Cortical Plasticity Induced by Spike-Triggered Microstimulation in Primate Somatosensory Cortex
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{"title"=>"Cortical Plasticity Induced by Spike-Triggered Microstimulation in Primate Somatosensory Cortex", "type"=>"journal", "authors"=>[{"first_name"=>"Weiguo", "last_name"=>"Song", "scopus_author_id"=>"55459542200"}, {"first_name"=>"Cliff C.", "last_name"=>"Kerr", "scopus_author_id"=>"23019430200"}, {"first_name"=>"William W.", "last_name"=>"Lytton", "scopus_author_id"=>"7004111060"}, {"first_name"=>"Joseph T.", "last_name"=>"Francis", "scopus_author_id"=>"35589927500"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"368465531", "doi"=>"10.1371/journal.pone.0057453", "sgr"=>"84874598541", "scopus"=>"2-s2.0-84874598541", "isbn"=>"1932-6203 (Electronic) 1932-6203 (Linking)", "pmid"=>"23472086"}, "id"=>"f6c1f3b6-eb8e-3702-a0ce-a121e6a9b1fd", "abstract"=>"Electrical stimulation of the nervous system for therapeutic purposes, such as deep brain stimulation in the treatment of Parkinson's disease, has been used for decades. Recently, increased attention has focused on using microstimulation to restore functions as diverse as somatosensation and memory. However, how microstimulation changes the neural substrate is still not fully understood. Microstimulation may cause cortical changes that could either compete with or complement natural neural processes, and could result in neuroplastic changes rendering the region dysfunctional or even epileptic. As part of our efforts to produce neuroprosthetic devices and to further study the effects of microstimulation on the cortex, we stimulated and recorded from microelectrode arrays in the hand area of the primary somatosensory cortex (area 1) in two awake macaque monkeys. We applied a simple neuroprosthetic microstimulation protocol to a pair of electrodes in the area 1 array, using either random pulses or pulses time-locked to the recorded spiking activity of a reference neuron. This setup was replicated using a computer model of the thalamocortical system, which consisted of 1980 spiking neurons distributed among six cortical layers and two thalamic nuclei. Experimentally, we found that spike-triggered microstimulation induced cortical plasticity, as shown by increased unit-pair mutual information, while random microstimulation did not. In addition, there was an increased response to touch following spike-triggered microstimulation, along with decreased neural variability. The computer model successfully reproduced both qualitative and quantitative aspects of the experimental findings. The physiological findings of this study suggest that even simple microstimulation protocols can be used to increase somatosensory information flow.", "link"=>"http://www.mendeley.com/research/cortical-plasticity-induced-spiketriggered-microstimulation-primate-somatosensory-cortex", "reader_count"=>79, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Student > Doctoral Student"=>3, "Researcher"=>22, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>4, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Student > Doctoral Student"=>3, "Researcher"=>22, "Student > Ph. D. Student"=>33, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>4, "Student > Bachelor"=>3, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Engineering"=>15, "Agricultural and Biological Sciences"=>24, "Medicine and Dentistry"=>6, "Neuroscience"=>19, "Sports and Recreations"=>1, "Physics and Astronomy"=>2, "Psychology"=>6, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>15}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Neuroscience"=>{"Neuroscience"=>19}, "Sports and Recreations"=>{"Sports and Recreations"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Psychology"=>{"Psychology"=>6}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Computer Science"=>{"Computer Science"=>2}, "Unspecified"=>{"Unspecified"=>4}}, "reader_count_by_country"=>{"Republic of Singapore"=>2, "United States"=>6, "Japan"=>1, "United Kingdom"=>1}, "group_count"=>4}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/977591"], "description"=>"<p>(<b>A</b>) We identified four types of units based on whether they responded to tactile stimuli both before and after microstimulation (“Always respond”), responded before but not after microstimulation (“Respond before”), responded after but not before microstimulation (“Respond after”), or did not respond to any tactile stimuli (“Never respond”). Nearly identical proportions of each type were observed in the experiment and in the simulation. (<b>B</b>) Mutual information (in bits) as a function of unit responsiveness type. Unit-pair mutual information was significantly increased following microstimulation for each unit type; units that always responded to stimuli had much larger mutual information than other unit types. Error bars show standard error. (<b>C</b>) Relationship between unit responsiveness and distance to stimulating electrode. Units that either never responded to tactile stimulation, or only responded before microstimulation, were statistically significantly closer to the stimulating electrode than units that responded both before and after microstimulation. * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["tactile"], "article_id"=>644763, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g006", "stats"=>{"downloads"=>2, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Responsiveness_to_tactile_stimulation_/644763", "title"=>"Responsiveness to tactile stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:56:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/977564"], "description"=>"<p>(<b>A</b>) Examples of unit-pair mutual information from single sessions before and after microstimulation. The white asterisk indicates the triggering reference unit. (<b>B</b>) Mutual information for all sessions, showing a 15% increase following microstimulation. (<b>C</b>) Multi-information for all sessions, showing a 25% increase following microstimulation. Circles and dots show data from subjects JK and AC8, respectively. (<b>D</b>) Cumulative distribution functions for mutual information in experimental (top) and simulated (bottom) conditions. * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["Computational biology", "biotechnology", "neuroscience"], "article_id"=>644748, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_mutual_information_measured_in_bits_/644748", "title"=>"Changes in mutual information (measured in bits).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:53:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/977558"], "description"=>"<p>(<b>A</b>) Example response patterns, showing normalized firing rate as a function of peristimulus time and unit number. (<b>B</b>) Ensemble firing rates increase following microstimulation in both experiment (session averages shown) and simulation; however, the simulation provides access to 100 times as many units. (<b>C</b>) Peristimulus time histograms. Similar response shapes are seen in the experiment and simulation, including increased prestimulus activity and increased peak firing rate. (<b>D</b>) Changes in the Fano factor averaged across all units. Neural variability decreases during tactile response, an effect enhanced following microstimulation in both the experimental and simulated conditions. (<b>E</b>) Stimulus-induced reductions in the Fano factor before and after experimental microstimulation across sessions. A larger post-stimulus decrease in the Fano factor is seen following microstimulation. Circles and dots show data from subjects JK and AC8, respectively. * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["responses"], "article_id"=>644745, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ensemble_network_level_responses_and_dynamics_before_and_after_microstimulation_/644745", "title"=>"Ensemble (network level) responses and dynamics before and after microstimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:52:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/977548"], "description"=>"<p>(<b>A</b>) Monkeys were seated comfortably in a non-human primate chair with their right arm and hand restrained in a KINARM. The finger to undergo tactile stimulation was fixed in a finger cast (customized based on individual finger and monkey) just above the solenoid plunger. (<b>B</b>) The delay from the solenoid control pulse to the plunger touching the skin was calibrated with a force sensor (error bars show SD). (<b>C</b>) Multi-electrode arrays were implanted close to the central sulcus (CS), in the hand representation area (S1 area 1). (<b>D</b>) Daily training sessions were comprised of three segments: tactile stimulation, microstimulation, and tactile stimulation. Each tactile stimulus had a duration of 0.3 s and indented the skin by 1 mm, and was applied with a mean frequency of 0.5 Hz. Microstimulation consisted of two biphasic pulses of amplitude 50 µA, and were triggered by spikes recorded from the reference unit, subject to a 5 ms delay. (<b>E</b>) Typical waveforms and inter-spike intervals (ISIs) of single and multi-units. (<b>F</b>) Activation maps show firing rate as a function of electrode position; each square corresponds to one electrode in the 10×10 array. There were broad cortical responses to tactile stimulation. The stimulating source is shown by the upward triangle, the stimulating sink by the downward triangle, and the triggering reference unit by the circle.</p>", "links"=>[], "tags"=>["protocols"], "article_id"=>644739, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g001", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Training_protocols_and_general_observations_/644739", "title"=>"Training protocols and general observations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:51:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/977573"], "description"=>"<p>(<b>A</b>) Two example conditioning phases showing that unit-pair mutual information increased after microstimulation following either intra-stimulation potentiation (top panel) or intra-stimulation depression (bottom panel). (<b>B</b>) Conditioning effects for multi-information, showing evidence of potentiation across sessions. (<b>C</b>) Mutual information as a function of distance between the units in experimental (left) and simulated (right) conditions. The mutual information was generally higher for nearby pairs than for distant ones, although this effect was less pronounced following microstimulation. In the simulation, the effect was especially pronounced within the first 100 µm. Experimental distances are approximate, since cell body locations cannot be precisely determined from recording electrodes; hence, slight scatter has been added to the electrode separations to show the density of points at each distance. (<b>D</b>) The effect of the reference unit used for spike-triggered microstimulation. Unit pairs that included the reference unit showed a greater increase in mutual information following microstimulation than pairs that did not. * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["Computational biology", "biotechnology", "neuroscience"], "article_id"=>644756, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conditioning_effects_on_mutual_information_in_bits_/644756", "title"=>"Conditioning effects on mutual information (in bits).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:54:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/977595"], "description"=>"<p>Different parameters before and after either random microstimulation conditioning or persistent touch conditioning (<b>A</b>) and their percentage changes (<b>B</b>). Random microstimulation had no statistically significant differences on peak firing rate (FR; in Hz), Fano factor (FF), unit-pair mutual information (in bits), or multi-information (in bits). Persistent tactile stimulation resulted in a statistically significant decrease in firing rate, but no significant changes in other variables. Error bars show standard error. * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["plasticity"], "article_id"=>644765, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g007", "stats"=>{"downloads"=>0, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Context_dependent_plasticity_effects_/644765", "title"=>"Context-dependent plasticity effects.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:56:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/977583"], "description"=>"<p>(<b>A</b>) Example of a unit-pair crosscorrelogram before and after microstimulation, showing the mean correlation (solid gray line) and 95% confidence interval (dotted gray lines). (<b>B</b>) The unit-pair correlation coefficient matrix, constructed from statistically significantly correlated unit-pairs from the ensemble, showed enhanced correlation after microstimulation. The mean correlation coefficient was significantly higher after microstimulation (Wilcoxon sign-rank test, <i>p</i><0.05). (<b>C</b>) A statistically significant increase in correlation between units was also observed between units across sessions (Wilcoxon sign-rank test, <i>p</i><0.05). (<b>D</b>) The cumulative distribution function for unit-pair correlations before and after microstimulation from the whole population also showed a statistically significant change (Kolmogorov-Smirnov test, <i>p</i><0.05). * = <i>p</i><0.05.</p>", "links"=>[], "tags"=>["Computational biology", "biotechnology", "neuroscience"], "article_id"=>644761, "categories"=>["Biological Sciences", "Biotechnology", "Neuroscience"], "users"=>["Weiguo Song", "Cliff C. Kerr", "William W. Lytton", "Joseph T. Francis"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0057453.g005", "stats"=>{"downloads"=>1, "page_views"=>22, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Unit_pair_correlation_changes_/644761", "title"=>"Unit-pair correlation changes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-03-06 08:55:41"}

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Relative Metric

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