Brain-machine Interface Learning is Facilitated by Specific Patterning of Distributed Cortical Feedback

Overview

Journal Sci Adv

Specialties Biology
Science

Date 2023 Sep 22

PMID 37738340

Authors

Aamir Abbasi

Henri Lassagne

Luc Estebanez

Dorian Goueytes

Daniel E Shulz

Valerie Ego-Stengel

Affiliations

Soon will be listed here.

Abstract

Neuroprosthetics offer great hope for motor-impaired patients. One obstacle is that fine motor control requires near-instantaneous, rich somatosensory feedback. Such distributed feedback may be recreated in a brain-machine interface using distributed artificial stimulation across the cortical surface. Here, we hypothesized that neuronal stimulation must be contiguous in its spatiotemporal dynamics to be efficiently integrated by sensorimotor circuits. Using a closed-loop brain-machine interface, we trained head-fixed mice to control a virtual cursor by modulating the activity of motor cortex neurons. We provided artificial feedback in real time with distributed optogenetic stimulation patterns in the primary somatosensory cortex. Mice developed a specific motor strategy and succeeded to learn the task only when the optogenetic feedback pattern was spatially and temporally contiguous while it moved across the topography of the somatosensory cortex. These results reveal spatiotemporal properties of the sensorimotor cortical integration that set constraints on the design of neuroprosthetics.

References

Sainburg R, Ghilardi M, Poizner H, Ghez C . Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol. 1995; 73(2):820-35. PMC: 11102602. DOI: 10.1152/jn.1995.73.2.820. View

Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P . Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A. 2003; 100(24):13940-5. PMC: 283525. DOI: 10.1073/pnas.1936192100. View

Monzee J, Lamarre Y, Smith A . The effects of digital anesthesia on force control using a precision grip. J Neurophysiol. 2003; 89(2):672-83. DOI: 10.1152/jn.00434.2001. View

Lassagne H, Goueytes D, Shulz D, Estebanez L, Ego-Stengel V . Continuity within the somatosensory cortical map facilitates learning. Cell Rep. 2022; 39(1):110617. DOI: 10.1016/j.celrep.2022.110617. View

Estebanez L, Bertherat J, Shulz D, Bourdieu L, Leger J . A radial map of multi-whisker correlation selectivity in the rat barrel cortex. Nat Commun. 2016; 7:13528. PMC: 5121329. DOI: 10.1038/ncomms13528. View

Mathis M, Mathis A, Uchida N . Somatosensory Cortex Plays an Essential Role in Forelimb Motor Adaptation in Mice. Neuron. 2017; 93(6):1493-1503.e6. PMC: 5491974. DOI: 10.1016/j.neuron.2017.02.049. View

Ceballo S, Piwkowska Z, Bourg J, Daret A, Bathellier B . Targeted Cortical Manipulation of Auditory Perception. Neuron. 2019; 104(6):1168-1179.e5. PMC: 6926484. DOI: 10.1016/j.neuron.2019.09.043. View

Dadarlat M, ODoherty J, Sabes P . A learning-based approach to artificial sensory feedback leads to optimal integration. Nat Neurosci. 2014; 18(1):138-44. PMC: 4282864. DOI: 10.1038/nn.3883. View

Knutsen P, Mateo C, Kleinfeld D . Precision mapping of the vibrissa representation within murine primary somatosensory cortex. Philos Trans R Soc Lond B Biol Sci. 2016; 371(1705). PMC: 5003853. DOI: 10.1098/rstb.2015.0351. View

10.

Diamond M, Arabzadeh E . Whisker sensory system - from receptor to decision. Prog Neurobiol. 2012; 103:28-40. DOI: 10.1016/j.pneurobio.2012.05.013. View

11.

Bensmaia S, Miller L . Restoring sensorimotor function through intracortical interfaces: progress and looming challenges. Nat Rev Neurosci. 2014; 15(5):313-25. DOI: 10.1038/nrn3724. View

12.

Valle G, Mazzoni A, Iberite F, DAnna E, Strauss I, Granata G . Biomimetic Intraneural Sensory Feedback Enhances Sensation Naturalness, Tactile Sensitivity, and Manual Dexterity in a Bidirectional Prosthesis. Neuron. 2018; 100(1):37-45.e7. DOI: 10.1016/j.neuron.2018.08.033. View

13.

Oby E, Golub M, Hennig J, Degenhart A, Tyler-Kabara E, Yu B . New neural activity patterns emerge with long-term learning. Proc Natl Acad Sci U S A. 2019; 116(30):15210-15215. PMC: 6660765. DOI: 10.1073/pnas.1820296116. View

14.

Sadtler P, Quick K, Golub M, Chase S, Ryu S, Tyler-Kabara E . Neural constraints on learning. Nature. 2014; 512(7515):423-6. PMC: 4393644. DOI: 10.1038/nature13665. View

15.

Arduin P, Fregnac Y, Shulz D, Ego-Stengel V . "Master" neurons induced by operant conditioning in rat motor cortex during a brain-machine interface task. J Neurosci. 2013; 33(19):8308-20. PMC: 6619624. DOI: 10.1523/JNEUROSCI.2744-12.2013. View

16.

Flesher S, Downey J, Weiss J, Hughes C, Herrera A, Tyler-Kabara E . A brain-computer interface that evokes tactile sensations improves robotic arm control. Science. 2021; 372(6544):831-836. PMC: 8715714. DOI: 10.1126/science.abd0380. View

17.

Tabot G, Dammann J, Berg J, Tenore F, Boback J, Vogelstein R . Restoring the sense of touch with a prosthetic hand through a brain interface. Proc Natl Acad Sci U S A. 2013; 110(45):18279-84. PMC: 3831459. DOI: 10.1073/pnas.1221113110. View

18.

Okun M, Lak A, Carandini M, Harris K . Long Term Recordings with Immobile Silicon Probes in the Mouse Cortex. PLoS One. 2016; 11(3):e0151180. PMC: 4784879. DOI: 10.1371/journal.pone.0151180. View

19.

Abbasi A, Goueytes D, Shulz D, Ego-Stengel V, Estebanez L . A fast intracortical brain-machine interface with patterned optogenetic feedback. J Neural Eng. 2018; 15(4):046011. DOI: 10.1088/1741-2552/aabb80. View

20.

Kremer Y, Leger J, Goodman D, Brette R, Bourdieu L . Late emergence of the vibrissa direction selectivity map in the rat barrel cortex. J Neurosci. 2011; 31(29):10689-700. PMC: 6622639. DOI: 10.1523/JNEUROSCI.6541-10.2011. View