Dysregulation of the Descending Pain System in Temporomandibular Disorders Revealed by Low-Frequency Sensory Transcutaneous Electrical Nerve Stimulation: A Pupillometric Study
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{"title"=>"Dysregulation of the descending pain system in temporomandibular disorders revealed by low-frequency sensory transcutaneous electrical nerve stimulation: A pupillometric study", "type"=>"journal", "authors"=>[{"first_name"=>"Annalisa", "last_name"=>"Monaco", "scopus_author_id"=>"7201638981"}, {"first_name"=>"Ruggero", "last_name"=>"Cattaneo", "scopus_author_id"=>"23472142200"}, {"first_name"=>"Luca", "last_name"=>"Mesin", "scopus_author_id"=>"6507424702"}, {"first_name"=>"Eleonora", "last_name"=>"Ortu", "scopus_author_id"=>"36638178900"}, {"first_name"=>"Mario", "last_name"=>"Giannoni", "scopus_author_id"=>"15848196800"}, {"first_name"=>"Davide", "last_name"=>"Pietropaoli", "scopus_author_id"=>"55822965316"}], "year"=>2015, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"604372009", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0122826", "scopus"=>"2-s2.0-84929380273", "pmid"=>"25905862", "sgr"=>"84929380273"}, "id"=>"6d01bae5-80b8-3d35-94fb-43572d907e75", "abstract"=>"Using computerized pupillometry, our previous research established that the autonomic nervous system (ANS) is dysregulated in patients suffering from temporomandibular disorders (TMDs), suggesting a potential role for ANS dysfunction in pain modulation and the etiology of TMD. However, pain modulation hypotheses for TMD are still lacking. The periaqueductal gray (PAG) is involved in the descending modulation of defensive behavior and pain through μ, κ, and δ opioid receptors. Transcutaneous electrical nerve stimulation (TENS) has been extensively used for pain relief, as low-frequency stimulation can activate µ receptors. Our aim was to use pupillometry to evaluate the effect of low-frequency TENS stimulation of μ receptors on opioid descending pathways in TMD patients. In accordance with the Research Diagnostic Criteria for TMD, 18 females with myogenous TMD and 18 matched-controls were enrolled. All subjects underwent subsequent pupillometric evaluations under dark and light conditions before, soon after (end of stimulation) and long after (recovery period) sensorial TENS. The overall statistics derived from the darkness condition revealed no significant differences in pupil size between cases and controls; indeed, TENS stimulation significantly reduced pupil size in both groups. Controls, but not TMD patients, displayed significant differences in pupil size before compared with after TENS. Under light conditions, TMD patients presented a smaller pupil size compared with controls; the pupil size was reduced only in the controls. Pupil size differences were found before and during TENS and before and after TENS in the controls only. Pupillometry revealed that stimulating the descending opioid pathway with low-frequency sensory TENS of the fifth and seventh pairs of cranial nerves affects the peripheral target. The TMD patients exhibited a different pattern of response to TENS stimulation compared with the controls, suggesting that impaired modulation of the descending pain system may be involved in TMD.", "link"=>"http://www.mendeley.com/research/dysregulation-descending-pain-system-temporomandibular-disorders-revealed-lowfrequency-sensory-trans", "reader_count"=>21, "reader_count_by_academic_status"=>{"Librarian"=>1, "Researcher"=>4, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>1, "Student > Postgraduate"=>3, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Librarian"=>1, "Researcher"=>4, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>1, "Student > Postgraduate"=>3, "Student > Master"=>3, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>3, "Unspecified"=>1, "Medicine and Dentistry"=>14, "Agricultural and Biological Sciences"=>1, "Neuroscience"=>2}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>14}, "Neuroscience"=>{"Neuroscience"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Turkey"=>1, "United States"=>2, "Uruguay"=>1, "Brazil"=>1, "Spain"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2037943"], "description"=>"<p>The data are expressed as means and standard deviations (in parentheses). Asterisks and circles show the statistically significant differences.</p><p>*paired t test within groups between the pre-TENS and TENS conditions in the control group: p = 0.03.</p><p>**paired t test within groups between the pre-TENS and post-TENS conditions in the control group: p = 0.01.</p><p>°unpaired t test between the groups before TENS: p = 0.0002.</p><p>°°unpaired t test between the groups during TENS: p = 0.01.</p><p>Comparison of the Pupil Size and Yellow-Green/Infrared Light (L/D) Ratio between the Control and TMD Groups.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1393005, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.t003", "stats"=>{"downloads"=>3, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_the_Pupil_Size_and_Yellow_Green_Infrared_Light_L_D_Ratio_between_the_Control_and_TMD_Groups_/1393005", "title"=>"Comparison of the Pupil Size and Yellow-Green/Infrared Light (L/D) Ratio between the Control and TMD Groups.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-23 03:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/2037942"], "description"=>"<p>The data are expressed as means and standard deviations (in parentheses). Asterisks and circles show the statistically significant differences.</p><p>*paired t test within groups between the pre-TENS and TENS conditions in the control group: p = 0.003.</p><p>**paired t test within groups between the pre-TENS and post-TENS conditions in the control group: p = 0.0005.</p><p>°unpaired t test between the groups before TENS: p = 0.001.</p><p>°°unpaired t test between the groups during TENS: p = 0.02.</p><p>Comparison between Pupil Size in the Control and TMD Groups in the Yellow-Green Light Condition.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1393004, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.t002", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_between_Pupil_Size_in_the_Control_and_TMD_Groups_in_the_Yellow_Green_Light_Condition_/1393004", "title"=>"Comparison between Pupil Size in the Control and TMD Groups in the Yellow-Green Light Condition.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-23 03:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/2037939"], "description"=>"<p>Larson [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122826#pone.0122826.ref055\" target=\"_blank\">55</a>] proposed that in anesthetized patients, opioid action can be exerted, blocking the efferents of inhibitory neurons to the EWN. Translating this hypothesis to non-anesthetized patients, it could be suggested that opioids reduce the inhibition of interneurons, increasing the effects of excitatory afferents of the EWN. The final effect was opioid miosis. In the figure, excitatory components of the model are shown in red, while inhibitory components are shown in black.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1393001, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.g002", "stats"=>{"downloads"=>1, "page_views"=>23, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Edinger_Westphal_Nucleus_EWN_Exerts_a_Tonic_Activity_on_the_Pupil_Sphincter_/1393001", "title"=>"The Edinger-Westphal Nucleus (EWN) Exerts a Tonic Activity on the Pupil Sphincter.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-23 03:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/2037937"], "description"=>"<p>Before beginning the experimental session, each enrolled subject was prepared with TENS electrodes and connected to a turned-off TENS device. Subsequently, they underwent three experimental phases: Pre TENS stimulation (green); During TENS stimulation (red); and Post TENS stimulation (blue). Pupillometer application and its removal occurred after the acclimation period and at the end of the experimental session, respectively (green). Based on the literature, central nervous system stimulation was obtained by sensory stimulation of cranial nerves V and VII with low-frequency TENS for 21 minutes (red) [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122826#pone.0122826.ref028\" target=\"_blank\">28</a>–<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122826#pone.0122826.ref032\" target=\"_blank\">32</a>]. To avoid operator interference, the pupillometer, electrodes and TENS device were removed only at the end of the experimental session.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1392999, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.g001", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Diagram_of_the_Experimental_Protocol_/1392999", "title"=>"Diagram of the Experimental Protocol.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-23 03:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/2037941"], "description"=>"<p>The data are expressed as the mean and standard deviation (in parentheses). Asterisks indicate statistically significant differences.</p><p>*paired t test within groups between the pre-TENS and TENS conditions: p = 0.02 in the control group and p = 0.001 in the TMD group.</p><p>**paired t test within groups between the pre-TENS and post-TENS conditions in the control group: p = 0.003.</p><p>Comparison between the Pupil Size in the Control and TMD Groups in Infrared Light.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1393003, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.t001", "stats"=>{"downloads"=>5, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_between_the_Pupil_Size_in_the_Control_and_TMD_Groups_in_Infrared_Light_/1393003", "title"=>"Comparison between the Pupil Size in the Control and TMD Groups in Infrared Light.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2015-04-23 03:57:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/2037940"], "description"=>"<p>The locus coeruleus-noradrenergic system (LC) has been suggested to be a key structure in arousal, and its firing frequency tone has been correlated with wakefulness, vigilance, and sensory and pain perception. The size of the pupil correlates with the activity of LC, and light increases the frequency of firing. The action of the LC excites the excitation pathway that directly induces pupil constriction and excites inhibitory interneurons in the inhibitory pathway, exciting the inhibitor of the inhibitor; the net result is a reduction of inhibition and, indirectly, an agonist effect of the excitatory pathway of pupil constriction. Opioids act on the inhibitory pathway, and TENS has been suggested to be activated via the ventral lateral PAG and the opioid pathway. According to Valentino [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122826#pone.0122826.ref074\" target=\"_blank\">74</a>] and Curtis [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0122826#pone.0122826.ref075\" target=\"_blank\">75</a>], opioids reduce the activation of the LC, and corticotropin-releasing hormone (CRH) increases the firing rate. It is possible that low-frequency sensory TENS inhibits LC inhibitory interneurons, increasing the tone of the pupillary constrictor of the LC. TMD patients could suffer from an impairment of the inhibitory pathway stemming from the ventral lateral PAG. Consequently, pupil constriction in response to light is not counterbalanced by inhibition (smaller pupil size under yellow-green light), and low-frequency sensory TENS is unable to further induce pupil constriction. Red, excitation pathway; black, inhibitory pathway.</p>", "links"=>[], "tags"=>["pag", "Research Diagnostic Criteria", "pupil size", "TENS stimulation", "pain modulation hypotheses", "Pupil size differences", "ans", "TMD patients", "light conditions", "Temporomandibular Disorders Revealed"], "article_id"=>1393002, "categories"=>["Biological Sciences", "Science Policy"], "users"=>["Annalisa Monaco", "Ruggero Cattaneo", "Luca Mesin", "Eleonora Ortu", "Mario Giannoni", "Davide Pietropaoli"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0122826.g003", "stats"=>{"downloads"=>3, "page_views"=>250, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mechanism_of_Endogenous_Opioid_Action_Induced_by_LF_TENS_in_Non_Anesthetized_Subjects_with_Pupil_Miosis_/1393002", "title"=>"Mechanism of Endogenous Opioid Action Induced by LF TENS in Non-Anesthetized Subjects with Pupil Miosis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-04-23 03:57:43"}

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Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}
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