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Ionic Gradients, Membrane Potential and Ionic Currents Constance Hammond

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CHAPTER 3 c0015 Ionic gradients, membrane potential and ionic currents Constance Hammond OUTLINE u0010 3.1 There is an unequal distribution of 3.4 The passive diffusion of ions through an u0025 ions across neuronal plasma membrane. open channel creates a current 45 The notion of concentration gradient 39 3.5 A particular membrane potential, the resting u0030 u0015 3.2 There is a difference of potential between membrane potential Vrest 46 the two faces of the membrane, called 3.6 A simple equivalent electrical circuit u0035 membrane potential ( V ) 42 m for the membrane at rest 48 u0020 3.3 Concentration gradients and membrane 3.7 How to experimentally change V 49 u0040 potential determine the direction of the rest passive movements of ions through ionic 3.8 Summary 50 u0045 channels: the electrochemical gradient 43 p0080 The neuronal plasma membrane delimits the whole 3.1 THERE IS AN UNEQUAL st0025 neuron, cell body, dendrites, dendritic spines, axon and DISTRIBUTION OF IONS ACROSS axon terminals. It is a barrier between the intracellular NEURONAL PLASMA MEMBRANE. and extracellular environments. The general structure of THE NOTION OF CONCENTRATION the neuronal plasma membrane is similar to that of other GRADIENT plasma membranes. It is made up of proteins inserted in a lipid bilayer, forming as a whole a ‘fl uid mosaic’ 3.1.1 The plasma membrane separates st0030 ( Figure 3.1 ). However, insofar as there are functions that two media of different ionic composition are exclusively neuronal, the neuronal membrane dif- fers from other plasma membranes by the nature, den- Regardless of the animal’s environment (seawater, p0090 freshwater or air), potassium (K + ) ions are the predomi- sity and spatial distribution of the proteins of which it is + composed. nant cations in the intracellular fl uid and sodium (Na ) ions are the predominant cations in the extracellular fl u- p0085 The presence of a large diversity of transmembrane id. The main anions of the intracellular fl uid are organic proteins called ionic channels (or simply ‘channels’) char- − acterizes the neuronal plasma membrane. They allow molecules (P ): negatively charged amino acids (gluta- the passive movement of ions across membranes and mate and aspartate), proteins, nucleic acids, phosphates, etc… which have a large molecular weight. In the extra- thus electrical signaling in the nervous system. Among − the ions present in the nervous system fl uids, Na + , K + , cellular fl uid, the predominant anions are chloride (Cl ) 2+ − ions. A marked difference between cytosolic and extra- Ca and Cl ions seem to be responsible for almost all 2+ of the action. cellular Ca concentrations is also observed ( Figure 3.2 ) . Cellular and Molecular Neurophysiology. DOI: 10.1016/B978-0-12-397032-9.00003-0 Copyright © 2015 Elsevier Ltd. All rights reserved 39 ISBN: 978-0-12-397032-9; PII: B978-0-12-397032-9.00003-0; Author: HAMMONDENGLISH; Document ID: 00003; Chapter ID: c0015 CC0015.indd0015.indd 3399 008/10/148/10/14 88:37:37 AAMM 40 3. IONIC GRADIENTS, MEMBRANE POTENTIAL AND IONIC CURRENTS Alpha-helix protein Glycolipid Oligosaccharide side chain Globular Phospholipid protein Hydrophobic segment of alpha-helix protein Cholesterol f0010 FIGURE 3.1 Fluid mosaic. Transmembrane proteins and lipids are kept together by non-covalent interactions (ionic and hydrophobic). From dictionary.laborlawtalk.com/Plasma_membrane. 2+ Spatial distribution of Ca ions inside the cell de- p0095 serves a more detailed description. Ca2+ ions are pres- (in mM) ent in the cytosol as ‘free’ Ca 2+ ions at a very low con- ϩ ϭ 8 7 2+ (in mM) [K ]e 3 centration (10 to 10 M) and as bound Ca ions (bound ϩ ϭ 2+ [Na ]e 140 to Ca -binding proteins). They are also distributed in Ϫ ϭ ϭϪ ϩ [Cl ]e 146 organelles able to sequester calcium, which include Vm 60 mV [K ] ϭ 140 i 2ϩ ϭ [Naϩ] ϭ 14 [Ca ]e 1.5 endoplasmic reticulum, calciosome and mitochondria, i 2+ Ϫ ϭ where they constitute the intracellular Ca stores. Free [Cl ]i 14 2ϩ ϭ 2+ [Ca ]i 0.0001 intracellular Ca ions present in the cytosol act as sec- Protein ond messengers and transduce electrical activity in neu- ϩ Ϫ rons into biochemical events such as exocytosis. Ca2+ ions bound to cytosolic proteins or present in organelle stores are not active Ca 2+ ions; only ‘free’ Ca2+ ions have Nucleus a role. In spite of the unequal distribution of ions across the p0100 plasma membrane, intracellular and extracellular media Mitochondrion are neutral ionic solutions: in each medium, the concen- tration of positive ions is equal to that of negative ions. According to Figure 3.2 , ++ + [Na ]e++ [K ]e 2[Ca2 ]e =++×= 140 3 (2 1.5) 146mM ϩ Ca2 store in − = endoplasmic [Cl ]e 146mM reticulum ++++2 + =++ × [Na ]ii [K ] 2[Ca ]i 14 140 0.0002(2 0.0001) = 154mM Plasma membrane − ΔpH ϭ 1.4 But [Cl ]i = 14 mM p0105 [Hϩ] intermembrane > [Hϩ] matrix In the intracellular compartment, other anions than p0110 f0015 FIGURE 3.2 There is an unequal distribution of ions across neu- chloride ions are present and compensate for the posi- ronal plasma membranes. Idealized nerve cell (depicted as a sphere) − 2 − with intra- and extracellular ionic concentrations. Membrane potential tive charges. These anions are HCO3 , PO4 , amino ac- is the difference of potential (in mV) between the intracellular and ex- ids, proteins, nucleic acids, etc. Most of these anions are tracellular faces of the plasma membrane. organic anions that do not cross the membrane. I. NEURONS: EXCITABLE AND SECRETORY CELLS THAT ESTABLISH SYNAPSES ISBN: 978-0-12-397032-9; PII: B978-0-12-397032-9.00003-0; Author: HAMMONDENGLISH; Document ID: 00003; Chapter ID: c0015 CC0015.indd0015.indd 4400 008/10/148/10/14 88:37:37 AAMM 3.1 UNEQUAL DISTRIBUTION OF IONS ACROSS NEURONAL PLASMA MEMBRANE 41 st0035 3.1.2 The unequal distribution of ions across (a) DNP Ϫ1 the neuronal plasma membrane is kept constant 100 0.2 mmol l by active transport of ions 50 p0115 A difference of concentration between two compart- 30 1 ments is called a ‘ concentration gradient ’. Measurements Ϫ s 20 + + 2+ − 2 of Na , K , Ca and Cl concentrations have shown that Ϫ concentration gradients for ions are constant in the ex- 10 ternal and cytosolic compartments, at the macroscopic level, during the entire neuronal life. 5 p moles-cm p0120 At least two hypotheses can explain this constancy: 3 + + 2+ − u0065 • N a , K , Ca and Cl ions cannot cross the plasma 2 membrane: plasma membrane is impermeable to these inorganic ions. In that case, concentration gradients 1 50 100 150 200 250 need to be established only once in the lifetime. Minutes + + 2+ u0070 • Plasma membrane is permeable to Na , K , Ca and − Cl ions but there are mechanisms that continuously (b) Active efflux of Naϩ re-establish the gradients and maintain constant the Passive influx of Naϩ Naϩ unequal distribution of ions. ϩ [Na ]e is constant p0135 This has been tested experimentally by measuring ϩ ionic fl uxes. When proteins are absent from a synthetic [Na ]i is constant ϩ lipid bilayer, no movements of ions occur across this Axon Na ATP ADP ϩ ϩ purely lipidic membrane. Owing to its central hydro- H2O Pi phobic region, the lipid bilayer has a low permeability + to hydrophilic substances such as ions, water and polar FIGURE 3.3 Na fl uxes through the membrane of giant axons of f0020 sepia. ( a ) Effect of dinitrophenol (DNP) on the outfl ux of *Na + as a molecules; i.e. the lipid bilayer is a barrier for the diffu- function of time. The axon is previously loaded with *Na+ . At t = 1, the sion of ions and most polar molecules. axon is transferred in a bath devoid of *Na + . The ordinate (logarithmic) p0140 The fi rst demonstrations of ionic fl uxes across plasma axis is the quantity of *Na + ions that appear in the bath (that leave the membrane by Hodgkin and Keynes (1955) were based axon) as a function of time. At t = 100 min, DNP (0.2 mM) is added to on the use of radioisotopes of K + or Na + ions. Experi- the bath for 90 min. The effl ux, which previously decreased linearly with time, is totally blocked after one hour of DNP. This blockade is ments were conducted on the isolated squid giant axon. reversible. ( b ) Passive and active Na + fl uxes are in opposite directions. When this axon is immersed in a bath containing a con- Plot ( a ) adapted from Hodgkin AL and Keynes RD (1955) Active trans- trol concentration of radioactive *Na + ( 24 Na + ) instead of port of cations in giant axons from sepia and loligo. J. Physiol. (Lond.) cold Na + ( 22 Na + ), *Na + ions constantly appear in the cy- 128, 28-60, with permission. toplasm. This *Na + infl ux is not affected by dinitrophe- nol (DNP), a blocker of ATP synthesis in mitochondria. It does not require energy expenditure. This is passive This experiment demonstrates that cells maintain p0150 transport. This result is in favor of the second hypothesis their ionic composition in the face of continuous pas- and leads to the following question: what are the mecha- sive exchange of all principal ions by active transport of nisms that maintain concentration gradients across neu- these ions in the reverse direction. In other words, ionic ronal membranes? composition of cytosol and extracellular compartments p0145 When the reverse experiment is conducted, the isolat- are maintained at the expense of a continuous basal me- ed squid giant axon is passively loaded with radioactive tabolism that provides energy (ATP) utilized to actively *Na + by performing the above experiment, and is then transport ions and thus to compensate for their passive transferred to a bath containing cold Na + .
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