Integration of Sensory Quanta in Cuneate Nucleus Neurons In Vivo
Publication Date
February 08, 2013
Journal
PLOS ONE
Authors
Fredrik Bengtsson, Romain Brasselet, Roland S. Johansson, Angelo Arleo, et al
Volume
8
Issue
2
Pages
e56630
DOI
https://dx.plos.org/10.1371/journal.pone.0056630
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0056630
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23409195
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3568041
Europe PMC
http://europepmc.org/abstract/MED/23409195
Web of Science
000314660300078
Scopus
84873615322
Mendeley
http://www.mendeley.com/research/integration-sensory-quanta-cuneate-nucleus-neurons-vivo
Events
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Mendeley | Further Information

{"title"=>"Integration of Sensory Quanta in Cuneate Nucleus Neurons In Vivo", "type"=>"journal", "authors"=>[{"first_name"=>"Fredrik", "last_name"=>"Bengtsson", "scopus_author_id"=>"13610350800"}, {"first_name"=>"Romain", "last_name"=>"Brasselet", "scopus_author_id"=>"37009643200"}, {"first_name"=>"Roland S.", "last_name"=>"Johansson", "scopus_author_id"=>"7102587956"}, {"first_name"=>"Angelo", "last_name"=>"Arleo", "scopus_author_id"=>"6602727179"}, {"first_name"=>"Henrik", "last_name"=>"Jörntell", "scopus_author_id"=>"35609755400"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84873615322", "pui"=>"368325866", "doi"=>"10.1371/journal.pone.0056630", "isbn"=>"2009091655", "sgr"=>"84873615322", "pmid"=>"23409195"}, "id"=>"077cece3-a8ee-3c10-8844-42c21322cdd1", "abstract"=>"Discriminative touch relies on afferent information carried to the central nervous system by action potentials (spikes) in ensembles of primary afferents bundled in peripheral nerves. These sensory quanta are first processed by the cuneate nucleus before the afferent information is transmitted to brain networks serving specific perceptual and sensorimotor functions. Here we report data on the integration of primary afferent synaptic inputs obtained with in vivo whole cell patch clamp recordings from the neurons of this nucleus. We find that the synaptic integration in individual cuneate neurons is dominated by 4-8 primary afferent inputs with large synaptic weights. In a simulation we show that the arrangement with a low number of primary afferent inputs can maximize transfer over the cuneate nucleus of information encoded in the spatiotemporal patterns of spikes generated when a human fingertip contact objects. Hence, the observed distributions of synaptic weights support high fidelity transfer of signals from ensembles of tactile afferents. Various anatomical estimates suggest that a cuneate neuron may receive hundreds of primary afferents rather than 4-8. Therefore, we discuss the possibility that adaptation of synaptic weight distribution, possibly involving silent synapses, may function to maximize information transfer in somatosensory pathways.", "link"=>"http://www.mendeley.com/research/integration-sensory-quanta-cuneate-nucleus-neurons-vivo", "reader_count"=>35, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>16, "Student > Postgraduate"=>1, "Student > Master"=>3, "Student > Bachelor"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>11, "Unspecified"=>1, "Agricultural and Biological Sciences"=>11, "Medicine and Dentistry"=>1, "Neuroscience"=>6, "Psychology"=>2, "Computer Science"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>11}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>6}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>11}, "Computer Science"=>{"Computer Science"=>3}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United Kingdom"=>1, "Italy"=>1, "India"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/492218"], "description"=>"<p>A: Histogram showing EPSP amplitude distribution for N = 100 simulated neurons with 130 primary afferent synapses each. The random EPSP distribution (grey) and specific EPSP distribution (black), the latter reproducing to the experimentally observed amplitude distribution (Fig. 6C), corresponded to the start and end points, respectively, of the simulation (runs 1–100). B: Relationship between number of synapses and information transfer. Top: Starting from synaptic weights drawn from random (uniform distribution; grey distribution in (A)) the number of synapses decreased significantly (p<0.01, ANOVA test) as the result of a gradient-based information maximization algorithm, rendering the weight distribution of primary afferent synapses from random to bimodal (with many synapses eliminated or having 0 synaptic efficacy) (black distribution in (A); Hartigan test, dip = 0.0275, p<0.001). Bottom: The mutual information between cuneate responses and primary inputs increased significantly (p<0.01, ANOVA test) with the number of synapses becoming virtually silent regarding EPSP effects. In both cases, the graphs display the mean value +/−s.d. C: Relationship between the number of primary afferents and the number of synapses required to achieve maximal information transfer. The value for 300 primary afferents was not measured but projected from the data using linear regression. D: Relationship between the maximal unitary EPSP peak amplitude, the EPSP time constant, and the mean number of synapses required to achieve maximal information transfer in the simulated cuneate neurons. White solid lines indicate mean values for the cuneate neurons recorded in the present study, white dashed lines indicate the standard deviation of these values.</p>", "links"=>[], "tags"=>["synaptic", "efficacy", "cuneate"], "article_id"=>162736, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g007", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Simulation_of_the_relationship_between_distribution_of_synaptic_efficacy_and_information_transfer_in_cuneate_neurons_/162736", "title"=>"Simulation of the relationship between distribution of synaptic efficacy and information transfer in cuneate neurons.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:41:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/491721"], "description"=>"<p><b>A</b>: Superimposed, consecutive, unitary EPSPs evoked by electrical skin stimulation by just suprathreshold stimulation in the receptive field. Histogram at bottom (bin width = 0.1 ms) illustrate the non-variable response latency times. Every stimulation evoked an EPSP at the same response latency time (i.e. the firing probability at this time was 1.0). Dashed line indicates time of stimulation in both (A) and (D). <b>B</b>: For comparison, a corresponding histogram of the response latency times of a primary afferent spike using just suprathreshold stimulation intensity. <b>C</b>: Histogram of EPSP amplitudes evoked at just suprathreshold stimulation intensities (same cell as in (A)). <b>D</b>: Superimposed, consecutive responses evoked by threshold electrical stimulation in the receptive field (N = 12 stimulations). Only 6 of these stimulations evoked EPSPs, which had variable response latency times but essentially non-variable amplitudes (‘all-or-none’). The dashed vertical line indicates time of stimulation. Histogram at bottom illustrates the response latency times of the 13 EPSP responses obtained over 50 stimulations. Same calibrations as in (A). <b>E</b>: Response latency times of a primary afferent spike at threshold stimulation intensity. Note qualitative similarity with the spread of response latency times for the EPSP, as opposed to the non-variable latency times in (A,B). <b>F</b>: Amplitudes of EPSPs with a response latency of 5–7 ms evoked in the same cuneate neuron as represented in (D) by repeated near-threshold stimuli of constant intensity. Note the all-or-none character of the evoked response. <b>G</b>: Spontaneous activity was typically very low, with occasional spontaneous EPSPs (asterisk). <b>H</b>: Superimposition of spontaneous EPSPs with similar peak amplitudes as the evoked EPSP in (A, C) from the same cell. The peak amplitudes of the EPSPs were normalized. <b>I</b>: Comparison of raw spontaneous EPSP (grey traces) with an average of evoked EPSPs (black trace). Note the near complete congruence between spontaneous and evoked EPSPs. (H,I) same calibrations as in (A).</p>", "links"=>[], "tags"=>["neuroscience"], "article_id"=>162241, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synaptic_responses_/162241", "title"=>"Synaptic responses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:38:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/491836"], "description"=>"<p>In order to explore the EPSP-to-spike coupling in the cuneate neuron, the recording was made without hyperpolarization, i.e. the neuron was recorded at its normal resting potential. Threshold electrical skin stimulation evoked all-or-none EPSPs, i.e. they sometimes occurred (arrows) and sometimes not (second trace from the top). When the EPSP did occur, the probability that it was followed by a spike was high (see text).</p>", "links"=>[], "tags"=>["stimulation", "cuneate", "neuron"], "article_id"=>162355, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Electrical_skin_stimulation_at_threshold_intensity_in_cuneate_neuron_at_rest_/162355", "title"=>"Electrical skin stimulation at threshold intensity in cuneate neuron at rest.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:39:02"}
  • {"files"=>["https://ndownloader.figshare.com/files/491647"], "description"=>"<p><b>A</b>: Location of the main cuneate nucleus (green) in the lower brain stem. The region recorded from is outlined. A 3d scale bar is inserted. LRN, lateral reticular nucleus. <b>B</b>: Example of a cuneate neuron, displayed in the sagittal plane, that was recorded from and stained with neurobiotin. <b>C & D</b>: Receptive field outlines of the cuneate neurons and of the primary afferents recorded from in this study. Outlines are indicated in different colors for clarity.</p>", "links"=>[], "tags"=>["receptive"], "article_id"=>162161, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recording_area_and_receptive_fields_/162161", "title"=>"Recording area and receptive fields.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:38:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/492020"], "description"=>"<p>Solid black trace shows IPSP (averaged) evoked in a cuneate neuron by electrical cutaneous stimulation applied through a pair of electrodes located in the skin (x–x) outside the neuron's cutaneous receptive field (outlined zone). The membrane potential of the neuron was held at −53 mV. Maximal evoked average EPSP (evoked inside the receptive field) is shown in grey to illustratethe temporal relationship between evoked EPSPs and IPSPs. The EPSP was recorded at a membrane potential of −67 mV to prevent spiking. The longer latency of the IPSP indicates an indirect, disynaptic activation, due to the extra synaptic relay over inhibitory interneurons.</p>", "links"=>[], "tags"=>["postsynaptic", "potentials", "evoked", "cutaneous"], "article_id"=>162539, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibitory_postsynaptic_potentials_IPSPs_evoked_by_electrical_cutaneous_stimulation_/162539", "title"=>"Inhibitory postsynaptic potentials (IPSPs) evoked by electrical cutaneous stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:40:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/491943"], "description"=>"<p>Superimposed raw traces (grey) and averaged responses (black) for stimulation intensities indicated to the right. Multiple stimulation intensities indicated to the right of a trace panel indicate that the averaged responses evoked by the different intensities were of the same amplitude. In panels with two different averaged responses overlayed, the top stimulation intensities correspond to the top trace and vice versa. This illustrates the stepwise changes in the responses obtained to a graded increase in stimulation intensity. At stimulation intensities indicated in brackets to the right, all-or-none responses that straddled between the levels of response amplitudes of the two averaged traces were evoked. Insets indicated by ‘net EPSP’ represent the net response added at the higher stimulation intensity (obtained by subtracting the average response obtained at the lower stimulation intensity from the average response obtained at the higher intensity). The net EPSP is overlayed with a scaled template EPSP obtained from the same neuron (grey). Vertical dashed lines indicate the average response latency time of the EPSPs recruited at the given stimulation intensity. (Arrow in brackets indicates possible EPSP component, but with a peak amplitude that was too low to be analyzed at the unitary level).</p>", "links"=>[], "tags"=>["epsps", "graded"], "article_id"=>162462, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g004", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recruitment_of_EPSPs_during_a_graded_increase_in_the_intensity_of_the_electrical_skin_stimulation_/162462", "title"=>"Recruitment of EPSPs during a graded increase in the intensity of the electrical skin stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:39:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/492086"], "description"=>"<p><b>A</b>: Response evoked by light, mechanical stimulation normally used for receptive field mapping. Filled arrows indicate onsets of presumed unitary EPSPs and empty arrows indicate compound EPSPs, defined as depolarizing events of more than 10 mV within 1 ms, presumably generated by multiple unitary EPSPs activated nearly simultaneously. <b>B</b>: In the same cell, responses evoked by very light mechanical skin stimulation. The amplitudes of action potentials are truncated. Note difference in voltage scale compared to (A). <b>C</b>: Histogram of the peak amplitudes of EPSPs evoked by 5–10 epochs of stimulation, for all cells explored with very light skin stimulation. <b>D</b>: For comparison, histogram of the amplitudes of EPSPs evoked at threshold electrical skin stimulation (black bars) and of unitary EPSPs evoked by suprathreshold electrical skin stimulation (grey bars) (cf. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0056630#pone-0056630-g004\" target=\"_blank\">Figure 4</a>).</p>", "links"=>[], "tags"=>["responses", "evoked", "cutaneous"], "article_id"=>162607, "categories"=>["Neuroscience"], "users"=>["Fredrik Bengtsson", "Romain Brasselet", "Roland S. Johansson", "Angelo Arleo", "Henrik Jörntell"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056630.g006", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EPSP_responses_evoked_by_cutaneous_stimulation_/162607", "title"=>"EPSP responses evoked by cutaneous stimulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-19 15:40:27"}

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Relative Metric

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