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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Netw. Physiol.</journal-id>
<journal-title>Frontiers in Network Physiology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Netw. Physiol.</abbrev-journal-title>
<issn pub-type="epub">2674-0109</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
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<article-meta>
<article-id pub-id-type="publisher-id">1362778</article-id>
<article-id pub-id-type="doi">10.3389/fnetp.2024.1362778</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Network Physiology</subject>
<subj-group>
<subject>Original Research</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Hamiltonian energy in a modified Hindmarsh&#x2013;Rose model</article-title>
<alt-title alt-title-type="left-running-head">Zheng et al.</alt-title>
<alt-title alt-title-type="right-running-head">
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fnetp.2024.1362778">10.3389/fnetp.2024.1362778</ext-link>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Zheng</surname>
<given-names>Qianqian</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1789023/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Xu</surname>
<given-names>Yong</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/432772/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Shen</surname>
<given-names>Jianwei</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/430118/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
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<aff id="aff1">
<sup>1</sup>
<institution>School of Science</institution>, <institution>Xuchang University</institution>, <addr-line>Xuchang</addr-line>, <addr-line>Henan</addr-line>, <country>China</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>School of Mathematics and Statistics</institution>, <institution>Northwestern Polytechnical University</institution>, <addr-line>Xi&#x2019;an</addr-line>, <addr-line>Shaanxi</addr-line>, <country>China</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>School of Mathematics and Statistics</institution>, <institution>North China University of Water Resources and Electric Power</institution>, <addr-line>Zhengzhou</addr-line>, <addr-line>Henan</addr-line>, <country>China</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>
<bold>Edited by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/559434/overview">Eckehard Sch&#xf6;ll</ext-link>, Technical University of Berlin, Germany</p>
</fn>
<fn fn-type="edited-by">
<p>
<bold>Reviewed by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/2646456/overview">Ling Kang</ext-link>, Fudan University, China</p>
<p>
<ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/490476/overview">Anna Zakharova</ext-link>, Humboldt University of Berlin, Germany</p>
</fn>
<corresp id="c001">&#x2a;Correspondence: Yong Xu, <email>hsux3@nwpu.edu.cn</email>; Jianwei Shen, <email>xcjwshen@gmail.com</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>26</day>
<month>03</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>4</volume>
<elocation-id>1362778</elocation-id>
<history>
<date date-type="received">
<day>29</day>
<month>12</month>
<year>2023</year>
</date>
<date date-type="accepted">
<day>04</day>
<month>03</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Zheng, Xu and Shen.</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Zheng, Xu and Shen</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>This paper investigates the Hamiltonian energy of a modified Hindmarsh&#x2013;Rose (HR) model to observe its effect on short-term memory. A Hamiltonian energy function and its variable function are given in the reduced system with a single node according to Helmholtz&#x2019;s theorem. We consider the role of the coupling strength and the links between neurons in the pattern formation to show that the coupling and cooperative neurons are necessary for generating the fire or a clear short-term memory when all the neurons are in sync. Then, we consider the effect of the degree and external stimulus from other neurons on the emergence and disappearance of short-term memory, which illustrates that generating short-term memory requires much energy, and the coupling strength could further reduce energy consumption. Finally, the dynamical mechanisms of the generation of short-term memory are concluded.</p>
</abstract>
<kwd-group>
<kwd>HR</kwd>
<kwd>pattern formation</kwd>
<kwd>network</kwd>
<kwd>matrix</kwd>
<kwd>Turing instability</kwd>
<kwd>delay</kwd>
</kwd-group>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Networks of Dynamical Systems</meta-value>
</custom-meta>
</custom-meta-wrap>
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</front>
<body>
<sec id="s1">
<title>1 Introduction</title>
<p>Short-term memory is a primary cognitive function of the brain. The transitions between the spontaneous and persistent states could lead to the emergence and disappearance of short-term memory in a bistable system (<xref ref-type="bibr" rid="B1">Amit and Brunel, 1997)</xref>. Continuous neural activity without external inputs was deemed an expression of short-term memory (<xref ref-type="bibr" rid="B27">Wang, 2001)</xref>. A phenomenological model of spatial working memory was developed to examine the dynamical interactions of multiple feedback mechanisms (<xref ref-type="bibr" rid="B4">Carter and Wang, 2007)</xref>. A growing body of evidence suggests memories may be kept through the mutual effect of persistent neural activity and activity-silent dynamics (<xref ref-type="bibr" rid="B23">Stokes, 2015</xref>; <xref ref-type="bibr" rid="B3">Barbosa et al., 2020)</xref>. Gaussian noise was treated as an essential factor in neuronal activity and its toggle switch (memory maintenance) (<xref ref-type="bibr" rid="B39">Zheng et al., 2020b)</xref>. Memory maintenance through persistent neural activity and a synaptic mechanism was compared in mice and two types of artificial neural networks to show their differences (<xref ref-type="bibr" rid="B9">Hu et al., 2021)</xref>. Then, computational modeling was constructed to prove how the circuits and networks affect working memory, which provides a novel theory for memory maintenance (<xref ref-type="bibr" rid="B7">Ghazizadeh and Ching, 2020)</xref>. In addition, the encoding style of the input information of the short-term memory was investigated to illustrate the dynamical mechanisms of short-term memory (<xref ref-type="bibr" rid="B10">Ichikawa and Kaneko, 2021</xref>; <xref ref-type="bibr" rid="B11">Jones and Ching, 2022</xref>; <xref ref-type="bibr" rid="B41">Zhou et al., 2023)</xref>. Hamilton energy, representing the utilization of energy (actual energy in the generation of short-term memory), should be considered to illustrate the dynamic mechanism of the generation of short-term memory.</p>
<p>Hindmarsh&#x2013;Rose (HR) model (1) (<italic>x</italic> is the membrane potential, <italic>y</italic> is the recovery variable of the fast current of <italic>K</italic>
<sup>&#x2b;</sup> or <italic>Na</italic>
<sup>&#x2b;</sup>, and <italic>z</italic> is the adaptation variable of the slow current of <italic>Ca</italic>
<sup>&#x2b;</sup> or other ions) was proposed to show the membrane potential of neuronal activity (<xref ref-type="bibr" rid="B8">Hindmarsh and Rose, 1982)</xref>, which has rich dynamical behaviors (<xref ref-type="bibr" rid="B29">Wang et al. 2021a</xref>; <xref ref-type="bibr" rid="B30">Wang et al. 2021b</xref>; <xref ref-type="bibr" rid="B28">Wang et al. 2022</xref>).<disp-formula id="e1">
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<label>(1)</label>
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<p>The synchronization and bifurcation (<xref ref-type="bibr" rid="B22">Song and Xu, 2013</xref>; <xref ref-type="bibr" rid="B16">Liebovitch et al., 2011</xref>; <xref ref-type="bibr" rid="B12">Kumar et al., 2016</xref>; <xref ref-type="bibr" rid="B38">Zheng et al. 2020a</xref>; <xref ref-type="bibr" rid="B37">Zheng et al. 2024</xref>; <xref ref-type="bibr" rid="B36">Zheng et al. 2023</xref>) of the HR model were often studied to demonstrate the dynamical mechanism of chaotic bursting or spikes (<xref ref-type="bibr" rid="B20">Shi and Wang, 2012</xref>; <xref ref-type="bibr" rid="B31">Wu et al., 2016</xref>; <xref ref-type="bibr" rid="B32">You, 2023a)</xref>. The interplay between neurons was analyzed to present the effect of the parameters and coupling strength on the appropriate functioning of the system (<xref ref-type="bibr" rid="B13">Lepek and Fronczak, 2018</xref>; <xref ref-type="bibr" rid="B18">Rajagopal et al., 2019</xref>; <xref ref-type="bibr" rid="B33">You, 2023b)</xref>. Energy is necessary for neuron activity (<xref ref-type="bibr" rid="B2">Attwell and Laughlin, 2001)</xref>. The Hamiltonian energy function is a vital tool to evaluate energy consumption when neurons are active (<xref ref-type="bibr" rid="B24">Torrealdea et al., 2006)</xref>. The average energy consumption of the HR model was given to display the energy consumption ratio in different situations, which could help optimize energy use (<xref ref-type="bibr" rid="B25">Torrealdea et al., 2009</xref>; <xref ref-type="bibr" rid="B21">Song et al., 2015</xref>; <xref ref-type="bibr" rid="B26">Usha and Subha, 2019)</xref>. The Hamilton energy balance of different functional neurons was discussed through the coupling strength, which contributes to designing functional assistive devices (<xref ref-type="bibr" rid="B35">Zhang et al., 2022</xref>; <xref ref-type="bibr" rid="B34">Yu et al., 2023)</xref>. Although the HR model could explain the generation of short-term memory (<xref ref-type="bibr" rid="B40">Zheng et al., 2022)</xref>, the utilization of energy should be further stated in short-term memory.</p>
<p>Short-term memory results from neuronal activity coming with a change in energy, and a physical neuron circuit plays a vital role in the synergistic effect of neurons and the generation of short-term memory. In this paper, the pattern formation of a modified HR model is investigated to find the dynamical mechanism of how the coupling strength and links (degree) affect the generation of short-term memory. The Hamiltonian energy function is derived in the HR model with a single node, which means the energy consumption varies at different states of neuronal activity. Then, the degree and stimuli from other neurons are studied through bifurcation, which means the energy is necessary to generate short-term memory. Finally, the related dynamical and biological mechanisms are obtained.</p>
</sec>
<sec id="s2">
<title>2 Model description</title>
<p>As the membrane potential of neurons is often coupled with others, the following network-organized HR model is introduced:<disp-formula id="e2">
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</mml:mfenced>
<mml:mo>,</mml:mo>
</mml:mtd>
</mml:mtr>
</mml:mtable>
</mml:math>
<label>(2)</label>
</disp-formula>
</p>
<p>where <italic>x</italic>
<sub>
<italic>i</italic>
</sub> is the membrane potential, <italic>I</italic> represents the <italic>ith</italic> neuron and <italic>i</italic> &#x3d; 1, &#x2026; , <italic>n</italic>, <italic>y</italic>
<sub>
<italic>i</italic>
</sub> is the recovery variable of the fast current of <italic>K</italic>
<sup>&#x2b;</sup> or <italic>Na</italic>
<sup>&#x2b;</sup>, and <italic>z</italic>
<sub>
<italic>i</italic>
</sub> is the adaptation variable of the slow current of <italic>Ca</italic>
<sup>&#x2b;</sup> or other ions. <italic>D</italic>
<sub>1</sub> is the coupling strength between neurons. <italic>L</italic>
<sub>
<italic>ij</italic>
</sub>(<italic>t</italic>) &#x3d; <italic>A</italic>
<sub>
<italic>ij</italic>
</sub> &#x2013; <italic>&#x3b4;</italic>
<sub>
<italic>ij</italic>
</sub>
<italic>k</italic>
<sub>
<italic>i</italic>
</sub>, where <italic>A</italic>
<sub>
<italic>ij</italic>
</sub> is the adjacent matrix and <italic>k</italic>
<sub>
<italic>i</italic>
</sub> is the degree of the <italic>ith</italic> node.</p>
<p>In order to obtain the Hamiltonian energy function of system (2), we consider a simplified model with a single node through the mean-field approach (<xref ref-type="bibr" rid="B17">McCullen and Wagenknecht, 2016)</xref>. The reduced system is<disp-formula id="e3">
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</mml:mtd>
</mml:mtr>
</mml:mtable>
</mml:math>
<label>(3)</label>
</disp-formula>
</p>
<p>where (<italic>x</italic>
<sub>0</sub>, <italic>y</italic>
<sub>0</sub>, <italic>z</italic>
<sub>0</sub>) (<xref ref-type="bibr" rid="B40">Zheng et al., 2022)</xref> is the equilibrium point of system (2) without a network, and <italic>x</italic>
<sub>0</sub> makes <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; <italic>f</italic>(<italic>x</italic>) &#x3d; &#x2212;<italic>c</italic> &#x2b; <italic>dx</italic>
<sup>2</sup> &#x2b; <italic>ax</italic>
<sup>3</sup> &#x2212; <italic>bx</italic>
<sup>2</sup> &#x2b; <italic>s</italic> (<italic>x</italic> &#x2212; <italic>x</italic>
<sub>
<italic>r</italic>
</sub>) &#x2b; <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x2b; <italic>d</italic>
<sub>1</sub>
<italic>k</italic>
<sub>
<italic>i</italic>
</sub> (<italic>x</italic>
<sub>0</sub> &#x2212; <italic>x</italic>
<sub>
<italic>i</italic>
</sub>) hold. In addition, <italic>x</italic>
<sub>0</sub> is the external stimulus from other neurons.</p>
<p>In this paper, we mainly investigate the dynamical behaviors of system (3) and its Hamiltonian equation. According to Helmholtz&#x2019;s theorem (<xref ref-type="bibr" rid="B5">Donald and Rose, 1986)</xref>, an autonomous ordinary differential equation <inline-formula id="inf1">
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</inline-formula> (<italic>F</italic>(<italic>X</italic>) can be treated as the velocity vector field) can be described in the usual forms of a Hamiltonian equation:<disp-formula id="equ1">
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</p>
<p>where <italic>G</italic>(<italic>X</italic>) is a skew-symmetric matrix in the Hamiltonian system. If <italic>G</italic>(<italic>X</italic>) is not a skew-symmetric matrix in a generalized Hamiltonian system, <italic>G</italic>(<italic>X</italic>) can be divided into two parts <italic>G</italic>(<italic>X</italic>) &#x3d; <italic>G</italic>
<sub>1</sub>(<italic>X</italic>) &#x2b; <italic>G</italic>
<sub>2</sub>(<italic>X</italic>): a skew-symmetric matrix <italic>G</italic>
<sub>1</sub>(<italic>X</italic>) and a symmetric matrix <italic>G</italic>
<sub>2</sub>(<italic>X</italic>) (<xref ref-type="bibr" rid="B19">Sarasola et al., 2004)</xref>. <italic>H</italic>(<italic>X</italic>) is an energy function. Then, we have<disp-formula id="equ2">
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</p>
<p>For the network-organized HR model (3), it can be written as (<xref ref-type="bibr" rid="B24">Torrealdea et al., 2006</xref>; <xref ref-type="bibr" rid="B25">Torrealdea et al., 2009</xref>; <xref ref-type="bibr" rid="B21">Song et al., 2015</xref>; <xref ref-type="bibr" rid="B26">Usha and Subha, 2019)</xref>
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<sec sec-type="results|discussion" id="s3">
<title>3 Numerical results and discussion</title>
<p>In this section, the finite difference method is applied to find numerical solutions for the network-organized HR model (3) with time step <italic>dt</italic> &#x3d; 0.01. These parameters <italic>a</italic> &#x3d; 1, <italic>b</italic> &#x3d; 3, <italic>c</italic> &#x3d; 1, <italic>d</italic> &#x3d; 5, <italic>r</italic> &#x3d; 0.01, s &#x3d; 4 are set (<xref ref-type="bibr" rid="B40">Zheng et al., 2022)</xref>. The small-world network is constructed with <italic>W</italic> (<italic>n</italic>, <italic>K</italic>, <italic>p</italic>) (the number of node <italic>n</italic>, nearest neighbor <italic>K</italic>, and reconnection probability <italic>p</italic>), which can be found can be found at <ext-link ext-link-type="uri" xlink:href="https://github.com/zhengqianqian35/network-code">https://github.com/zhengqianqian35/network-code</ext-link>. We give the concept of the average Hamiltonian energy for time and nodes:<disp-formula id="equ10">
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</p>
<p>where the integration period is set at <italic>T</italic> &#x3d; 5,000 time units. In order to exclude the influence of initial conditions, <italic>t</italic>
<sub>0</sub> is the starting time of the cycle after the system tends to a stable state. In addition, we assume <italic>H</italic> &#x3d; <italic>H</italic> (<italic>x</italic>
<sub>
<italic>i</italic>
</sub>, <italic>y</italic>
<sub>
<italic>i</italic>
</sub>, <italic>z</italic>
<sub>
<italic>i</italic>
</sub>)/100. From <xref ref-type="fig" rid="F1">Figure 1</xref>, only one real equilibrium point (<italic>x</italic>
<sub>0</sub>, <italic>y</italic>
<sub>0</sub>, <italic>z</italic>
<sub>0</sub>) exists in system (1) when <italic>a</italic> &#x3d; 1, <italic>b</italic> &#x3d; 3, <italic>c</italic> &#x3d; 1, <italic>d</italic> &#x3d; 5, <italic>r</italic> &#x3d; 0.01, s &#x3d; 4, which guarantees the uniqueness of system (3).</p>
<fig id="F1" position="float">
<label>FIGURE 1</label>
<caption>
<p>Distribution of the equilibrium point in system (3) when <italic>a</italic> &#x3d; &#x7c; 1, <italic>b</italic> &#x3d; &#x7c; 3, <italic>c</italic> &#x3d; &#x7c; 1, <italic>d</italic> &#x3d; &#x7c; 5, <italic>r</italic> &#x3d; &#x7c; 0.01, s &#x3d; &#x7c; 4. <bold>(A)</bold> Distribution of the equilibrium point when <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 1. <bold>(B)</bold> Distribution of the equilibrium point when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 1.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g001.tif"/>
</fig>
<p>In general, the generation of neural function results from the collaboration of multiple neurons. Therefore, we consider the strength <italic>d</italic>
<sub>1</sub> of the coupling between neurons and the number of links <italic>K</italic>. First, a small-world network with <italic>W</italic> (100, 8, 0.01) is given. The pattern formation is chaotic (<xref ref-type="fig" rid="F2">Figure 2A</xref>) when the strength <italic>d</italic> &#x3d; 0.01 is weak, which means the nervous system does not work. The pattern formation starts to become clear and tends to sync with the increase of <italic>d</italic>
<sub>1</sub> (<xref ref-type="fig" rid="F2">Figure 2</xref>b,c). Ultimately, the pattern formation becomes synchronized; namely, all the neurons become completely phase synchronized (<xref ref-type="fig" rid="F2">Figure 2D</xref>). The short-term memory needs to be clarified when <italic>d</italic>
<sub>1</sub> is weak. Only when all the neurons work perfectly together is a clear short-term memory formed (<xref ref-type="fig" rid="F2">Figure 2</xref>), which is also the mechanism by which adequate short-term memory is produced.</p>
<fig id="F2" position="float">
<label>FIGURE 2</label>
<caption>
<p>Pattern formation when <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 4 and <italic>W</italic> (100, &#x7c; 8, &#x7c; 0.01). <bold>(A)</bold> Pattern formation when <italic>d</italic>
<sub>1</sub> &#x7c; &#x3d; &#x7c; 0.01. <bold>(B)</bold> Pattern formation when <italic>d</italic>
<sub>1</sub> &#x7c; &#x3d; &#x7c; 0.05. <bold>(C)</bold> Pattern formation when <italic>d</italic>
<sub>1</sub> &#x7c; &#x3d; &#x7c; 0.3. <bold>(D)</bold> Pattern formation when <italic>d</italic>
<sub>1</sub> &#x7c; &#x3d; &#x7c; 1.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g002.tif"/>
</fig>
<p>Then, the number of cooperative neurons will be considered to generate short-term memory. The links between neurons can be treated as the number of collaborative neurons in our analysis, which could be measured by <italic>K</italic>. When <italic>K</italic> is small, the pattern formation is chaotic, and every neuron is relatively independent (<xref ref-type="fig" rid="F3">Figure 3A</xref>). This condition is not suitable for the generation of short-term memory. When <italic>K</italic> &#x3d; 2, the pattern formation shows some neurons are in sync (<xref ref-type="fig" rid="F3">Figure 3B</xref>); namely, multiple short-term memories are produced simultaneously. In this case, short-term memory is often fuzzy. The short-term memory gradually becomes clear when <italic>K</italic> becomes large (<xref ref-type="fig" rid="F3">Figure 3C</xref>). Eventually, multiple neurons work together to form a clear short-term memory when all the neurons are in sync (<xref ref-type="fig" rid="F3">Figure 3D</xref>).</p>
<fig id="F3" position="float">
<label>FIGURE 3</label>
<caption>
<p>Pattern formation when <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 4, <italic>d</italic>
<sub>1</sub> &#x7c; &#x3d; &#x7c; 1 and <italic>W</italic> (100, <italic>K</italic>, &#x7c; 0.01). <bold>(A)</bold> Pattern formation when <italic>K</italic> &#x3d; &#x7c; 0. <bold>(B)</bold> Pattern formation when <italic>K</italic> &#x3d; &#x7c; 2. <bold>(C)</bold> Pattern formation when <italic>K</italic> &#x3d; &#x7c; 4. <bold>(D)</bold> Pattern formation when <italic>K</italic> &#x3d; &#x7c; 6.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g003.tif"/>
</fig>
<p>Finally, it is found that the link probability does not work because <italic>p</italic> cannot change the number of cooperative neurons and the coupling strength.</p>
<sec id="s3-1">
<title>3.1 Hamiltonian energy with external stimulus</title>
<p>System (3) can be written as<disp-formula id="e4">
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<label>(4)</label>
</disp-formula>
</p>
<p>where <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; <italic>d</italic>
<sub>1</sub>
<italic>k</italic>
<sub>
<italic>i</italic>
</sub> (<italic>d</italic>
<sub>1</sub> &#x3d; 0.01), and the effect of <italic>x</italic>
<sub>0</sub> is similar to <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> is a constant. <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> and the coupling strength play a vital role in the electrical activity, which is the basis of the generation of fire. Therefore, we consider the role of <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> and <italic>D</italic>
<sub>
<italic>i</italic>
</sub> in the Hamiltonian energy, change in Hamiltonian energy, and membrane potential when <italic>x</italic>
<sub>0</sub> &#x3d; 1.</p>
<p>It is well known that the coupling between neurons is necessary for generating fire or short-term memory (<xref ref-type="fig" rid="F2">Figure 2</xref>). Because only the <italic>ith</italic> neuron evolutes with system (4), and other neurons are fixed at (<italic>x</italic>
<sub>0</sub>, <italic>y</italic>
<sub>0</sub>, <italic>z</italic>
<sub>0</sub>), <italic>D</italic>
<sub>
<italic>i</italic>
</sub> can also be regarded as the size of the network degree. When the coupling strength is small, or the number of links is few, no spike or memory is generated; namely, the neurons are resting (<xref ref-type="fig" rid="F4">Figure 4A</xref>). The membrane potential began to change periodically with the increase in <italic>D</italic>
<sub>
<italic>i</italic>
</sub>, which means the emergence and disappearance of short-term memory (<xref ref-type="fig" rid="F4">Figure 4B</xref>). Meanwhile, the Hamiltonian energy and change in Hamiltonian energy change with the membrane potential, which means the generation of the short-term memory takes more energy. However, short-term memory is the result of multiple neurons working together. If one neuron is very tightly connected to other neurons, all the neurons will tend to be in one state because other neurons are fixed at (<italic>x</italic>
<sub>0</sub>, <italic>y</italic>
<sub>0</sub>, <italic>z</italic>
<sub>0</sub>). Namely, system (4) of a neuron will tend to a stable state when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> is larger (<xref ref-type="fig" rid="F4">Figure 4C</xref>).</p>
<fig id="F4" position="float">
<label>FIGURE 4</label>
<caption>
<p>Hamiltonian energy, change in Hamiltonian energy, and membrane potential when <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 1, <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 1. <bold>(A)</bold> Evolution when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 0.1. <bold>(B)</bold> Evolution when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 1. <bold>(C)</bold> Evolution when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 1.5.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g004.tif"/>
</fig>
<p>Next, we show the continuous changes in <italic>x</italic>, <italic>H</italic>
<sub>1</sub>, <italic>H</italic>
<sub>2</sub> with <italic>D</italic>
<sub>
<italic>i</italic>
</sub> (<xref ref-type="fig" rid="F5">Figure 5</xref>). From <xref ref-type="fig" rid="F5">Figure 5A</xref>, the bifurcation occurs with the increase in <italic>D</italic>
<sub>
<italic>i</italic>
</sub>. The average Hamiltonian energy decreases gradually at the beginning because the utilization of energy is relatively low when the neuron is in a resting state (<xref ref-type="fig" rid="F5">Figure 5B</xref>). When the membrane potential is periodic, the average Hamiltonian energy will be a sudden increase (<xref ref-type="fig" rid="F5">Figure 5B</xref>). Meanwhile, the rise of coupling strength also reduces the consumption of Hamiltonian energy, which is why the average Hamiltonian energy decreases with <italic>D</italic>
<sub>
<italic>i</italic>
</sub> (<xref ref-type="fig" rid="F5">Figure 5B</xref>). It is found that the max&#x2013;min value of Hamiltonian energy (<xref ref-type="fig" rid="F5">Figure 5C</xref>) and its variation (<xref ref-type="fig" rid="F5">Figure 5D</xref>) is significantly associated with the bifurcation, which is essential to show the relationship between the consumption of energy and the membrane potential (the generation of short-term memory). In a word, generating short-term memory will take a lot of energy, and the coupling strength could further reduce energy consumption.</p>
<fig id="F5" position="float">
<label>FIGURE 5</label>
<caption>
<p>Average Hamiltonian energy, average change in Hamiltonian energy, and membrane potential when <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 1. <bold>(A)</bold> Bifurcation of membrane potential. <bold>(B)</bold> Average Hamiltonian energy. <bold>(C)</bold> Max&#x2013;min value of Hamiltonian energy. <bold>(D)</bold> Max&#x2013;min value of Hamiltonian energy variation.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g005.tif"/>
</fig>
<p>The role of <italic>x</italic>
<sub>0</sub> from other neurons&#x2019; external stimulus (<xref ref-type="bibr" rid="B15">Li et al., 2024b</xref>; <xref ref-type="bibr" rid="B14">Li et al., 2024a</xref>; <xref ref-type="bibr" rid="B6">Du et al., 2024)</xref> is the same as <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> when other parameters are fixed. When the external stimulation of other neurons contributing to the <italic>ith</italic> neuron is weak, system (4) (the Hamiltonian energy, change in Hamiltonian energy, and membrane potential) is stable (<xref ref-type="fig" rid="F4">Figure 4A</xref>). The periodical spike occurs (<xref ref-type="fig" rid="F6">Figure 6A</xref>) in the membrane potential when <italic>x</italic>
<sub>0</sub> increases, which corresponds to the emergence and disappearance of short-term memory. It is found that energy consumption is relatively large in preparation for the spike, and the energy varies significantly in the spike (<xref ref-type="fig" rid="F6">Figure 6A</xref>), which can be treated as an indicator of the generation of the spike (short-term memory). The frequency of spikes will increase (<xref ref-type="fig" rid="F6">Figure 6B</xref>) when external stimuli are enhanced. However, it is insufficient to support two identical spikes of membrane potential <italic>x</italic> (<xref ref-type="fig" rid="F6">Figure 6B</xref>) due to the lack of external stimulus or the Hamiltonian energy <italic>H</italic> (<xref ref-type="fig" rid="F6">Figure 6B</xref>). Therefore, the formation of short-term memory requires a process of accumulating energy, and the energy breaks out when a spike occurs. The more energy accumulates, the greater the energy change (<italic>H</italic>
<sub>
<italic>t</italic>
</sub>). If <italic>x</italic>
<sub>0</sub> continues to increase, there will be more spikes, but their intensity is different (<xref ref-type="fig" rid="F6">Figure 6C</xref>). A constant spike is created when <italic>x</italic>
<sub>0</sub> is very large (<xref ref-type="fig" rid="F6">Figure 6D</xref>), which is also the ordinary emergence and disappearance of short-term memory. However, the external stimulus from other neurons will inhibit the generation of the spike and put the <italic>ith</italic> neuron in a resting state (<xref ref-type="fig" rid="F7">Figure 7A</xref>). From <xref ref-type="fig" rid="F7">Figure 7</xref>, the spike is impossible without extensive external energy input, and it has excellent fluctuations at the beginning (<xref ref-type="fig" rid="F7">Figure 7A</xref>). We find the average Hamiltonian energy increases with <italic>x</italic>
<sub>0</sub> (<xref ref-type="fig" rid="F7">Figure 7B</xref>). The max&#x2013;min value of Hamiltonian energy (<xref ref-type="fig" rid="F7">Figure 7C</xref>) and the max&#x2013;min value of Hamiltonian energy variation (<xref ref-type="fig" rid="F7">Figure 7D</xref>) are consistent with the bifurcation of <italic>x</italic>.</p>
<fig id="F6" position="float">
<label>FIGURE 6</label>
<caption>
<p>Hamiltonian energy, change in Hamiltonian energy, and membrane potential when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 0.1, <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 1. <bold>(A)</bold> Evolution when <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 5. <bold>(B)</bold> Evolution when <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 10. <bold>(C)</bold> Evolution when <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 20. <bold>(D)</bold> Evolution when <italic>x</italic>
<sub>0</sub> &#x7c; &#x3d; &#x7c; 200.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g006.tif"/>
</fig>
<fig id="F7" position="float">
<label>FIGURE 7</label>
<caption>
<p>Average Hamiltonian energy, change in Hamiltonian energy, and membrane potential when <italic>D</italic>
<sub>
<italic>i</italic>
</sub> &#x3d; &#x7c; 1, <italic>I</italic>
<sub>
<italic>ext</italic>
</sub> &#x3d; &#x7c; 1. <bold>(A)</bold> Bifurcation of membrane potential. <bold>(B)</bold> Average Hamiltonian energy. <bold>(C)</bold> Max&#x2013;min value of Hamiltonian energy. <bold>(D)</bold> Max&#x2013;min value of Hamiltonian energy variation.</p>
</caption>
<graphic xlink:href="fnetp-04-1362778-g007.tif"/>
</fig>
<p>Finally, we conclude the dynamical mechanism of the generation of short-term memory: the energy from other neurons is necessary for short-term memory, proving that short-term memory results from multiple neuronal activities. Energy requires a process of accumulation to maintain a complete spike. The excessive influence of other neurons can make the <italic>ith</italic> neurons lose their dominance and align with the dynamic behaviors of other neurons.</p>
</sec>
</sec>
<sec sec-type="conclusion" id="s4">
<title>4 Conclusion</title>
<p>Energy plays a vital role in neuronal activity, which is the basis of the generation of short-term memory. In this paper, the pattern formation could represent the collecting dynamics of short-term memory through the Hamiltonian energy, showing the neuronal activity in generating short-term memory. Therefore, the interplay between neurons is considered through a simple network to show the effect of the external stimulus and coupling strength (degree) on the dynamical behaviors. It is found that the Hamiltonian energy, change in the Hamiltonian energy, and membrane potential are consistent. The excessive influence of other neurons can make the <italic>ith</italic> neurons lose their dominance and align with the dynamic behaviors of other neurons, which could show the synergistic effect of neurons through a physical neuron circuit. In addition, the energy from other neurons is necessary for short-term memory, proving that short-term memory results from multiple neuronal activities. Generating short-term memory requires much energy, and energy requires a process of accumulation to maintain a complete spike. Meanwhile, the coupling strength could further reduce energy consumption, which provides a novel way to reduce the energy consumption in information storage and processing. However, more short-term memory descriptions should be completed next.</p>
</sec>
</body>
<back>
<sec sec-type="data-availability" id="s5">
<title>Data availability statement</title>
<p>The original contributions presented in the study are included in the article/Supplementary Material; further inquiries can be directed to the corresponding authors.</p>
</sec>
<sec id="s6">
<title>Author contributions</title>
<p>QZ: writing&#x2013;original draft and writing&#x2013;review and editing. YX: writing&#x2013;original draft and writing&#x2013;review and editing. JS: writing&#x2013;original draft and writing&#x2013;review and editing.</p>
</sec>
<sec sec-type="funding-information" id="s7">
<title>Funding</title>
<p>The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by the National Natural Science Foundation of China (12002297 and 12272135), Basic Research Project of Universities in Henan Province (21zx009), Program for Science &#x26; Technology Innovation Talents in Universities of Henan Province (22HASTIT018), Funding of Henan Province for merit-based overseas students (2023), Outstanding Young Backbone Teacher of Xuchang University (2022), and Training Program for Young Key Teachers in Colleges and Universities of Henan Province (2023GGJS144). Natural Science Foundation of Henan (242300421396).</p>
</sec>
<sec sec-type="COI-statement" id="s8">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
<p>The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.</p>
</sec>
<sec sec-type="disclaimer" id="s9">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors, and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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