The Roles of Potassium and Calcium Currents in the Bistable Firing Transition
Healthy brains display a wide range of firing patterns, from synchronized oscillations during slow-wave sleep to desynchronized firing during movement. These physiological activities coexist with periods of pathological hyperactivity in the epileptic brain, where neurons can fire in synchronized bur...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-09-01
|
| Series: | Brain Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-3425/13/9/1347 |
| _version_ | 1797581029040455680 |
|---|---|
| author | Fernando S. Borges Paulo R. Protachevicz Diogo L. M. Souza Conrado F. Bittencourt Enrique C. Gabrick Lucas E. Bentivoglio José D. Szezech Antonio M. Batista Iberê L. Caldas Salvador Dura-Bernal Rodrigo F. O. Pena |
| author_facet | Fernando S. Borges Paulo R. Protachevicz Diogo L. M. Souza Conrado F. Bittencourt Enrique C. Gabrick Lucas E. Bentivoglio José D. Szezech Antonio M. Batista Iberê L. Caldas Salvador Dura-Bernal Rodrigo F. O. Pena |
| author_sort | Fernando S. Borges |
| collection | DOAJ |
| description | Healthy brains display a wide range of firing patterns, from synchronized oscillations during slow-wave sleep to desynchronized firing during movement. These physiological activities coexist with periods of pathological hyperactivity in the epileptic brain, where neurons can fire in synchronized bursts. Most cortical neurons are pyramidal regular spiking (RS) cells with frequency adaptation and do not exhibit bursts in current-clamp experiments (in vitro). In this work, we investigate the transition mechanism of spike-to-burst patterns due to slow potassium and calcium currents, considering a conductance-based model of a cortical RS cell. The joint influence of potassium and calcium ion channels on high synchronous patterns is investigated for different synaptic couplings (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>g</mi><mi>syn</mi></msub></semantics></math></inline-formula>) and external current inputs (<i>I</i>). Our results suggest that slow potassium currents play an important role in the emergence of high-synchronous activities, as well as in the spike-to-burst firing pattern transitions. This transition is related to the bistable dynamics of the neuronal network, where physiological asynchronous states coexist with pathological burst synchronization. The hysteresis curve of the coefficient of variation of the inter-spike interval demonstrates that a burst can be initiated by firing states with neuronal synchronization. Furthermore, we notice that high-threshold (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">L</mi></msub></semantics></math></inline-formula>) and low-threshold (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">T</mi></msub></semantics></math></inline-formula>) ion channels play a role in increasing and decreasing the parameter conditions (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>g</mi><mi>syn</mi></msub></semantics></math></inline-formula> and <i>I</i>) in which bistable dynamics occur, respectively. For high values of <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">L</mi></msub></semantics></math></inline-formula> conductance, a synchronous burst appears when neurons are weakly coupled and receive more external input. On the other hand, when the conductance <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">T</mi></msub></semantics></math></inline-formula> increases, higher coupling and lower <i>I</i> are necessary to produce burst synchronization. In light of our results, we suggest that channel subtype-specific pharmacological interactions can be useful to induce transitions from pathological high bursting states to healthy states. |
| first_indexed | 2024-03-10T22:58:20Z |
| format | Article |
| id | doaj.art-65f637f77b404c35835fe243fa9af73f |
| institution | Directory Open Access Journal |
| issn | 2076-3425 |
| language | English |
| last_indexed | 2024-03-10T22:58:20Z |
| publishDate | 2023-09-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Brain Sciences |
| spelling | doaj.art-65f637f77b404c35835fe243fa9af73f2023-11-19T09:49:38ZengMDPI AGBrain Sciences2076-34252023-09-01139134710.3390/brainsci13091347The Roles of Potassium and Calcium Currents in the Bistable Firing TransitionFernando S. Borges0Paulo R. Protachevicz1Diogo L. M. Souza2Conrado F. Bittencourt3Enrique C. Gabrick4Lucas E. Bentivoglio5José D. Szezech6Antonio M. Batista7Iberê L. Caldas8Salvador Dura-Bernal9Rodrigo F. O. Pena10Department of Physiology and Pharmacology, State University of New York Downstate Health Sciences University, Brooklyn, NY 11203, USAInstitute of Physics, University of São Paulo, São Paulo 05508-090, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilGraduate Program in Science, State University of Ponta Grossa, Ponta Grossa 84010-330, BrazilInstitute of Physics, University of São Paulo, São Paulo 05508-090, BrazilDepartment of Physiology and Pharmacology, State University of New York Downstate Health Sciences University, Brooklyn, NY 11203, USADepartment of Biological Sciences, Florida Atlantic University, Jupiter, FL 33458, USAHealthy brains display a wide range of firing patterns, from synchronized oscillations during slow-wave sleep to desynchronized firing during movement. These physiological activities coexist with periods of pathological hyperactivity in the epileptic brain, where neurons can fire in synchronized bursts. Most cortical neurons are pyramidal regular spiking (RS) cells with frequency adaptation and do not exhibit bursts in current-clamp experiments (in vitro). In this work, we investigate the transition mechanism of spike-to-burst patterns due to slow potassium and calcium currents, considering a conductance-based model of a cortical RS cell. The joint influence of potassium and calcium ion channels on high synchronous patterns is investigated for different synaptic couplings (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>g</mi><mi>syn</mi></msub></semantics></math></inline-formula>) and external current inputs (<i>I</i>). Our results suggest that slow potassium currents play an important role in the emergence of high-synchronous activities, as well as in the spike-to-burst firing pattern transitions. This transition is related to the bistable dynamics of the neuronal network, where physiological asynchronous states coexist with pathological burst synchronization. The hysteresis curve of the coefficient of variation of the inter-spike interval demonstrates that a burst can be initiated by firing states with neuronal synchronization. Furthermore, we notice that high-threshold (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">L</mi></msub></semantics></math></inline-formula>) and low-threshold (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">T</mi></msub></semantics></math></inline-formula>) ion channels play a role in increasing and decreasing the parameter conditions (<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>g</mi><mi>syn</mi></msub></semantics></math></inline-formula> and <i>I</i>) in which bistable dynamics occur, respectively. For high values of <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">L</mi></msub></semantics></math></inline-formula> conductance, a synchronous burst appears when neurons are weakly coupled and receive more external input. On the other hand, when the conductance <inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mi>I</mi><mi mathvariant="normal">T</mi></msub></semantics></math></inline-formula> increases, higher coupling and lower <i>I</i> are necessary to produce burst synchronization. In light of our results, we suggest that channel subtype-specific pharmacological interactions can be useful to induce transitions from pathological high bursting states to healthy states.https://www.mdpi.com/2076-3425/13/9/1347ion channelsfiring pattern transitionburst synchronizationbistabilityhysteresis |
| spellingShingle | Fernando S. Borges Paulo R. Protachevicz Diogo L. M. Souza Conrado F. Bittencourt Enrique C. Gabrick Lucas E. Bentivoglio José D. Szezech Antonio M. Batista Iberê L. Caldas Salvador Dura-Bernal Rodrigo F. O. Pena The Roles of Potassium and Calcium Currents in the Bistable Firing Transition Brain Sciences ion channels firing pattern transition burst synchronization bistability hysteresis |
| title | The Roles of Potassium and Calcium Currents in the Bistable Firing Transition |
| title_full | The Roles of Potassium and Calcium Currents in the Bistable Firing Transition |
| title_fullStr | The Roles of Potassium and Calcium Currents in the Bistable Firing Transition |
| title_full_unstemmed | The Roles of Potassium and Calcium Currents in the Bistable Firing Transition |
| title_short | The Roles of Potassium and Calcium Currents in the Bistable Firing Transition |
| title_sort | roles of potassium and calcium currents in the bistable firing transition |
| topic | ion channels firing pattern transition burst synchronization bistability hysteresis |
| url | https://www.mdpi.com/2076-3425/13/9/1347 |
| work_keys_str_mv | AT fernandosborges therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT paulorprotachevicz therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT diogolmsouza therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT conradofbittencourt therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT enriquecgabrick therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT lucasebentivoglio therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT josedszezech therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT antoniombatista therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT iberelcaldas therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT salvadordurabernal therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT rodrigofopena therolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT fernandosborges rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT paulorprotachevicz rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT diogolmsouza rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT conradofbittencourt rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT enriquecgabrick rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT lucasebentivoglio rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT josedszezech rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT antoniombatista rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT iberelcaldas rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT salvadordurabernal rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition AT rodrigofopena rolesofpotassiumandcalciumcurrentsinthebistablefiringtransition |