Professional Education

  • Doctor of Philosophy, Georgia State University (2013)
  • Master of Science, Georgia State University (2011)
  • Bachelor of Science, Shanghai University (2007)

Stanford Advisors

  • Lu Chen, Postdoctoral Faculty Sponsor

All Publications

  • Acetylcholine elongates neuronal growth cone filopodia via activation of nicotinic acetylcholine receptors DEVELOPMENTAL NEUROBIOLOGY Zhong, L. R., Estes, S., Artinian, L., Rehder, V. 2013; 73 (7): 487-501


    In addition to acting as a classical neurotransmitter in synaptic transmission, acetylcholine (ACh) has been shown to play a role in axonal growth and growth cone guidance. What is not well understood is how ACh acts on growth cones to affect growth cone filopodia, structures known to be important for neuronal pathfinding. We addressed this question using an identified neuron (B5) from the buccal ganglion of the pond snail Helisoma trivolvis in cell culture. ACh treatment caused pronounced filopodial elongation within minutes, an effect that required calcium influx and resulted in the elevation of the intracellular calcium concentration ([Ca]i ). Whole-cell patch clamp recordings showed that ACh caused a reduction in input resistance, a depolarization of the membrane potential, and an increase in firing frequency in B5 neurons. These effects were mediated via the activation of nicotinic acetylcholine receptors (nAChRs), as the nAChR agonist dimethylphenylpiperazinium (DMPP) mimicked the effects of ACh on filopodial elongation, [Ca]i elevation, and changes in electrical activity. Moreover, the nAChR antagonist tubucurarine blocked all DMPP-induced effects. Lastly, ACh acted locally at the growth cone, because growth cones that were physically isolated from their parent neuron responded to ACh by filopodial elongation with a similar time course as growth cones that remained connected to their parent neuron. Our data revealed a critical role for ACh as a modulator of growth cone filopodial dynamics. ACh signaling was mediated via nAChRs and resulted in Ca influx, which, in turn, caused filopodial elongation.

    View details for DOI 10.1002/dneu.22071

    View details for Web of Science ID 000320190800001

    View details for PubMedID 23335470



    Dopamine (DA) plays fundamental roles as a neurotransmitter and neuromodulator in the central nervous system. How DA modulates the electrical excitability of individual neurons to elicit various behaviors is of great interest in many systems. The buccal ganglion of the freshwater pond snail Helisoma trivolvis contains the neuronal circuitry for feeding and DA is known to modulate the feeding motor program in Helisoma. The buccal neuron B5 participates in the control of gut contractile activity and is surrounded by dopaminergic processes, which are expected to release DA. In order to study whether DA modulates the electrical activity of individual B5 neurons, we performed experiments on physically isolated B5 neurons in culture and on B5 neurons within the buccal ganglion in situ. We report that DA application elicited a strong hyperpolarization in both conditions and turned the electrical activity from a spontaneously firing state to an electrically silent state. Using the cell culture system, we demonstrated that the strong hyperpolarization was inhibited by the D2 receptor antagonist sulpiride and the phospholipase C (PLC) inhibitor U73122, indicating that DA affected the membrane potential of B5 neurons through the activation of a D2-like receptor and PLC. Further studies revealed that the DA-induced hyperpolarization was inhibited by the K channel blockers 4-aminopyridine and tetraethylammonium, suggesting that K channels might serve as the ultimate target of DA signaling. Through its modulatory effect on the electrical activity of B5 neurons, the release of DA in vivo may contribute to a neuronal output that results in a variable feeding motor program.

    View details for DOI 10.1016/j.neuroscience.2012.10.005

    View details for Web of Science ID 000313938700010

    View details for PubMedID 23069757

  • Nitric oxide as intracellular modulator: internal production of NO increases neuronal excitability via modulation of several ionic conductances EUROPEAN JOURNAL OF NEUROSCIENCE Artinian, L., Zhong, L., Yang, H., Rehder, V. 2012; 36 (10): 3333-3343


    Nitric oxide (NO) has been shown to regulate neuronal excitability in the nervous system, but little is known as to whether NO, which is synthesized in certain neurons, also serves functional roles within NO-producing neurons themselves. We investigated this possibility by using a nitric oxide synthase (NOS)-expressing neuron, and studied the role of intrinsic NO production on neuronal firing properties in single-cell culture. B5 neurons of the pond snail Helisoma trivolvis fire spontaneous action potentials (APs), but once the intrinsic activity of NOS was inhibited, neurons became hyperpolarized and were unable to fire evoked APs. These striking long-term effects could be attributed to intrinsic NO acting on three types of conductances, a persistent sodium current (I(NaP) ), voltage-gated Ca currents (I(Ca) ) and small-conductance calcium-activated potassium (SK) channels. We show that NOS inhibitors 7-nitroindazole and S-methyl-l-thiocitrulline resulted in a decrease in I(NaP) , and that their hyperpolarizing and inhibiting effects on spontaneous spiking were mimicked by the inhibitor of I(NaP) , riluzole. Moreover, inhibition of NOS, soluble guanylate cyclase (sGC) or protein kinase G (PKG) attenuated I(Ca) , and blocked spontaneous and depolarization-induced spiking, suggesting that intrinsic NO controlled I(Ca) via the sGC/PKG pathway. The SK channel inhibitor apamin partially prevented the hyperpolarization observed after inhibition of NOS, suggesting a downregulation of SK channels by intrinsic NO. Taken together, we describe a novel mechanism by which neurons utilize their self-produced NO as an intrinsic modulator of neuronal excitability. In B5 neurons, intrinsic NO production is necessary to maintain spontaneous tonic and evoked spiking activity.

    View details for DOI 10.1111/j.1460-9568.2012.08260.x

    View details for Web of Science ID 000311299700004

    View details for PubMedID 22913584

  • Nitric Oxide Acts as a Volume Transmitter to Modulate Electrical Properties of Spontaneously Firing Neurons via Apamin-Sensitive Potassium Channels JOURNAL OF NEUROSCIENCE Artinian, L., Tornieri, K., Zhong, L., Baro, D., Rehder, V. 2010; 30 (5): 1699-1711


    Nitric oxide (NO) is a radical and a gas, properties that allow NO to diffuse through membranes and potentially enable it to function as a "volume messenger." This study had two goals: first, to investigate the mechanisms by which NO functions as a modulator of neuronal excitability, and second, to compare NO effects produced by NO release from chemical NO donors with those elicited by physiological NO release from single neurons. We demonstrate that NO depolarizes the membrane potential of B5 neurons of the mollusk Helisoma trivolvis, initially increasing their firing rate and later causing neuronal silencing. Both effects of NO were mediated by inhibition of Ca-activated iberiotoxin- and apamin-sensitive K channels, but only inhibition of apamin-sensitive K channels fully mimicked all effects of NO on firing activity, suggesting that the majority of electrical effects of NO are mediated via inhibition of apamin-sensitive K channels. We further show that single neurons release sufficient amounts of NO to affect the electrical activity of B5 neurons located nearby. These effects are similar to NO release from the chemical NO donor NOC-7 [3-(2-hydroxy-1-methyl-2-nitrosohydazino)-N-methyl-1-propyanamine], validating the use of NO donors in studies of neuronal excitability. Together with previous findings demonstrating a role for NO in neurite outgrowth and growth cone motility, the results suggest that NO has the potential to shape the development of the nervous system by modulating both electrical activity and neurite outgrowth in neurons located in the vicinity of NO-producing cells, supporting the notion of NO functioning as a volume messenger.

    View details for DOI 10.1523/JNEUROSCI.4511-09.2010

    View details for Web of Science ID 000274246700013

    View details for PubMedID 20130179