Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation

Pioneering work with nonhuman primates and recent human studies established intracortical microstimulation (ICMS) in primary somatosensory cortex (S1) as a method of inducing discriminable artificial sensation. However, these artificial sensations do not yet provide the breadth of cutaneous and proprioceptive percepts available through natural stimulation. In a tetraplegic human with two microelectrode arrays implanted in S1, we report replicable elicitations of sensations in both the cutaneous and proprioceptive modalities localized to the contralateral arm, dependent on both amplitude and frequency of stimulation. Furthermore, we found a subset of electrodes that exhibited multimodal properties, and that proprioceptive percepts on these electrodes were associated with higher amplitudes, irrespective of the frequency. These novel results demonstrate the ability to provide naturalistic percepts through ICMS that can more closely mimic the body’s natural physiological capabilities. Furthermore, delivering both cutaneous and proprioceptive sensations through artificial somatosensory feedback could improve performance and embodiment in brain-machine interfaces.

[1]  D. Borton,et al.  Delivering the Sense of Touch to the Human Brain , 2017, Neuron.

[2]  Benoit P. Delhaye,et al.  The neural basis of perceived intensity in natural and artificial touch , 2016, Science Translational Medicine.

[3]  Stephen T. Foldes,et al.  Intracortical microstimulation of human somatosensory cortex , 2016, Science Translational Medicine.

[4]  Jeffrey M Yau,et al.  Neurophysiology of Tactile Perception : A Tribute to Steven Hsiao Feeling form : the neural basis of haptic shape perception , 2016 .

[5]  Lee E Miller,et al.  Toward a Proprioceptive Neural Interface that Mimics Natural Cortical Activity. , 2016, Advances in experimental medicine and biology.

[6]  S. Bensmaia,et al.  Behavioral assessment of sensitivity to intracortical microstimulation of primate somatosensory cortex , 2015, Proceedings of the National Academy of Sciences.

[7]  R. Andersen,et al.  Decoding motor imagery from the posterior parietal cortex of a tetraplegic human , 2015, Science.

[8]  Steven S. Hsiao,et al.  Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex , 2015, Neuron.

[9]  Joseph E O'Doherty,et al.  A learning–based approach to artificial sensory feedback leads to optimal integration , 2014, Nature Neuroscience.

[10]  Spencer Kellis,et al.  A cognitive neuroprosthetic that uses cortical stimulation for somatosensory feedback , 2014, Journal of neural engineering.

[11]  L. Miller,et al.  Restoring sensorimotor function through intracortical interfaces: progress and looming challenges , 2014, Nature Reviews Neuroscience.

[12]  R. J. Vogelstein,et al.  Restoring the sense of touch with a prosthetic hand through a brain interface , 2013, Proceedings of the National Academy of Sciences.

[13]  E. Fetz,et al.  Direct electrical stimulation of the somatosensory cortex in humans using electrocorticography electrodes: a qualitative and quantitative report , 2013, Journal of neural engineering.

[14]  Peter J. Ifft,et al.  Active tactile exploration enabled by a brain-machine-brain interface , 2011, Nature.

[15]  Sabine Kastner,et al.  , Extrastriate Cortex as Revealed by Functional MRI Mechanisms of Directed Attention in the Human , 2009 .

[16]  R. Romo,et al.  Neuronal correlates of subjective sensory experience , 2005, Nature Neuroscience.

[17]  Li Min Chen,et al.  Modality maps within primate somatosensory cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Sandra E. Black,et al.  Task-Relevant Modulation of Contralateral and Ipsilateral Primary Somatosensory Cortex and the Role of a Prefrontal-Cortical Sensory Gating System , 2002, NeuroImage.

[19]  C I Moore,et al.  Referred phantom sensations and cortical reorganization after spinal cord injury in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[20]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[21]  R. Romo,et al.  Sensing without Touching Psychophysical Performance Based on Cortical Microstimulation , 2000, Neuron.

[22]  Leslie G. Ungerleider,et al.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. , 1998, Science.

[23]  R. Romo,et al.  Somatosensory discrimination based on cortical microstimulation , 1998, Nature.

[24]  Richard M. Napier,et al.  Large-Scale Sprouting of Cortical Connections After Peripheral Injury in Adult Macaque Monkeys , 1998 .

[25]  R. Daroff,et al.  Clinical Neurology for Psychiatrists , 1995, Neurology.

[26]  C. Ghez,et al.  Loss of proprioception produces deficits in interjoint coordination. , 1993, Journal of neurophysiology.

[27]  J. Kaas,et al.  The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. , 1983, Annual review of neuroscience.

[28]  J. Kaas,et al.  What, if anything, is SI? Organization of first somatosensory area of cortex. , 1983, Physiological reviews.

[29]  B. Whitsel,et al.  Anterior parietal cortical topographic organization in macaque monkey: a reevaluation. , 1982, Journal of neurophysiology.

[30]  J. Kaas,et al.  Multiple representations of the body within the primary somatosensory cortex of primates. , 1979, Science.

[31]  R. S. Snider,et al.  NEUROPHYSIOLOGY , 1921, Insect Physiology and Biochemistry.