Hand Control With Invasive Feedback Is Not Impaired by Increased Cognitive Load
Giacomo Valle, Edoardo D'Anna, Ivo Strauss, Francesco Clemente, Giuseppe Granata, Riccardo Di Iorio, Marco Controzzi, Thomas Stieglitz, Paolo M Rossini, Francesco M Petrini, Silvestro Micera, Giacomo Valle, Edoardo D'Anna, Ivo Strauss, Francesco Clemente, Giuseppe Granata, Riccardo Di Iorio, Marco Controzzi, Thomas Stieglitz, Paolo M Rossini, Francesco M Petrini, Silvestro Micera
Abstract
Recent experiments have shown that neural stimulation can successfully restore sensory feedback in upper-limb amputees improving their ability to control the prosthesis. However, the potential advantages of invasive sensory feedback with respect to non-invasive solutions have not been yet identified. Our hypothesis was that a difference would appear when the subject cannot focus all the attention to the use of the prosthesis, but some additional activities require his/her cognitive attention, which is a quite common situation in real-life conditions. To verify this hypothesis, we asked a trans-radial amputee, equipped with a bidirectional hand prosthesis, to perform motor tasks also in combination with a cognitive task. Sensory feedback was provided via intraneural (invasive) or electro-tactile (non-invasive) stimulation. We collected also data related to self-confidence. While both approaches were able to significantly improve the motor performance of the subject when no additional cognitive effort was asked, the manual accuracy was not affected by the cognitive task only when intraneural feedback was provided. The highest self-confidence was obtained when intraneural sensory feedback was provided. Our findings show that intraneural sensory feedback is more robust to dual tasks than non-invasive feedback. This is the first direct comparison between invasive and non-invasive approaches for restoring sensory feedback and it could suggest an advantage of using invasive solutions. Clinical Trial Registration: www.ClinicalTrials.gov, identifier NCT02848846.
Keywords: cognitive load; electrical stimulation; neural interfaces; neural sensory feedback; prosthesis; superficial sensory feedback; upper limb amputees.
Copyright © 2020 Valle, D’Anna, Strauss, Clemente, Granata, Di Iorio, Controzzi, Stieglitz, Rossini, Petrini and Micera.
Figures
References
- Belter J. T., Segil J. L., Dollar A. M., Weir R. F. (2013). Mechanical design and performance specifications of anthropomorphic prosthetic hands: a review. J. Rehabil. Res. Dev. Wash. 50 599–618.
- Biddiss E. A., Chau T. T. (2007). Upper limb prosthesis use and abandonment: a survey of the last 25 years. Prosthet. Orthot. Int. 31 236–257. 10.1080/03093640600994581
- Blackburn H. L., Benton A. L. (1957). Revised administration and scoring of the digit span test. J. Consult. Psychol. 21 139–143. 10.1037/h0047235
- Clemente F., D’Alonzo M., Controzzi M., Edin B. B., Cipriani C. (2016). Non-invasive, temporally discrete feedback of object contact and release improves grasp control of closed-loop myoelectric transradial prostheses. IEEE Trans. Neural Syst. Rehabil. Eng. 24 1314–1322. 10.1109/TNSRE.2015.2500586
- D’Anna E., Petrini F. M., Artoni F., Popovic I., Simanić I., Raspopovic S., et al. (2017). A somatotopic bidirectional hand prosthesis with transcutaneous electrical nerve stimulation based sensory feedback. Sci. Rep. 7:10930. 10.1038/s41598-017-11306-w
- D’Anna E., Valle G., Mazzoni A., Strauss I., Iberite F., Patton J., et al. (2019). A closed-loop hand prosthesis with simultaneous intraneural tactile and position feedback. Sci. Robot. 4:eaau8892 10.1126/scirobotics.aau8892
- Davis T. S., Wark H. A. C., Hutchinson D. T., Warren D. J., O’Neill K., Scheinblum T., et al. (2016). Restoring motor control and sensory feedback in people with upper extremity amputations using arrays of 96 microelectrodes implanted in the median and ulnar nerves. J. Neural Eng. 13:036001. 10.1088/1741-2560/13/3/036001
- Jones G., Macken B. (2015). Questioning short-term memory and its measurement: why digit span measures long-term associative learning. Cognition 144 1–13. 10.1016/j.cognition.2015.07.009
- Land M., Mennie N., Rusted J. (1999). The roles of vision and eye movements in the control of activities of daily living. Perception 28 1311–1328. 10.1068/p2935
- Lezak M. D., Howieson D. B., Bigler E. D., Tranel D. (2012). Neuropsychological Assessment. Oxford: Oxford University Press.
- Lovett M. C., Daily L. Z., Reder L. M. (2000). A source activation theory of working memory: cross-task prediction of performance in ACT-R. Cogn. Syst. Res. 1 99–118. 10.1016/S1389-0417(99)00012-11
- Marasco P. D., Hebert J. S., Sensinger J. W., Shell C. E., Schofield J. S., Thumser Z. C., et al. (2018). Illusory movement perception improves motor control for prosthetic hands. Sci. Transl. Med. 10:aao6990. 10.1126/scitranslmed.aao6990
- Meyer T. M. (2003). Psychological aspects of mutilating hand injuries. Hand Clin. 19 41–49. 10.1016/s0749-0712(02)00056-2
- Okorokova E., He Q., Bensmaia S. J. (2018). Biomimetic encoding model for restoring touch in bionic hands through a nerve interface. J. Neural Eng. 15:066033. 10.1088/1741-2552/aae398
- Osborn L. E., Dragomir A., Betthauser J. L., Hunt C. L., Nguyen H. H., Kaliki R. R., et al. (2018). Prosthesis with neuromorphic multilayered e-dermis perceives touch and pain. Sci. Robot. 19:eaat3818. 10.1126/scirobotics.aat3818
- Petrini F. M., Valle G., Strauss I., Granata G., Di Iorio R., D’Anna E., et al. (2018). Six-months assessment of a hand prosthesis with intraneural tactile feedback. Ann. Neurol. 85 137–154. 10.1002/ana.25384
- Raspopovic S., Capogrosso M., Petrini F. M., Bonizzato M., Rigosa J., Di Pino G., et al. (2014). Restoring natural sensory feedback in real-time bidirectional hand prostheses. Sci. Transl. Med. 6:222ra19. 10.1126/scitranslmed.3006820
- Raveh E., Friedman J., Portnoy S. (2018). Evaluation of the effects of adding vibrotactile feedback to myoelectric prosthesis users on performance and visual attention in a dual-task paradigm. Clin. Rehabil. 32 1308–1316. 10.1177/0269215518774104
- Risso G., Valle G., Iberite F., Strauss I., Stieglitz T., Controzzi M., et al. (2019). Optimal integration of intraneural somatosensory feedback with visual information: a single-case study. Sci. Rep. 9:7916. 10.1038/s41598-019-43815-43811
- Schiefer M. A., Graczyk E. L., Sidik S. M., Tan D. W., Tyler D. J. (2018). Artificial tactile and proprioceptive feedback improves performance and confidence on object identification tasks. PLoS One 13:e0207659. 10.1371/journal.pone.0207659
- Tan D. W., Schiefer M. A., Keith M. W., Anderson J. R., Tyler J., Tyler D. J. (2014). A neural interface provides long-term stable natural touch perception. Sci. Transl. Med. 6:257ra138. 10.1126/scitranslmed.3008669
- Valle G., Mazzoni A., Iberite F., D’Anna E., Strauss I., Granata G., et al. (2018). Biomimetic intraneural sensory feedback enhances sensation naturalness, tactile sensitivity, and manual dexterity in a bidirectional prosthesis. Neuron 100:37.e–45.e. 10.1016/j.neuron.2018.08.033
- Williams R. M., Turner A. P., Orendurff M., Segal A. D., Klute G. K., Pecoraro J., et al. (2006). Does having a computerized prosthetic knee influence cognitive performance during amputee walking? Arch. Phys. Med. Rehabil. 87 989–994. 10.1016/j.apmr.2006.03.006
Source: PubMed