Graded Signals: Is the All-Or-None Law Exceptional? Why Spikes?
How common are spikeless neurons? Such neurons, producing only signals of graded amplitude, abound in the vertebrate retina and in arthropod ventral cord ganglia and a few other places. We cannot yet discern principles about where nature uses them; they do not correlate with small cells or short axon cells or amacrine cells or with chemically or electrically transmitting cells. Their apparent absence in gastropods is puzzling; they may well turn up but even so, we are led to suggest that this trait is an option in evolution, not a functional requirement. In the vertebrate brain and cord their apparent absence may only reflect the difficulty of demonstrating them; I am betting they are common.
A larger mystery is this: how general may be the use of graded signals even among neurons that can spike? Between spikes it may be general or only common or really rare that axon terminals or dendrites or somata influence adjacent neurons by graded, perhaps feeble and slow transmitter release or by electric fields. Evidence that such influence happens is strong; no evidence limits its generality.
Even the impulses near the terminals of long axons may commonly or perhaps usually propagate nondecrementally only up to a point, then pass a boundary and begin to fall below a safety factor of 1.0, reaching the end and releasing transmitter or passing current to a graded degree. The degree may depend on spike intervals, on presynaptic synapses, on the state of the terminal and subterminal membranes, and on the cellular milieu at the moment—which involves neuroglial function and includes the concentration of modulators, ions, nonspecific metabolites, and the width of the fluctuating intercellular space.
Paraneurons, such as pinealocytes, pancreatic endocrine cells, SIFcells in sympathetic ganglia, secondary sense cells, and others, are not all spikeless but their usual mode of response is probably graded.
The functional significance of signals of graded amplitude as opposed to all-or-none pulses with graded intervals presumably includes the summation of converging signals without refractory periods and the simplicity of linear and nonlinear interactions.
The functional significance of all-or-none nerve impulses (spikes) can no longer be considered to be mainly an adaptation to long distance signalling; they are well known in unicellular organisms and small-sized, lower invertebrates as well as in many local, short axon and even amacrine cells of higher animals. I believe—that is to say, I am betting spikes have another value, namely in encoding information, in addition to faithful propagation where long axons do occur. Pulse codes (number of impulses, intervals, distribution of intervals, and derivatives of these) may offer advantages over amplitude of graded signals in independence from perturbation and in signal to noise ratios.
KeywordsHair Cell Olfactory Bulb Amacrine Cell Vertebrate Retina Intrinsic Neuron
Unable to display preview. Download preview PDF.
- Bennett MVL (1967): Mechanisms of electroreception. In: Lateral Line Detectors, Cahn P ed. Bloomington: Indiana University Press, pp 313–393Google Scholar
- Bishop GH (1956): Natural history of the nerve impulse. Physiol Rev 36: 376–399Google Scholar
- Bremer F (1944): L’activité “spontanée” des centres nerveux. Bull Acad Roy Med Belg (Ser 6) 9: 148–173Google Scholar
- Fain GL (1981): Integration by spikeless neurones in the retina. In: Neurones Without Impulses, Roberts A, Bush BMH, eds. Cambridge: Cambridge University Press, pp 29–59Google Scholar
- Fujita T (1989): Present status of the paraneuron concept. Arch Histol Cytol 52(Suppl):l-8Google Scholar
- Gerard RW (1941): The interaction of neurones. Ohio J Sci 41: 160–172Google Scholar
- HarderW (1968): Die Beziehungen zwischenElektrorezeptoren, elektrischen Organen, Seitenlinienorganen und Nervensystemen bei den Mormyridae (Teleostei, Pisces). Z Vgl Physiol 59: 272–318Google Scholar
- Maynard DM (1967): Organization of central ganglia. In: Invertebrate Nervous Systems, Wiersma CAG, ed. Chicago: University of Chicago Press, pp 231–255Google Scholar
- Parry DA (1947): The function of the insect ocellus. J Exp Biol 24: 211–219Google Scholar
- Roberts A, Bush BMH (1981): Neurones Without Impulses. Cambridge: Cambridge University PressGoogle Scholar
- Shepherd GM (1981): Synaptic and impulse loci in olfactory bulb dendritic circuits. In Neurones Without Impulses, Roberts A, Bush BMH, eds. Cambridge: Cambridge University Press, pp 255–267Google Scholar
- Vowles DM (1964): Models of the insect brain. In: Neural Theory and Modeling, Reiss RF ed. Stanford: Stanford University Press, pp 377–399Google Scholar
- Werblin FS, Dowling JE (1969): Organisation of the retina of the mud puppy. Necturus maculosus II. Intracellular recording. J Neurophysio132: 339–355Google Scholar
- Zakon H (1986): The electroreceptive periphery. In: Electroreception, Bullock TH, Heiligenberg W, eds. New York: John Wiley and Sons, pp 103–156Google Scholar