control. This research has implications for movement disorders like Parkinson’s disease, and psychiatric disorders like Autism Spectrum Disorders and Obsessive-Compulsive conditions.

 

2002 -                  Ph.D. in Biomedical Sciences, GABBA Doctoral Program,

                           University of California at Los Angeles, USA and

                           Abel Salazar Biomedical Institute, University of Porto, Portugal

1996 -                  DVM (May 1996), Faculty of Veterinary Medicine,

                           Technical University of Lisbon, Portugal.

2005 -                  Postdoctoral Fellow, Duke University Medical Center, USA

  • Aaron Koralek, Postdoc
  • Akira Fushiki, Postdoc
  • Alana Mendelson, Postdoc
  • Alice Mosberger, Postdoc
  • Ana Mafalda Vicente, Postdoc
  • Anders Nelson, Postdoc
  • Gabriela Martins, Associate Research Scientist
  • Helena Seuffert, Research Assistant
  • Helio Rodrigues, Staff Associate
  • Ines Vaz, PhD Student
  • Jonathan Tang, Postdoc.
  • Joshua Greene, Postdoc
  • Leonor Remedio, Postdoc
  • Leslie Sibener, PhD student
  • Marcela Carmona, Postdoc
  • Mariana Correia, Staff Associate
  • Michael Ramsey, Research Assistant
  • Samaher Fageiri, Postdoc
  • Tiffany Chen, Research Assistant
  • Ulkar Aghayeva, Postdoc
  • Vivek Athalye, Postdoc
  • Zirong Gu, Postdoc
  • Nelson A, Abdelmeish B, Costa RM (2020). Corticospinal neurons encode complex motor signals that are broadcast to dichotomous striatal circuits. Submitted; Preprint bioRxiv. doi: https://doi.org/10.1101/2020.08.31.275180
  • Koralek A, Costa RM (2020). Sustained dopaminergic plateaus and noradrenergic depressions mediate dissociable aspects of exploitative states. Submitted; Preprint bioRxiv. doi: 10.1101/822650
  • McElvain LE, Chen Y, Moore JD, Brigidi GS, Bloodgood BLLim BK, Costa RM, Kleinfeld D (2021). Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon. Neuron, S0896-6273(21)00187-2. doi: 10.1016/j.neuron.2021.03.017.
  • Castro-Rodrigues P, Akam T, Snorrason I, Camacho M, Paixao V, Barahona-Correa JB, Dayan P, Simposon HB, Costa RM, Oliveira-Maia A (2020). Explicit knowledge of task structures is the primary determinant of human model-based action. Submitted; Preprint medRxiv. doi: 10.1101/2020.09.06.20189241
  • Akam T, Rodrigues-Vaz I, Marcelo I, Zhang X, Pereira M, Oliveira R, Dayan P, Costa RM (2020). Anterior cingulate cortex represents action-state predictions and causally mediates model-based reinforcement learning in a two-step decision task. Neuron, 109(1):149-163.e7. doi: 10.1016/j.neuron.2020.10.013.
  • Botta P, Fushiki A, Vicente AM, Hammond LA, Mosberger AC, Gerfen CR, Peterka D, Costa RM (2020). An amygdala circuit mediates experience-dependent momentary exploratory arrests. Cell, 183(3): 605-619.e22. doi: 10.1016/j.cell.2020.09.023.
  • Fernandes AB, Alves da Silva J, Almeida J, Cui G, Gerfen CR, Costa RM, Oliveira-Maia A (2020). Postingestive modulation of food seeking depends on vagal-mediated dopamine neuron activity. Neuron, 106(5):778-788.e6. doi: 10.1016/j.neuron.2020.03.009.
  • Godinho-Silva C, Domingues RG, Rendas M, Raposo B, Ribeiro H, Silva JA, Vieria A, Costa, RM, Barbosa-Morais NL, Carvalho T, Veiga-Fernandes H (2019). Light-entrained and brain-tuned circadian circuits regulate ILC3 and gut homeostasis. Nature, 574:254-258. doi: 10.1038/s41586-019-1579-3.
  • Rao-Ruiz P, Couey JJ, Marcelo IM, Bouwkamp CG, Slump DE, Matos MR, van der Loo RJ, Martins GJ, van den Hout M, van IJcken WF, Costa RM, van den Oever MC, Kushner SA (2019). Engram-specific transcriptome profiling of contextual memory consolidation. Nature Communications. 10; 2232. doi: 10.1038/s41467-019-09960-x.
  • French CA, Veloz MV, Zhou K Fisher SE*, Costa RM*, De Zeeuw CI* (2019). Differential effects of Foxp2 disruption in distinct motor circuits. Molecular Psychiatry, 24:447-462. doi: 10.1038/s41380-018-0199-x.
  • Athalye VR, Santos, F, Carmena JM*, Costa RM* (2018). Evidence for a neural law of effect. Science, 359(6379):1024-1029. doi: 10.1126/science.aao6058.
  • Neely, RM*, Koralek AC*, Athalye VR, Santos, F, Costa RM* Carmena JM* (2018). Volitional modulation of primary visual cortex activity requires the Basal Ganglia. Neuron, 97(6): 1356-1368.e4. doi: 10.1016/j.neuron.2018.01.051.
  • Silva JA, Tecuapetla F., Paixão VB, Costa RM (2018). Dopamine neuron activity before action initiation gates and invigorates future movements. Nature, 54(7691):244-248. doi: 10.1038/nature25457.
  • Rijo-Ferreira F, Carvalho T, Afonso C, Sanches-Vaz M, Costa RM, Figueiredo LM, Takahashi JS (2018) Sleeping sickness is a circadian disorder. Nature Communications, 9(1):62. doi: 10.1038/s41467-017-02484-2.
  • Klaus A*, Martins GM*, Paixão VB, Zhou P, Paninski L, Costa RM (2017). The spatiotemporal organization of the striatum encodes action space. Neuron, 95(5).  doi: 10.1016/j.neuron.2017.08.015.
  • Galvão-Ferreira P, Lipinski M, Santos F, Barco A, Costa RM (2017). Skill learning modulates RNA Pol II poising at immediate early genes in the adult striatum. eNeuro. 17;4(2). doi: 10.1523/ENEURO.0074-17.2017.
  • Afonso C, Paixão VB, Klaus A, Lunghi M, Piro F, Emiliani C, Di Cristina M, Costa RM (2017) Toxoplasma-induced changes in host risk behaviour are independent of parasite-derived AaaH2 tyrosine hydroxylase. Scientific Reports, 7(1):13822. doi: 10.1038/s41598-017-13229-y.
  • Athalye VR, Ganguly K, Costa RM*, Carmena JM* (2017). Emergence of coordinated neural dynamics underlies neuroprosthetic learning and skillful control. Neuron, 93(4):955-970.  doi: 10.1016/j.neuron.2017.01.016.
  • Tecuapetla F, Jin X., Lima SQ, Costa RM (2016). Complementary contributions of striatal projection pathways to action initiation and execution. Cell, 166(3):703-15. doi: 10.1016/j.cell.2016.06.032.
  • Gremel CM, Chancey J, Atwood B, Luo G, Neve R, Ramakrishnan C, Deisseroth K, Lovinger DM, Costa RM (2016). Endocannabinoid modulation of orbitostriatal circuits gates habit formation. Neuron, 90(6):1312-24. doi: 10.1016/j.neuron.2016.04.043.
  • Vicente AM*, Galvão-Ferreira P*, Tecuapetla F, Costa RM (2016). Direct and indirect striatal projection pathways reinforce different action strategies. Current Biology, 26(7):R267-9. doi: 10.1016/j.cub.2016.02.036.
  • Akam T, Costa RM, Dayan P (2015). Simple Plans or Sophisticated Habits? State, Transition and Learning Interactions in the Two-step Task. PLoS Computational Biology, 11(12):e1004648. doi: 10.1371/journal.pcbi.1004648.
  • Santos F, Jin X, Oliveira, R, Costa RM. (2015). Corticostriatal dynamics encode the refinement of behavioral variability during skill learning. eLife, 4:e09423. doi:10.7554/eLife.09423.
  • Cao VY, Ye Y, Mastwal S, Ren M, Coon M, Liu Q, Costa RM*, Wang KH* (2015). Motor Learning Consolidates Arc-expressing Neuronal Ensembles in Secondary Motor Cortex. Neuron, 86(6):1385-92. doi: 10.1016/j.neuron.2015.05.022.
  • Tecuapetla F, Matias S, Dugue GP, Mainen ZF, Costa RM (2014). Balanced activity in basal ganglia projection pathways is critical for contraversive movements. Nature Communications; 5:4315. doi: 10.1038/ncomms5315
  • Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM (2014). Deep brain optical measurement of cell type-specific neural activity in mice performing an operant task. Nature Protocols, 9(6):1213-28. doi: 10.1038/nprot.2014.080.
  • Clancy KB, Koralek AC, Costa RM*, Feldman DE*, Carmena JM* (2014). Volitional modulation of optically recorded calcium signals during neuroprosthetic learning. Nature Neuroscience, 17(6):807-9. doi: 10.1038/nn.3712.
  • Jin X, Tecuapetla F, Costa RM (2014). Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nature Neuroscience, 17(3):423-30. doi: 10.1038/nn.3632.
  • Gomez-Marin A, Paton JJ, Kampff AR, Costa RM, Mainen ZF (2014) Big behavioral data: psychology, ethology and the foundations of neuroscience. Nature Neuroscience, 17(11):1455-62. doi: 10.1038/nn.3812
  • Gremel, CM & Costa RM (2013). Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nature Communications, 4:2264. doi:10.1038/ncomms3264.
  • Gremel CM & Costa RM (2013). Premotor cortex is critical for goal-directed actions. Frontiers in Computational Neuroscience, 7:110. doi: 10.3389/fncom.2013.00110.
  • Koralek AC, Costa RM, Carmena JM (2013). Temporally precise cell-specific coherence develops in corticostriatal networks during learning. Neuron, 4;79(5):865-72. doi: 10.1016/j.neuron.2013.06.047.
  • Cao VY, Ye Y, Mastwal SS, Lovinger DM, Costa RM, Wang KH (2013). In vivo two-photon imaging of experience-dependent molecular changes in cortical neurons. Journal Visualized Experiments, 5(71). doi:pii: 50148. 10.3791/50148
  • Cui, G*, Jun SB*, Jin, X, Pham, MD, Vogel SS, Lovinger DM & Costa RM. (2013) Concurrent activation of striatal direct- and indirect-pathways during action initiation. Nature. 494(7436):238-42. doi: 10.1038/nature11846.
  • Koralek, AC*, Jin, X*, Long II, JD, Costa RM*, Carmena JM*. (2012). Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature, 483(7389):331-5. doi: 10.1038/nature10845.
  • Afonso C, Paixão VB, Costa, RM (2012). Chronic Toxoplasma Infection Modifies the Structure and the Risk of Host Behavior. PLoS One, 7(3):e32489. doi: 10.1371/journal.pone.0032489.
  • Hilário, MR, Holloway, T, Jin, X, Costa, RM (2012). Different dorsal striatum circuits mediate action discrimination and action generalization. European Journal of Neuroscience, 35(7):1105-14. doi: 10.1111/j.1460-9568.2012.08073.
  • French CA, Jin X, Campbell TG, Gerfen E, Groszer M, Fisher SE, Costa RM (2011). An aetiological Foxp2 mutation causes aberrant striatal activity and alters plasticity during skill learning. Molecular Psychiatry, 17(11):1077-85. doi: 10.1038/mp.2011.105.
  • Jin X & Costa RM (2010). Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature;466(7305):457-62. doi: 10.1038/nature09263.
  • Electrophysiology 
  • Neural Circuits 
  • Optogenetics 
  • Movement 
  • Neural circuits of motor control 
  • Imaging and electrophysiology