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Impaired spatial memory in adult vitamin D deficient BALB/c mice is associated with reductions in spine density, nitric oxide, and neural nitric oxide synthase in the hippocampus

  • Received: 24 November 2021 Revised: 11 January 2022 Accepted: 20 January 2022 Published: 26 January 2022
  • Vitamin D deficiency is prevalent in adults and is associated with cognitive impairment. However, the mechanism by which adult vitamin D (AVD) deficiency affects cognitive function remains unclear. We examined spatial memory impairment in AVD-deficient BALB/c mice and its underlying mechanism by measuring spine density, long term potentiation (LTP), nitric oxide (NO), neuronal nitric oxide synthase (nNOS), and endothelial NOS (eNOS) in the hippocampus. Adult male BALB/c mice were fed a control or vitamin D deficient diet for 20 weeks. Spatial memory performance was measured using an active place avoidance (APA) task, where AVD-deficient mice had reduced latency entering the shock zone compared to controls. We characterised hippocampal spine morphology in the CA1 and dentate gyrus (DG) and made electrophysiological recordings in the hippocampus of behaviourally naïve mice to measure LTP. We next measured NO, as well as glutathione, lipid peroxidation and oxidation of protein products and quantified hippocampal immunoreactivity for nNOS and eNOS. Spine morphology analysis revealed a significant reduction in the number of mushroom spines in the CA1 dendrites but not in the DG. There was no effect of diet on LTP. However, hippocampal NO levels were depleted whereas other oxidation markers were unaltered by AVD deficiency. We also showed a reduced nNOS, but not eNOS, immunoreactivity. Finally, vitamin D supplementation for 10 weeks to AVD-deficient mice restored nNOS immunoreactivity to that seen in in control mice. Our results suggest that lower levels of NO and reduced nNOS immunostaining contribute to hippocampal-dependent spatial learning deficits in AVD-deficient mice.

    Citation: Md. Mamun Al-Amin, Robert K. P. Sullivan, Suzy Alexander, David A. Carter, DanaKai Bradford, Thomas H. J. Burne. Impaired spatial memory in adult vitamin D deficient BALB/c mice is associated with reductions in spine density, nitric oxide, and neural nitric oxide synthase in the hippocampus[J]. AIMS Neuroscience, 2022, 9(1): 31-56. doi: 10.3934/Neuroscience.2022004

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  • Vitamin D deficiency is prevalent in adults and is associated with cognitive impairment. However, the mechanism by which adult vitamin D (AVD) deficiency affects cognitive function remains unclear. We examined spatial memory impairment in AVD-deficient BALB/c mice and its underlying mechanism by measuring spine density, long term potentiation (LTP), nitric oxide (NO), neuronal nitric oxide synthase (nNOS), and endothelial NOS (eNOS) in the hippocampus. Adult male BALB/c mice were fed a control or vitamin D deficient diet for 20 weeks. Spatial memory performance was measured using an active place avoidance (APA) task, where AVD-deficient mice had reduced latency entering the shock zone compared to controls. We characterised hippocampal spine morphology in the CA1 and dentate gyrus (DG) and made electrophysiological recordings in the hippocampus of behaviourally naïve mice to measure LTP. We next measured NO, as well as glutathione, lipid peroxidation and oxidation of protein products and quantified hippocampal immunoreactivity for nNOS and eNOS. Spine morphology analysis revealed a significant reduction in the number of mushroom spines in the CA1 dendrites but not in the DG. There was no effect of diet on LTP. However, hippocampal NO levels were depleted whereas other oxidation markers were unaltered by AVD deficiency. We also showed a reduced nNOS, but not eNOS, immunoreactivity. Finally, vitamin D supplementation for 10 weeks to AVD-deficient mice restored nNOS immunoreactivity to that seen in in control mice. Our results suggest that lower levels of NO and reduced nNOS immunostaining contribute to hippocampal-dependent spatial learning deficits in AVD-deficient mice.



    In a diverse world, the dynamics of neural networks has been studied extensively due to their convergence and stability are important in real applications, such as pattern recognition, image and signal processing, associative memories and so on [1,2,3]. A lot of literatures have been reported for different types of neural networks based on their various topological structures. To name a few, Cohen-Grossberg neural networks [4], bi-directonal associative memory (BAM) neural networks [5], Hopfield-type neural networks [6] and cellular neural networks [7].

    Among them, Cohen-Grossberg neural networks were originally introduced by Cohen and Grossberg in 1983, which can be reduced to Hopfield-type neural networks and cellular neural networks as well in [4]. And the dynamics of such neural networks have received increasing interest, such as stability, synchronization and stabilization [8,9,10,11,12]. In order to make a detailed description between different layers of networks, BAM neural networks have been proposed by Kosko in 1988, and many methods and techniques were developed to discuss the dynamical characteristics of BAM neural networks in [13,14,15,16]. Recently, a class of Cohen-Grossberg-type BAM neural networks have drawn significant attention owing to the wide application in practice [17,18,19,20].

    In fact, time delays occur in neural networks due to the finite speed of signal propagation. Generally, time delays can be divided into several types, such as discrete-type delays [21], distributed-type delays [22] and neutral-type delays [23]. As we all know, it is difficult to verify the dynamics of neutral delayed neural networks since they contain important information about the derivative of the past state. Some authors focused on neutral neural networks and several results have been obtained. For example, Cheng et al. [24] discussed neutral Cohen-Grossberg neural networks by means of Lyapunov stability method. Liu and Zong [25] dealt with a kind of neutral BAM neural networks based on some new integral inequalities and the Lyapunov-Krasovskii functional approach.

    On the other hand, many real-world systems often receive sudden external disturbance, which entail systems undergo abrupt changes in very short time. This phenomenon is viewed as impulse [26,27,28]. The existence of impulse is also one of the key factors leading to the instability of neural networks. Recently impulsive neural networks have aroused a lot of interest [29,30,31]. Gu et al. [32] established the existence and global exponential stability of BAM-type impulsive neural networks with time-varying delays. They mainly used the method of the continuation theorem of coincidence degree theory and Lyapunov functional analysis. Liao et al. [33] gave the results of global asymptotic stability of periodic solutions for inertial delayed BAM neural networks by combining Mawhin continuation theorem of coincidence degree theory, Lyapunov functional method and inequality techniques. Especially, they seek periodic solutions by means of Lyapunov functional method instead of the prior estimate method. The addition of delays and impulses in neural networks make it more accurate to describe the evolutionary process of the systems.

    To the best of our knowledge, Cohen-Grossberg-type BAM neural networks with neutral delays and impulses have not been investigated. The aim of this paper is to establish the existence and asymptotic stability of periodic solutions.

    To study the dynamics of neural networks, many methods and techniques are developed, such as the matrix theory, set-valued maps theory and functional differential inclusions. Our results are based on the famous Mawhin coincidence degree theory and Lyapunov functional analysis. To do this, our highlights lie in four aspects:

    Proposing a new model with neutral-type time delays and impulses, some previous considered neural network models can be regarded as the special cases of ours, such as [15,20,32].

    Establishing some sufficient conditions to guarantee the existence and asymptotic stability of the periodic solutions by means of Mawhin coincidence degree theory and the contraction of a suitable Lyapunov functional. We not only employ the method of the prior classical estimation in Section 3, but also seek periodic solutions by means of Lyapunov functional method in Appendix.

    The impulse terms in this paper are more relaxing from linear functions as well in [16].

    The theoretical findings play a key role in designing the electric implementation of Cohen-Grossberg-type BAM neural networks and processing its signals transmission.

    This paper is organized as follows. In Section 2, the model description and necessary knowledge are provided. In Section 3, by using the continuation theorem of coincidence degree theory, some conditions for the existence of periodic solutions are obtained. In Section 4, the global asymptotic stability of periodic solutions is discussed. In Section 5, an illustrative example is given to show the effectiveness of our criterions.

    Consider the following Cohen-Grossberg-type BAM neural networks with neutral-type time delays and impulses, i.e.,

    {˙xi(t)=ai(xi(t))[bi(xi(t))mj=1aij(t)fj(yj(tτij(t)))mj=1bij(t)fj(˙yj(t˜τij(t)))Ii(t)],t>0,ttk,Δxi(tk)=xi(t+k)xi(tk)=Iik(xi(tk)),i=1,2,,n,k=1,2,,˙yj(t)=cj(yj(t))[dj(yj(t))ni=1cji(t)gi(xi(tσji(t)))ni=1dji(t)gi(˙xi(t˜σji(t)))Jj(t)],t>0,ttk,Δyj(tk)=yj(t+k)yj(tk)=Jjk(yj(tk)),j=1,2,,m,k=1,2,. (2.1)

    The initial conditions associated with (2.1) are of the form

    {xi(t)=φi(t),t(τ,0],τ=max1in,1jm{τij},i=1,2,,n,yj(t)=ψj(t),t(σ,0],σ=max1in,1jm{σji},j=1,2,,m, (2.2)

    where

    τij=max0tω{τij(t),˜τij(t)}, and σji=max0tω{σji(t),˜σji(t)}.

    Obviously Δxi(tk) and Δyj(tk) are the impulses at moments tk and t1<t2< is a strictly increasing sequence such that limk+tk=+.

    The ecological meaning of parameters are as follows. Among the system (2.1), xi(t), yj(t) represent the potential (or voltage) of cell i, j at time t respectively; n, m correspond to the number of neurons in the Xlayer and Ylayer; ai(), cj() denote amplification functions; bi(), dj() mean appropriately behaved functions such that the solutions of system (2.1) remain bounded; aij(t), bij(t), cji(t), dji(t) describe the connection strengths of connectivity between cell i and j at the time t; fj(), gi() are the activation functions; Ii(t), Jj(t) show the external inputs at time t.

    In order to establish the existence of periodic solutions of systems (2.1) and (2.2), we assume the following hypotheses:

    (H1) τij(t), ˜τij(t), σji(t), ˜σji(t), aij(t), bij(t), cji(t), dji(t) are continuous ωperiodic functions and

    aMij=max0tωaij(t),bMij=max0tωbij(t),cMji=max0tωcji(t),dMji=max0tωdji(t).

    (H2) fj(x), gi(y) are bounded and globally Lipschitz continuous, i.e., there exist positive constants Fj, Gi, ˜Fj, ˜Gi, such that

    |fj(x)fj(y)|Fj|xy|,|fj(x)|˜Fj,j=1,2,,m,
    |gi(x)gi(y)|Gi|xy|,|gi(y)|˜Gi,i=1,2,,n.

    It is easy to see that

    |fj(x)|Fj|x|+|fj(0)|,|gi(x)|Gi|x|+|gi(0)|,fory=0.

    (H3) ai(u), bi(u), cj(u), dj(u)C(R,R), and there exist positive constants aLi, aMi, cLj, cMj, bLi, bMi, dLj, dMj, such that

    0<aLiai(u)aMi,0<bLi|u|bi(u)bMi|u|,i=1,2,,n,
    0<cLjcj(u)cMj,0<dLj|u|dj(u)dMj|u|,j=1,2,,m.

    (H4) for all x,yR, there exists a positive integer p such that

    tk+p=tk+ω,Ii(k+p)(x)=Iik(x),Jj(k+p)(y)=Jjp(y).

    (H5) Iik() and Jjk() are bounded and Lipschitz continuous functions, that is, there exist constants si, rj, sik and rjk such that

    |Iik(x)Iik(y)|sik|xy|,|Iik()|<si,i=1,2,,n,
    |Jjk(x)Jjk(y)|rjk|xy|,|Jjk()|<rj,j=1,2,,m.

    It is easy to see that

    |Iik(x)|sik|x|+|Iik(0)|,|Jjk(x)|rjk|x|+|Jjk(0)|,fory=0.

    Before presenting our results on the existence and stability of periodic solutions of systems (2.1) and (2.2), we briefly introduce the Mawhin coincidence degree theorem [34].

    Let X and Y be two Banach spaces, L:DomLXY be a linear mapping and N:XY be a continuous mapping. The mapping L is called a Fredholm mapping of index zero if dimKerL=codimImL<+ and ImL is closed in Y. If L is a Fredholm mapping of index zero, there exist continuous projectors P:XX and Q:YY such that ImP=KerL, KerQ=ImL=Im(IQ), then the restriction Lp of L to DomLKerP is invertible. We denote the inverse of that mapping by Kp. If Ω is an open bounded subset of X, the mapping N is said to be Lcompact on ˉΩ if QN(ˉΩ) is bounded and Kp(IQ)N:ˉΩX is compact. Since ImQ is isomorphic to KerL, there exists an isomorphism J:ImQKerL.

    Lemma 1. Let X and Y be two Banach spaces, L:DomLXY be a Fredholm mapping with index zero, ΩX be an open bounded set and N:ˉΩY be Lcompact on ˉΩ. Assume that:

    (a) for each λ(0,1) and xΩDomL, LxλNx,

    (b) for each xΩKerL, QNx0,

    (c) deg{JQN,ΩKerL,0}0. Then equation Lx=λNx has at least one solution in ˉΩDomL.

    In this section, we study the existence of periodic solutions of systems (2.1) and (2.2) based on Mawhin coincidence degree theorem.

    Let

    z(t)=(xT(t),yT(t))T=(x1(t),,xn(t),y1(t),,ym(t))T,

    obviously if z(t) is a solution of systems (2.1) and (2.2) defined on [0,ω] such that z(0)=z(t), then according to the periodicity of systems (2.1) and (2.2) in t, the function z(t) defined by

    z(t)=z(tkω),t[lω,(l+1)ω]{tk},k=1,2,, l=1,2.

    in which z(t) is left continuous at t=tk. Thus z(t) is an ωperiodic solution of systems (2.1) and (2.2).

    For any non-negative integer q, let Cq[0,ω:t1,,tp]={z:[0,ω]Rn+mz(q)(t) exists for tt1,,tp;z(q)(t+) and z(q)(t)exists at t1,,tp and z(j)(tk)=z(j)(tk),k=1,,p, j=1,,q}.

    In order to establish the existence of ωperiodic solutions of systems (2.1) and (2.2), we take

    X={zC[0,ω:t1,,tp]|z(t)=z(t+ω)},Y=X×R(n+m)×(p+1),

    and

    z=n+mi=1max0tω|zi(t)|=ni=1max0tω|xi(t)|+mj=1max0tω|yj(t)|,

    then X and Y are both Banach space.

    Set

    L:DomLXY,z(˙z(t),Δz(t1),Δz(t2),,Δz(tp),0), (3.1)

    where DomL={zC1[0,ω:t1,,tp],z(t)=z(t+ω)}.

    From N:XY, we have

    Nz=((A1(t)An(t)B1(t)Bm(t)),(Δx1(t1)Δxn(t1)Δy1(t1)Δym(t1)),(Δx1(t2)Δxn(t2)Δy1(t2)Δym(t2)),,(Δx1(tp)Δxn(tp)Δy1(tp)Δym(tp)),(0000),), (3.2)

    where

    Ai(t)=ai(xi(t))[bi(xi(t))mj=1aij(t)fj(yj(tτij(t)))mj=1bij(t)fj(˙yj(t˜τij(t)))Ii(t)],

    and

    Bj(t)=cj(yj(t))[dj(yj(t))ni=1cji(t)gi(xi(tσji(t)))ni=1dji(t)gi(˙xi(t˜σji(t)))Jj(t)].

    Obviously,

    KerL=Rn+m,

    and

    ImL={(h,C1,C2,,Cp,d)Y:ω0h(s)ds+pk=1Ck+d=0}=X×R(n+m)×p×{0},

    thus

    dimKerL=codimImL=n+m.

    It is easy to show that ImL is closed in Y and L is a Fredholm mapping of index zero.

    Lemma 2. Let L and N are two mappings defined by (3.1) and (3.2), then N is Lcompact on ˉΩ for any open bounded set ΩX..

    Proof. Define two projectors:

    Pz=1ωω0z(t)dt,

    and

    Qz=Q(h,C1,C2,,Cp,d)=(1ω[ω0h(s)ds+pk=1Ck+d],0,,0,0).

    It is obvious that P and Q are continuous and satisfy

    ImP=KerL and ImL=KerQ=Im(IQ).

    Furthermore, the generalized inverse Kp=L1p is given by

    Kpz=t0h(s)ds+t>tkCk1ωω0t0h(s)dsdtpk=1Ck.

    Then the expression of QNz is

    QNz=((1ωω0Ai(s)ds+1ωpk=1Iik(xi(tk)))n×1(1ωω0Bj(s)ds+1ωpk=1Jjk(yj(tk)))m×1,0,,0,0),

    and

    Kp(IQ)Nz=((t0Ai(s)ds+t>tkIik(xi(tk)))n×1(t0Bj(s)ds+t>tkJjk(yj(tk)))m×1)((1ωω0t0Ai(s)dsdt+(tω12)ω0Ai(s)ds)n×1(1ωω0t0Bj(s)dsdt+(tω12)ω0Bj(s)ds)m×1)((pk=1Iik(xi(tk)))n×1(pk=1Jjk(yj(tk)))m×1).

    Thus QN and Kp(IQ)N are both continuous.

    Consider the sequence {Kp(IQ)N}, for any open bounded set ΩX and any zΩ, we have

    Kp(IQ)Nz=max0tωni=1|t0Ai(s)ds+t>tkIik(xi(tk))1ωω0t0Ai(s)dsdt(tω12)ω0Ai(s)dspk=1Iik(xi(tk))|+max0tωmj=1|t0Bj(s)ds+t>tkJjk(yj(tk))1ωω0t0Bj(s)dsdt(tω12)ω0Bj(s)dspk=1Jjk(yj(tk))|ni=152ω0|Ai(s)|ds+2psi+mj=152ω0|Bj(s)|ds+2prj,

    then Kp(IQ)N is uniformly bounded on Ω. For any z,˜zΩ, we have

    Kp(IQ)NzKp(IQ)N˜z=max0tωni=1|t>tk(Iik(xi(tk))Iik(˜xi(tk)))pk=1(Iik(xi(tk))Iik(˜xi(tk)))|+max0tωmj=1|t>tk(Jjk(yj(tk))Jjk(˜yj(tk)))pk=1(Jjk(yj(tk))Jjk(˜yj(tk)))|ni=1pk=1|(Iik(xi(tk))Iik(˜xi(tk)))|+mj=1pk=1|(Jjk(yj(tk))Jjk(˜yj(tk)))|ni=1pk=1sik|xi(tk)˜xi(tk)|+mi=1pk=1rjk|yj(tk)˜yj(tk)|,

    then Kp(IQ)N is equicontinuous on Ω. By virtue of the Arzela-Ascoli Theorem, Kp(IQ)N(Ω) is a sequentially compact set. Therefore, Kp(IQ)N(ˉΩ) is compact. Moreover, QN(ˉΩ) is bounded. Thus, N is Lcompact on ˉΩ for any open bounded set ΩX.

    Now, we need to show that there exists a domain Ω that satisfies all the requirements given in Lemma 1.

    Theorem 1. Assume that (H1)-(H5) hold, systems (2.1) and (2.2) have at least one ωperiodic solution.

    Proof. Corresponding to the operator equation Lz=λNz, λ(0,1), we have

    {˙xi(t)=λai(xi(t))[bi(xi(t))mj=1aij(t)fj(yj(tτij(t)))mj=1bij(t)fj(˙yj(t˜τij(t)))Ii(t)],t>0,ttk,Δxi(tk)=xi(t+k)xi(tk)=λIik(xi(tk)),i=1,2,,n,k=1,2,,˙yj(t)=λcj(yj(t))[dj(yj(t))ni=1cji(t)gi(xi(tσji(t)))ni=1dji(t)gi(˙xi(t˜σji(t)))Jj(t)],t>0,ttk,Δyj(tk)=yj(t+k)yj(tk)=λJjk(yj(tk)),j=1,2,,m,k=1,2,. (3.3)

    Suppose that (x1(t),,xn(t),y1(t),,ym(t))TX is a solution of system (3.3) for some λ(0,1). Integrating system (3.3) over the interval [0,ω], we obtain

    {ω0{ai(xi(s))[bi(xi(s))mj=1aij(t)fj(yj(sτij(s)))mj=1bij(t)fj(˙yj(s˜τij(s)))Ii(s)]}ds+pk=1Iik(xi(tk))=0,ω0{cj(yj(s))[dj(yj(s))ni=1cji(t)gi(xi(sσji(s)))ni=1dji(t)gi(˙xi(s˜σji(s)))Jj(s)]}ds+pk=1Jjk(yj(tk))=0. (3.4)

    Let ξ, η[0,ω], and

    xi(ξ)=inf0tωxi(t), i=1,2,,n;yj(η)=inf0tωyj(t), j=1,2,,m.

    From (3.4), we have

    xi(ξ)aLibLiωω0ai(xi(s))bi(xi(s))ds=ω0{ai(xi(s))[mj=1aij(t)fj(yj(sτij(s)))mj=1bij(t)fj(˙yj(s˜τij(s)))Ii(s)]}ds+pk=1Iikxi(tk)ω0|ai(xi(s))[mj=1aij(t)fj(yj(sτij(s)))mj=1bij(t)fj(˙yj(s˜τij(s)))Ii(s)]|ds+|pk=1Iikxi(tk)|aMiωmj=1(aMij+bMij)˜Fj+pk=1Iikxi(tk),

    that is,

    xi(ξ)aMiωmj=1(aMij+bMij)˜Fj+pk=1Iikxi(tk)aLibLiω:=T1i.

    Similarly we obtain

    yj(η)cMjωni=1(cMji+dMji)˜Gi+pk=1Jjkyj(tk)cLjdLjω:=T2j.

    Again set ξ+, η+[0,ω], and

    xi(ξ+)=sup0tωxi(t), i=1,2,,n;yj(η+)=sup0tωyj(t), j=1,2,,m,

    obviously

    xi(ξ+)aMiωmj=1(aMij+bMij)˜Fj+pk=1Iikxi(tk)aMibMiω:=T+1i.
    yj(η+)cMjωni=1(cMji+dMji)˜Gi+pk=1Jjkyj(tk)cMjdMjω:=T+2j.

    Denote Hi=max0tω|zi(t)|<max{|T+1i|,|T1i|}, and

    H=n+mi=1Hi+E,

    where E is a sufficiently large positive constant. It is obvious that H is independent of λ. Let

    Ω={z(t)=(xT(t),yT(t))TX:z(t)<H, z(t+k)Ω, k=1,2,p}.

    where x(t)=(x1(t),,xn(t))T, y(t)=(y1(t),,ym(t))T.

    Next we check the three conditions in Lemma 1.

    (a) For each λ(0,1), z(t)ΩDomL with the norm z(t)=H, we have LzλNz.

    (b) For any zΩRn+m, z is a constant vector in Rn+m, z=H, then QNz0.

    (c) Let J:ImQKerL, then

    JQNz=QNz=((1ωω0Ai(s)ds+1ωpk=1Iik(xi(tk)))n×1(1ωω0Bj(s)ds+1ωpk=1Jjk(yj(tk)))m×1,0,,0,0).

    Define Ψ:KerL×[0,1]X by

    Ψ(z,μ)=μz+(1μ)QNz.

    It is easy to verify Ψ(z,μ)(0,0,,0) for any zΩKerL.

    Therefore

    deg{JQN,ΩkerL,(0,0,...,0)}=°{QNz,ΩkerL,(0,0,...,0)}=°{z,ΩkerL,(0,0,...,0)}0.

    All the conditions in Lemma 1 have been verified. We conclude that Lz=Nz has at least one ωperiodic solution. This implies that systems (2.1) and (2.2) have at least one ωperiodic solution.

    Remark 1. The method of the estimation for Ω is classical and effective. In fact, a new study method is cited in [33], utilizing Lyapunov method to study periodic solutions for neural networks. Hence, we also established Lemma 3 and gave a detailed proof in Appendix.

    In this section, we will construct a new Lyapunov functional to study the global asymptotic stability of periodic solutions of systems (2.1) and (2.2).

    Theorem 2. Assume that (H1)–(H5) hold, and

    (H6) ai(u) and cj(u) are globally Lipschitz continuous, that is, for any (u,v)R, there exist constants hai and hcj such that

    |ai(u)ai(v)|hai|uv|,i=1,2,,n,
    |cj(u)cj(v)|hcj|uv|,j=1,2,,m.

    (H7) for all i, j (i=1,2,,n,j=1,2,,m), there exist constants Labi and Lcdj such that

    |ai(u)bi(u)ai(v)bi(v)|Labi|uv|,|cj(u)dj(u)cj(v)dj(v)|Lcdj|uv|,(u,v)R.

    (H8) there exist positive constants θi, θn+j and γ(0,min(Λ1i,Λ2j)) such that

    θi(Λ1iγ)+mj=1θn+jcMjcMjiGi1σMjieγσMji<0,

    and

    θn+j(Λ2jγ)+ni=1θiaMiaMijFj1τMijeγτMij<0,

    where

    Λ1i=Labihaimj=1(aMij+bMij)˜FjhaiIMi,
    Λ2j=Lcdjhcjni=1(cMji+dMji)˜GihcjJMj,

    in which

    IMi=max0tωIi(t),JMj=max0tωJj(t),τMij=max0tωτij(t),
    σMji=max0tωσji(t),˜τMij=max0tωτij(t),˜σMji=max0tωσji(t),.

    and 1τMij>0, 1σMji>0, 1˜τMij>0,1˜σMji>0.

    (H9) 2<Iik<0, 2<Jjk<0, i=1,2,,n, j=1,2,,m, k=1,2,,p. Then the ωperiodic solution (xT(t),yT(t))T of systems (2.1) and (2.2) is global asymptotic stable.

    Proof. From Theorem 1, we find that systems (2.1) and (2.2) has at least one ωperiodic solution under assumptions (H1)-(H5). Let (xT(t),yT(t))T be one ωperiodic solution of systems (2.1) and (2.2). For any solution (x(t)T,y(t)T)T of system (2.1), we let

    ui(t)=xi(t)xi(t),vj(t)=yj(t)yj(t),

    then

    ˙ui(t)=˙xi(t)˙xi(t),˙vj(t)=˙yj(t)˙yj(t).

    It is easy to see that system (2.1) can be reduced to the following system

    {dui(t)dt=[ai(ui(t)+xi(t))bi(ui(t)+xi(t))ai(xi(t))bi(xi(t))]+ai(ui(t)+xi(t))mj=1aij(t)fj(yj(tτij(t)))ai(ui(t)+xi(t))mj=1aij(t)fj(yj(tτij(t)))+ai(ui(t)+xi(t))mj=1bij(t)fj(˙yj(t˜τij(t)))ai(ui(t)+xi(t))mj=1bij(t)fj(˙yj(t˜τij(t)))+(ai(ui(t)+xi(t))ai(xi(t)))mj=1aij(t)fj(yj(tτij(t)))+(ai(ui(t)+xi(t))ai(xi(t)))mj=1bij(t)fj(˙yj(t˜τij(t)))+(ai(ui(t)+xi(t))ai(xi(t)))Ii(t),t[o,ω],ttk,Δxi(tk)=xi(t+k)xi(tk)=Iik(xi(tk)),i=1,2,,n,k=1,2,,dvj(t)dt=[cj(vj(t)+yj(t))dj(vj(t)+yj(t))cj(yj(t))dj(yj(t))]+cj(vj(t)+yj(t))ni=1cji(t)gi(xi(tσji(t)))cj(vj(t)+yj(t))ni=1cji(t)gi(xi(tσji(t)))+cj(vj(t)+yj(t))ni=1dji(t)gi(˙xi(t˜σji(t)))cj(vj(t)+yj(t))ni=1dji(t)gi(˙xi(t˜σji(t)))+(cj(vj(t)+yj(t))cj(yj(t)))ni=1cji(t)gi(xi(tσji(t)))+(cj(vj(t)+yj(t))cj(yj(t)))ni=1dji(t)gi(˙xi(t˜σji(t)))+(cj(vj(t)+yj(t))cj(yj(t)))Jj(t),t[o,ω],ttk,Δyj(tk)=yj(t+k)yj(tk)=Jjk(yj(tk)),j=1,2,,m,k=1,2,. (4.1)

    From system (4.1), we have

    D+ui(t)[Labihaimj=1(aMij+bMij)˜FjhaiIMi]|ui(t)|+aMimj=1aMijFj(vj(tτij(t)))+aMimj=1bMijFj(˙vj(t˜τij(t))), (4.2)

    and

    D+vj(t)[Lcdjhcjni=1(cMji+dMji)˜GihcjJMj]|vj(t)|+cMjni=1cMjiGi(ui(tσji(t)))+cMjni=1dMjiGi(˙ui(t˜σji(t))), (4.3)

    for all i=1,2,,n and j=1,2,,m.

    Define V(t)=V1(t)+V2(t), where

    V1(t)=ni=1[θieγt|ui(t)|+aMimj=1θiaMijFj1τMijttτij(t)|vj(s)|eγ(s+τMij)ds+aMimj=1θibMijFj1˜τMij+t˜τij(t)|˙vj(s)|eγ(s+˜τMij)ds], (4.4)

    and

    V2(t)=mj=1[θn+jeγt|vj(t)|+cMjni=1θn+jcMjiGi1σMjittσji(t)|ui(s)|eγ(s+σMji)ds+cMjni=1θn+jdMjiGi1˜σMji+t˜σji(t)|˙ui(s)|eγ(s+˜σMji)ds], (4.5)

    From (4.2) and (4.3), we have

    D+V1(t)ni=1θi((Labihaimj=1(aMij+bMij)˜FjhaiIMiγ))|ui(t)|eγt+θieγtaMimj=1aMijFj(vj(tτij(t)))+θieγtaMimj=1bMijFj(˙vj(t˜τij(t)))+aMimj=1θiaMijFj1τMij[|vj(t)|eγ(t+τMij)|vj(tτij(t))|eγ(tτij(t)+τMij)(1τij(t))]+aMimj=1θibMijFj1˜τMij[|˙vj(t˜τij(t))|eγ(t˜τij(t)+˜τMij)(1˜τij(t))].

    According to

    1τij(t)1τMij,eγ(tτij(t)+τMij)eγt,
    1˜τij(t)1˜τMij,eγ(t˜τij(t)+˜τMij)eγt,

    we obtain

    D+V1(t)ni=1[θi(Λ1iγ)|ui(t)|eγt+mj=1θiaMiaMijFj1τMij|vj(t)|eγ(t+τMij)],

    where

    Λ1i=Labihaimj=1(aMij+bMij)˜FjhaiIMi.

    Similarly to the calculation of D+V1(t), we have

    D+V2(t)mj=1[θn+j(Λ2iγ)|vj(t)|eγt+ni=1θn+jcMjcMjiGi1σMji|ui(t)|eγ(t+σMji)],

    Hence

    D+V(t)eγtni=1[θi(Λ1iγ)+mj=1θn+jcMjcMjiGi1σMjieγσMji]|ui(t)|+eγtmj=1[θn+j(Λ2iγ)+ni=1θiaMiaMijFj1τMijeγτMij]|vj(t)|<0.

    In view of assumption (H3), we have

    V(t+k)=ni=1[θieγt+k|ui(t+k)|+aMimj=1θiaMijFj1τMijt+kt+kτij(t+k)|vj(s)|eγ(s+τMij)ds+mj=1θiaMibMijFj1˜τMij+t+k˜τij(t+k)|˙vj(s)|eγ(s+˜τMij)ds]+mj=1[θn+jeγt+k|vj(t+k)|+cMjni=1θn+jcMjiGi1σMjit+kt+kσji(t+k)|ui(s)|eγ(s+σMji)ds+mj=1ni=1θn+jcMjdMjiGi1˜σMji+t+k˜σji(t+k)|˙ui(s)|eγ(s+˜σMji)ds]ni=1[θieγtk|(1+Iik)ui(tk)|+aMimj=1θiaMijFj1τMijtktkτij(tk)|vj(s)|eγ(s+τMij)ds+mj=1θiaMibMijFj1˜τMij+tk˜τij(tk)|˙vj(s)|eγ(s+˜τMij)ds]+mj=1[θn+jeγtk|(1+Jjk)vj(tk)|+cMjni=1θn+jcMjiGi1σMjitktkσji(tk)|ui(s)|eγ(s+σMji)ds+mj=1ni=1θn+jcMjdMjiGi1˜σMji+tk˜σji(tk)|˙ui(s)|eγ(s+˜σMji)ds]V(tk).

    Thus, by the standard Lyapunov functional theory, the periodic solution (xT,yT)T is global asymptotic stable. The proof is complete.

    Remark 2. In [20], the authors discussed a model describing dynamics of delayed Cohen-Grossberg-type BAM neural networks without impulses. In our paper, we not only consider the impact of impulses and construct a new Lyapunov functional to establish the existence and the global asymptotic stability of periodic solutions.

    Remark 3. In [16], the impulsive function is linear. We discussed a kind of more general bounded and Lipschitz continuous functions in this paper.

    Remark 4. In [32], the authors discussed a kind of BAM neural networks with time-varying delays and impulses. In this paper, we propose a new kind of Cohen-Grossberg-type BAM neural network systems, which have a more wide application in practice. Obviously Cohen-Grossberg-type BAM neural networks can be reduced to Hopfield-type BAM neural networks and cellular BAM neural networks.

    Corollary 1. Suppose that the assumptions (H1)–(H3) hold, then the systems (2.1) and (2.2) without impulses has at least one ωperiodic solution.

    Remark 5. The consideration of neutral delays may affect the stability of systems since the presence of delays may induce complex behaviors for the schemes. The existence of delays plays an increasingly important role in many disciplines like economic, mathematics, science, and engineering, which can also help describe propagation and transport phenomena or population dynamics, etc. For instance, in economic systems, presence delays appear in a natural way since decisions and effects are separated by some time interval.

    As applications, we present an example to illustrate our main results in Theorem 1 and Theorem 2.

    Example 1. Consider the Cohen-Grossberg-type BAM neural networks with m=n=1, which is given as

    {˙x1(t)=a1(x1(t))[b1(x1(t))a11(t)f1(y1(tτ11(t)))b11(t)f1(˙y1(t˜τ11(t)))I1(t)],t>0,ttk,Δx1(tk)=I1k(x1(tk)),k=1,2,,˙y1(t)=c1(y1(t))[d1(y1(t))c11(t)g1(x1(tσ11(t)))d11(t)g1(˙x1(t˜σ11(t)))J1(t)],t>0,ttk,Δy1(tk)=J1k(y1(tk)),k=1,2,, (5.1)

    where

    a1(u)=13+13sinu,b1(u)=u(1313sinu),c1(u)=12+12cosu,d1(u)=u(1212cosu),
    f1(u)=sinu,g1(u)=12(|sinu+1||sinu1|),I1(t)=115(2+sint),
    J1(t)=115(2+cost),a11(t)=b11(t)=c11(t)=d11(t)=130sint,
    τ11=˜τ11=σ11=˜σ11=110sint,I1k(u)=1+sinu,J1k(u)=1+cosu.

    By a straightforward calculation, we obtain

    aM11=bM11=cM11=dM11=130,˜F1=1,˜G1=1,IM1=JM1=115,
    ha1=13,hc1=12,aL1=cL1=0,aM1=cM1=23,bL1=dL1=0,
    bM1=dMj=1,Lab1=19,Lcd1=14,τM11=˜τM11=σM11=˜σM11=110.

    Thus

    Λ11=445 and Λ21=1360.

    Choose γ=1100(0,min(Λ11,Λ21)), there exist positive constants θ1=100 and θ2=50, such that

    θ1(Λ11γ)+θ2cM1cM11G11σMjieγσM11=100×(4451100)+10081×e110006.653085802263323<0,

    and

    θ2(Λ21γ)+θ1aM1aM11F11τM11eγτM11=50×(4451100)+20081×e110001.472838271193313<0.

    By Theorem 1, system (5.1) has a 2πperiodic solution. From Theorem 2, all other solutions of system (5.1) converges asymptotically to the periodic solution as t+.

    We have introduced Cohen-Grossberg-type BAM neural networks (2.1) and (2.2) with neutral-type time delays and impulses, and obtained some results on the existence and stability of periodic solutions. The impulse terms in (2.1) are bounded and Lipschitz continuous functions instead of linear functions. What's more, we utilized both the method of the classical estimation and Lyapunov functional construction to search for the region of periodic solutions.

    The existing proof of periodic solution is very classical and effective approach and the method has been widely applied to studying the periodic solution for more 25 years. The proof of the global stability part has some novel in constructing Laypunov function. Hence, we also apply the new Lyapunov function [33] as in the stability to entail the proof of the existing part.

    Lemma 3. For any λ(0,1), consider the operator equation Lz=λNz, if the periodic solutions of system (3.3) exist, then they are bounded and the boundary is independent of the choice of λ under assumption (H1)-(H5), Namely, there exists a positive constant ˉH0 such that when (xT(t),yT(t))T=(x1(t),,xn(t),y1(t),,ym(t))TˉH0.

    Proof. Suppose that (x1(t),,xn(t),y1(t),,ym(t))TX is a solution of system (3.3) for some λ(0,1). It can be thus obtained from system (3.3) that

    D+xi(t)λ[aLibLi|xi(t)|mj=1aMi(aMij+bMij)˜FjaMiIMi]λ[ζ11|xi(t)|ζ12], (6.1)

    and

    D+yj(t)λ[cLjdLj|yj(t)|ni=1cMj(cMji+dMji)˜GicMjJMj]λ[ζ21|xi(t)|ζ22], (6.2)

    for all i=1,2,,n and j=1,2,,m, where

    ζ11=aLibLi,ζ12=mj=1aMi(aMij+bMij)˜Fj+aMiIMi,
    ζ21=cLjdLj,ζ22=ni=1cMj(cMji+dMji)˜Gi+cMjJMj.

    Define V(t)=V1(t)+V2(t), where

    V1(t)=ni=1μ1i|xi(t)|2+ni=1μ2i|xi(t)|,

    and

    V2(t)=mj=1δ1j|yj(t)|2+mj=1δ2j|yj(t)|,

    in which μ1i,μ2i,δ1j,δ2j>0. Since (x1(t),,xn(t),y1(t),,ym(t))T is a periodic solution of system (3.3), then V(x1(t),,xn(t),y1(t),,ym(t)) is a periodic function.

    One may further get

    D+V1(t)2λni=1μ1i|xi(t)|(ζ11|xi(t)|ζ12)λni=1μ2i(ζ11|xi(t)|ζ12)=ni=1[2λζ11μ1i|xi(t)|2+(2λμ1iζ12λμ2iζ11)|xi(t)|+λμ2iζ12],

    and

    D+V2(t)2λmj=1δ1j|yj(t)|(ζ21|yj(t)|ζ22)λmj=1δ2j(ζ21|yj(t)|ζ22)=mj=1[2λζ21δ1j|yj(t)|2+(2λδ1jζ22λδ2jζ21)|yj(t)|+λδ2jζ22].

    Thus

    D+V(t)ni=1[2λζ11μ1i|xi(t)|2+(2λμ1iζ12λμ2iζ11)|xi(t)|+λμ2iζ12]+mj=1[2λζ21δ1j|yj(t)|2+(2λδ1jζ22λδ2jζ21)|yj(t)|+λδ2jζ22].

    From

    2λζ11μ1i|xi(t)|2+(2λμ1iζ12λμ2iζ11)|xi(t)|+λμ2iζ12=0,

    and

    2λζ21δ1j|yj(t)|2+(2λδ1jζ22λδ2jζ21)|yj(t)|+λδ2jζ22=0,

    there exist positive constants h1,h2 such that the solutions satisfy

    maxt[0,ω]|xi(t)|>h1,maxt[0,ω]|yj(t)|>h2.

    It follows that when xi(t)>h1,yj(t)>h2, we can choose a positive constant ˜H=nh1+mh2, such that (x1(t),,xn(t),y1(t),,ym(t))T>˜H, and

    2λζ11μ1i|xi(t)|2+(2λμ1iζ12λμ2iζ11)|xi(t)|+λμ2iζ12<0,

    and

    2λζ21δ1j|yj(t)|2+(2λδ1jζ22λδ2jζ21)|yj(t)|+λδ2jζ22<0.

    Hence,

    D+V(t)<0.

    In fact, if (x1(t),,xn(t),y1(t),,ym(t))T is unbounded, then for any ˉH>˜H, we have

    (x1(t),,xn(t),y1(t),,ym(t))T>ˉH>˜H.

    It follows that D+V(t)<0, which contradicts the fact that V(x1(t),,xn(t),y1(t),,ym(t)) is a periodic function. This implies that (x1(t),,xn(t),y1(t),,ym(t))TˉH0, where ˉH0 is a positive constant. This completes the proof.

    The authors wish to express sincere thanks to the anonymous reviewers for their very careful corrections, valuable comments and suggestions for improving the quality of the paper. This work is supported by the Natural Science Foundation of China (Grants No. 11771185 and 11871251) and Natural Science Foundation of Jiangsu Higher Education Institutions (18KJB180027).

    The authors confirm no conflicts of interest in this paper.


    Acknowledgments



    This research was supported by the National Health and Medical Research Council grant APP1070081 to TB and a University of Queensland International PhD Scholarship to MA. Imaging/Analysis was performed at the Queensland Brain Institute's Advanced Microscopy Facility.

    Conflict of interest



    The authors declare no conflict of interest.

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