Skip to main content

Advertisement

Log in

The Probabilistic Cell: Implementation of a Probabilistic Inference by the Biochemical Mechanisms of Phototransduction

  • Regular Article
  • Published:
Acta Biotheoretica Aims and scope Submit manuscript

Abstract

When we perceive the external world, our brain has to deal with the incompleteness and uncertainty associated with sensory inputs, memory and prior knowledge. In theoretical neuroscience probabilistic approaches have received a growing interest recently, as they account for the ability to reason with incomplete knowledge and to efficiently describe perceptive and behavioral tasks. How can the probability distributions that need to be estimated in these models be represented and processed in the brain, in particular at the single cell level? We consider the basic function carried out by photoreceptor cells which consists in detecting the presence or absence of light. We give a system-level understanding of the process of phototransduction based on a bayesian formalism: we show that the process of phototransduction is equivalent to a temporal probabilistic inference in a Hidden Markov Model (HMM), for estimating the presence or absence of light. Thus, the biochemical mechanisms of phototransduction underlie the estimation of the current state probability distribution of the presence of light. A classical descriptive model describes the interactions between the different molecular messengers, ions, enzymes and channel proteins occurring within the photoreceptor by a set of nonlinear coupled differential equations. In contrast, the probabilistic HMM model is described by a discrete recurrence equation. It appears that the binary HMM has a general solution in the case of constant input. This allows a detailed analysis of the dynamics of the system. The biochemical system and the HMM behave similarly under steady-state conditions. Consequently a formal equivalence can be found between the biochemical system and the HMM. Numerical simulations further extend the results to the dynamic case and to noisy input. All in all, we have derived a probabilistic model equivalent to a classical descriptive model of phototransduction, which has the additional advantage of assigning a function to phototransduction. The example of phototransduction shows how simple biochemical interactions underlie simple probabilistic inferences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Baylor DA, Matthews G, Yau KW (1980) Two components of electrical dark noise in toad retinal outer segments. J Physiol 309:591-621

    Google Scholar 

  • Bessière P, Laugier C, Siegwart R (eds) (2008) Probabilistic reasoning and decision making in sensory-motor systems (Springer tracts in advanced robotics). Springer

  • Burkhardt DA (1994) Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. J Neurosci 14(3 Pt 1):1091–1105

    Google Scholar 

  • Burns ME, Baylor DA (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annu Rev Neurosci 24:779–805

    Article  Google Scholar 

  • Burns ME, Lamb TD (2004) Visual transduction by rod and cone photoreceptor, vol 1. MIT Press, Chap 16, pp 215–233

  • Chichilnisky EJ, Rieke F (2005) Detection sensitivity and temporal resolution of visual signals near absolute threshold in the salamander retina. J Neurosci 25(2):318–330

    Article  Google Scholar 

  • Colas F, Droulez J, Wexler M, Bessière P (2007) A unified probabilistic model of the perception of three-dimensional structure from optic flow. Biol Cybern 97(5):461–477

    Article  Google Scholar 

  • Deneve S (2008) Bayesian spiking neurons: inference. Neural Comput 20(1):91–117

    Article  Google Scholar 

  • Dizhoor AM, Hurley JB (1999) Regulation of photoreceptor membrane guanylyl cyclases by guanylyl cyclase activator proteins. Methods 19(4):521–531

    Article  Google Scholar 

  • Doya K, Ishii S, Pouget A, Rao RPN (eds) (2007) Bayesian brain: probabilistic approaches to neural coding. The MIT Press, Cambridge

    Google Scholar 

  • Ernst MO, Banks MS (2002) Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415(6870):429–433

    Article  Google Scholar 

  • Fain GL, Matthews HR, Cornwall MC, Koutalos Y (2001) Adaptation in vertebrate photoreceptors. Physiol Rev 81(1):117–151

    Google Scholar 

  • Frings S (2009) Primary processes in sensory cells: current advances. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 195(1):1–19

    Article  Google Scholar 

  • Gold JI, Shadlen MN (2002) Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and reward. Neuron 36(2):299–308

    Article  Google Scholar 

  • Hamer RD, Nicholas SC, Tranchina D, Lamb TD, Jarvinen JL (2005) Toward a unified model of vertebrate rod phototransduction. Vis Neurosci 22(4):417–436

    Article  Google Scholar 

  • Hodgkin AL, Nunn BJ (1988) Control of light-sensitive current in salamander rods. J Physiol 403:439–471

    Google Scholar 

  • Jaynes ET (2003) Probability theory: the logic of science. Cambridge University Press, Cambridge

    Google Scholar 

  • Knill DC, Richards W (eds) (2008) Perception as Bayesian inference, 1st edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Koch KW, Stryer L (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334(6177):64–66

    Article  Google Scholar 

  • Körding KP, Wolpert DM (2004) Bayesian integration in sensorimotor learning. Nature 427(6971):244–247

    Article  Google Scholar 

  • Koutalos Y, Nakatani K, Yau KW (1995) The cgmp-phosphodiesterase and its contribution to sensitivity regulation in retinal rods. J Gen Physiol 106(5):891–921

    Article  Google Scholar 

  • Laurens J, Droulez J (2007) Bayesian processing of vestibular information. Biol Cybern 96(4):389–404

    Article  Google Scholar 

  • Ma WJJ, Beck JM, Latham PE, Pouget A (2006) Bayesian inference with probabilistic population codes. Nat Neurosci 9(11):1432–1438

    Article  Google Scholar 

  • Marr D (1982) Vision: a computational investigation into the human representation and processing of visual information. The MIT Press, Cambridge

    Google Scholar 

  • Nikonov S, Lamb TD, Pugh EN (2000) The role of steady phosphodiesterase activity in the kinetics and sensitivity of the light-adapted salamander rod photoresponse. J Gen Physiol 116(6):795–824

    Article  Google Scholar 

  • Perlman I, Normann R (1998) Light adaptation and sensitivity controlling mechanisms in vertebrate photoreceptors. Prog Retin Eye Res 17(4):523–563

    Article  Google Scholar 

  • Pugh EN, Lamb TD (1993) Amplification and kinetics of the activation steps in phototransduction. Biochim Biophys Acta 1141(2–3):111–149

    Article  Google Scholar 

  • Pugh EN, Duda T, Sitaramayya A, Sharma RK (1997) Photoreceptor guanylate cyclases: a review. Biosci Rep 17(5):429–473

    Article  Google Scholar 

  • Pugh EN, Nikonov S, Lamb TD (1999) Molecular mechanisms of vertebrate photoreceptor light adaptation. Curr Opin Neurobiol 9(4):410–418

    Article  Google Scholar 

  • Rabiner LR (1989) A tutorial on hidden markov models and selected applications in speech recognition. Proc IEEE 77(2):257–286

    Article  Google Scholar 

  • Rao RPN, Olshausen B, Lewicki MS (eds) (2002) Probabilistic models of the brain: perception and neural function, illustrated edition edn. The MIT Press, Cambridge

    Google Scholar 

  • Rieke F, Baylor DA (1996) Molecular origin of continuous dark noise in rod photoreceptors. Biophys J 71(5):2553–2572

    Article  Google Scholar 

  • Rieke F, Baylor DA (1998a) Origin of reproducibility in the responses of retinal rods to single photons. Biophys J 75(4):1836–1857

    Article  Google Scholar 

  • Rieke F, Baylor DA (1998b) Single-photon detection by rod cells of the retina. Rev Mod Phys 70(3):1027–1036

    Article  Google Scholar 

  • Sagoo MS, Lagnado L (1997) G-protein deactivation is rate-limiting for shut-off of the phototransduction cascade. Nature 389(6649):392–395

    Article  Google Scholar 

  • Shepherd GM (1991) Sensory transduction: entering the mainstream of membrane signaling. Cell 67(5):845–851

    Article  Google Scholar 

  • Sterling S (2004) How retinal circuits optimize the transfer of visual information, vol 1. MIT Press, Chap 17, pp 234–259

  • Torre V, Ashmore JF, Lamb TD, Menini A (1995) Transduction and adaptation in sensory receptor cells. J Neurosci 15(12):7757–7768

    Google Scholar 

  • van Hateren H (2005) A cellular and molecular model of response kinetics and adaptation in primate cones and horizontal cells. J Vis 5(4):331–347

    Google Scholar 

  • Weiss Y, Simoncelli EP, Adelson EH (2002) Motion illusions as optimal percepts. Nature Neurosci 5(6):598–604

    Article  Google Scholar 

  • Whitlock GG, Lamb TD (1999) Variability in the time course of single photon responses from toad rods: termination of rhodopsins activity. Neuron 23(2):337–351

    Article  Google Scholar 

  • Yang T, Shadlen MN (2007) Probabilistic reasoning by neurons. Nature 447(7148):1075–1080

    Article  Google Scholar 

  • Zemel RS, Dayan P, Pouget A (1998) Probabilistic interpretation of population codes. Neural Comput 10(2):403–430

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by European program BACS (Bayesian Approach to Cognitive Systems) FP&-IST-027140. We also thank Francis Colas for fruitful discussions and Michael Zugaro for giving helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Audrey Houillon.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Houillon, A., Bessière, P. & Droulez, J. The Probabilistic Cell: Implementation of a Probabilistic Inference by the Biochemical Mechanisms of Phototransduction. Acta Biotheor 58, 103–120 (2010). https://doi.org/10.1007/s10441-010-9104-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10441-010-9104-y

Keywords

Navigation