What Are the Mechanisms for Analogue and Digital Signalling in the Brain? Dominique Debanne, Andrzej Bialowas, Sylvain Rama

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What Are the Mechanisms for Analogue and Digital Signalling in the Brain? Dominique Debanne, Andrzej Bialowas, Sylvain Rama What are the mechanisms for analogue and digital signalling in the brain? Dominique Debanne, Andrzej Bialowas, Sylvain Rama To cite this version: Dominique Debanne, Andrzej Bialowas, Sylvain Rama. What are the mechanisms for analogue and digital signalling in the brain?. Nature Reviews Neuroscience, Nature Publishing Group, 2013, 14, pp.63-69. hal-01766838 HAL Id: hal-01766838 https://hal-amu.archives-ouvertes.fr/hal-01766838 Submitted on 25 Apr 2018 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. examples of graded transmission in the absence of spiking activity have also been What are the mechanisms for described in invertebrate neurons (see REF. 7 for a review). analogue and digital There is now evidence that analogue signalling exists at spiking synapses, where signalling in the brain? neurotransmitter release is evoked by action potentials rather than being tonic. In this article, we discuss recent work suggesting the possibility of mixed analogue–digital signal- Dominique Debanne, Andrzej Bialowas and Sylvain Rama ling at local axonal connections in CNS cir- cuits, with an emphasis on the hippocampus. Abstract | Synaptic transmission in the brain generally depends on action This has important and exciting implications potentials. However, recent studies indicate that subthreshold variation in the for our understanding of information presynaptic membrane potential also determines spike-evoked transmission. processing in this part of the brain. The informational content of each presynaptic action potential is therefore greater than initially expected. The contribution of this synaptic property, Analogue and digital signalling Synapses translating analogue presynap- which is a fast (from 0.01 to 10 s) and state-dependent modulation of functional tic membrane potential fluctuation into coupling, has been largely underestimated and could have important graded tonic release of transmitter display consequences for our understanding of information processing in neural a significantly higher rate of information networks. We discuss here how the membrane voltage of the presynaptic transfer than synapses using presynaptic terminal might modulate neurotransmitter release by mechanisms that do not spike train coding. The dynamic range at involve a change in presynaptic Ca2+ influx. tonic-release, analogue synapses is indeed very large, and a single analogue synapse is able to continuously encode virtually The principal function of the CNS is to is actively propagated along the axon. infinite information levels. For instance, adapt an organism’s behaviour to changes in Neuronal information is therefore transmit- graded synapses in the fly retina trans- the environment — a process that is thought ted to the postsynaptic neuron as discrete mit more than 1,500 bits of information to be mediated by modulation of neuronal amounts of neurotransmitter released by the per second: that is, one or two orders of circuits through synaptic modifications. presynaptic neuron in an all-or-none mode. magnitude larger than spiking neurons8,9. Understanding the cellular and molecular This mode of neuronal signalling is thus However, this comes at the price of mechanisms underlying activity-dependent ‘digital’: the neuron either fires or it does high energy consumption. For example, regulation of synaptic strength is therefore not, and neurotransmitter release follows photoreceptors in the retina continuously a major issue in neurobiology. Recent work this binary mode (FIG. 1a). release their neurotransmitter at a high rate indicates that in addition to changes in post- However, neuronal information is not (20–80 vesicles per active zone per second), synaptic receptor expression and synaptic only transmitted digitally, and subthreshold indicating that each active zone may release vesicle release probability, synaptic strength activity that originates in the dendrites and as many as a few million vesicles per day10. in mammalian neurons is regulated by reaches the soma can be conveyed along the Another drawback of analogue signalling subthreshold variations of voltage that are axon to the presynaptic element, in which it is that it is constrained by biophysical laws generated far from the synapse1–4. influences the arriving action potential and such as voltage dissipation along neuronal In most neurons, the proximal region of thus tunes the flow of neuronal information processes over long distances. Therefore, the axon (the axon initial segment (AIS)) via ‘analogue’ coding. Clear examples of pure analogue signalling in neurons is contains a high density of Na+ channels, and analogue transmission of neuronal infor- better suited for local rather than distal is therefore a hotspot for neuronal excita- mation can be found in the inner ear or in transmission of information. tion. Small synaptic potentials that are gen- the retina, in which photoreceptors, bipolar By contrast, digital synapses are able erated in the dendrites summate temporally, and horizontal cells signal photostimula- to signal activity far from the site of spike and if the resulting potential reaches the tion by producing graded potentials with- initiation because neuronal information threshold for action potential generation, out action potentials6. These cells generally encoded in the form of action potentials a spike is initiated at the AIS. According to release transmitter continuously (tonic is carried over very long distances along this view, the AIS is the final site for den- release), and their high rate of spontaneous axons without voltage dissipation, as active dritic integration of synaptic responses5, release is directly modulated by membrane currents regenerate action potentials along which produces an action potential that potential fluctuations (FIG. 1b). Similar the axon11,12. Another major advantage of Digital Analogue AD a b c Pre TH EPSC Post d Vm soma = –65 mV b1 b2 Vm soma = –45 mV –45 mV Vm –65 mV Axonal distance AD Digital Figure 1 | Digital, analogue and hybrid (analogue–digital) modes c | Hybrid analogue–digital (AD) transmission. Both subthreshold fluc- Nature Reviews | Neuroscience of synaptic transmission. a | Digital mode of synaptic transmission tuations (red trace) and spiking activity (upper black trace) are transmit- in the CNS. A scheme of two synaptically connected neurons is shown ted. Note that when the presynaptic spike is produced after a prolonged on the left. Transmission (right) is stereotyped and occurs in an period of depolarization (red trace), the spike-evoked synaptic response all-or-none (digital) manner (that is, only if a presynaptic action potential (blue trace) is enhanced compared with when there is no prolonged is elicited). Note that subthreshold depolarization (indicated by the depolarization (upper and lower black traces). d | Spatial gradient of arrowhead) produces neither a presynaptic spike nor a postsynaptic hybrid and digital transmission. Because of cable properties, AD trans- response. b | Analogue transmission is a graded mode of transmission of mission is restricted to proximal presynaptic boutons (b1), whereas pure presynaptic voltage fluctuations. The two horizontal dashed lines indi- digital transmission occurs at distal boutons (b2). EPSC, excitatory cate the baselines. The blue trace represents postsynaptic activity. postsynaptic current; TH, spike threshold; Vm, membrane voltage. digital signalling is its relatively low energy synapses, including cortical2,3,19, cerebel- that a voltage response decays exponentially cost. The kinetics of voltage-gated currents lar20,21 and hippocampal synapses1,22. In along passive cables. The space constant is underlying the action potential are tuned these examples, synaptic transmission the axonal distance for which voltage drops to minimize energetic consumption13,14. evoked by single action potentials is to 37% of its initial value. It depends on both Therefore, in many ways, digital signalling enhanced as the result of analogue-medi- geometrical and electrical factors of the may appear to be an improvement on ana- ated depolarization (10–30 mV) of the pre- axon: the axon membrane resistance, which logue signalling. However, it has also several synaptic element for a few tens to hundreds is determined by the relative contribution limitations. Because of its discrete nature, of milliseconds (FIG. 1c). of conducting (pore-forming proteins) and the coding of information by a single digital non-conducting (lipids) molecules, and synapse is generally poor in comparison Voltage propagation in axons axial resistance, which is controlled by the with analogue synapses. Thus, combining A prerequisite for analogue–digital intra-axonal medium and the axon diam- analogue and digital signalling should in facilitation (ADF) is that analogue voltage eter. Thus, a large space constant is generally principle offer a balance between the dual changes produced in the somatodendritic obtained for low intra-axonal resistance or advantages low energy cost and highly regions are capable of spreading along the
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