Review
Sensory systems

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Abstract

Our understanding of sensory systems has grown impressively in recent years as a result of intense efforts to characterize the mechanisms underlying perception. A large body of evidence has accrued regarding the processes through which sensory information at the biochemical, electrophysiological, and systems levels contributes to the conscious experience of a stimulus. Our efforts to understand the function of sensory systems have been aided by the development of new techniques, including powerful methods of molecular biology, refined short- and long-term approaches to recording from single and multiple neurons, and non-invasive neuroimaging techniques that allow us to study activity within the human brain while subjects perform a variety of cognitive tasks. In future research, the last approach is likely to form a bridge between the large body of electrophysiological knowledge acquired in animal experiments and that currently being obtained in human imaging research.

Introduction

Sensory systems perform a variety of common tasks. Each employs specialized peripheral receptors to respond to the environment, integrates the information derived simultaneously from different receptors, transmits information to central structures using a neural code, and eventually compares the result with sensations received in the past or those owing to other sensory systems. It is therefore hardly surprising that sensory systems share certain organizational principles, such as convergence and divergence, topographic projection, multiplicity of representation, parallel paths, stereotypical connectivity, and hierarchical organization.

In this anniversary issue, we selectively review four areas of sensory processing that have been intensively studied during the past decade of neuroscientific research: the transduction of sensory inputs, the nature of neural coding, the modular organization represented by parallel pathways and hierarchies of analysis, and the relation of sensory neural signals to the subjective processes of perceiving, deciding, and acting.

Section snippets

Chemical transduction

In the realm of sensory transduction, the 1990s were the decade of the nose. Years of slow but steady progress had earlier established the molecular analogy between olfactory transduction and phototransduction. Olfactory neuroscience then leapt forward following the identification of the missing piece of the puzzle, the large family of receptor molecules. In addition to clarifying the initial steps of olfactory transduction, this discovery has proven important for our understanding of

Conclusions

In this review, we have touched upon some basic principles shared by most sensory systems. A great deal of progress was made over the past ten years in the reviewed areas, but numerous questions concerning even the simplest organization principles of each modality remain await further investigation.

We do not know why so many topographically organized sensory areas are required. Why are there so many stages in the hierarchies of analysis? What is actually done at each level, and how are the

Acknowledgements

The authors thank S Smirnakis for comments on the manuscript. The original research from our laboratories is supported by National Institutes of Health grants DC00241 and DC00317 and by the Max-Planck-Gesellschaft. AJ Hudspeth is an Investigator of Howard Hughes Medical Institute.

References (125)

  • MN Shadlen et al.

    Noise, neural codes and cortical organization

    Curr Opin Neurobiol

    (1994)
  • G Buzsaki et al.

    Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks

    Curr Opin Neurobiol

    (1995)
  • P Konig et al.

    Correlated firing in sensory-motor systems

    Curr Opin Neurobiol

    (1995)
  • G Laurent

    Olfactory processing: maps, time and codes

    Curr Opin Neurobiol

    (1997)
  • R Ritz et al.

    Synchronous oscillatory activity in sensory systems: new vistas on mechanisms

    Curr Opin Neurobiol

    (1997)
  • S Nirenberg et al.

    Population coding in the retina

    Curr Opin Neurobiol

    (1998)
  • W Bair

    Spike timing in the mammalian visual system

    Curr Opin Neurobiol

    (1999)
  • LH Carney

    Temporal response properties of neurons in the auditory pathway

    Curr Opin Neurobiol

    (1999)
  • JR Schilling et al.

    Frequency-shaped amplification changes the neural representation of speech with noise-induced hearing loss

    Hear Res

    (1998)
  • JC Wong et al.

    Effects of high sound levels on responses to the vowel [Epsilon] in cat auditory nerve

    Hear Res

    (1998)
  • DV Smith et al.

    Neural coding of gustatory information

    Curr Opin Neurobiol

    (1999)
  • R Romo et al.

    Sensing and deciding in the somatosensory system

    Curr Opin Neurobiol

    (1999)
  • R Granger et al.

    Higher olfactory processes: perceptual learning and memory

    Curr Opin Neurobiol

    (1991)
  • VA Lamme et al.

    Feedforward, horizontal, and feedback processing in the visual cortex

    Curr Opin Neurobiol

    (1998)
  • CD Gilbert

    Plasticity in visual perception and physiology

    Curr Opin Neurobiol

    (1996)
  • KS Rockland et al.

    Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey

    Brain Res

    (1979)
  • MM Merzenich et al.

    Cochleotopic organization of primary auditory cortex in the cat

    Brain Res

    (1973)
  • MM Merzenich et al.

    Representation of the cochlear partition of the superior temporal plane of the macaque monkey

    Brain Res

    (1973)
  • JP Rauschecker

    Cortical processing of complex sounds

    Curr Opin Neurobiol

    (1998)
  • S Funahashi et al.

    Delay-period activity in the primate prefrontal cortex encoding multiple spatial positions and their order of presentation

    Behav Brain Res

    (1997)
  • J Bullier et al.

    Parallel versus serial processing: new vistas on the distributed organization of the visual system

    Curr Opin Neurobiol

    (1995)
  • C Dulac et al.

    A novel family of genes encoding putative pheromone receptors in mammals

    Cell

    (1995)
  • H Matsunami et al.

    A family of candidate taste receptors in human and mouse

    Nature

    (2000)
  • CI Bargmann

    Neurobiology of the Caenorhabditis elegans genome

    Science

    (1998)
  • H Zhao et al.

    Functional expression of a mammalian odorant receptor

    Science

    (1998)
  • T Leinders-Zufall et al.

    Ultrasensitive pheromone detection by mammalian vomeronasal neurons

    Nature

    (2000)
  • ER Troemel et al.

    Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans

    Cell

    (1996)
  • M Huang et al.

    Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans

    Nature

    (1994)
  • RG Walker et al.

    A Drosophila mechanosensory transduction channel

    Science

    (2000)
  • HA Colbert et al.

    OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans

    J Neurosci

    (1997)
  • G Gu et al.

    Genetic interactions affecting touch sensitivity in Caenorhabditis elegans

    Proc Natl Acad Sci USA

    (1996)
  • Manley G: Cochlear mechanisms from a phylogenetic viewpoint. Proc Natl Acad Sci USA 2000, in...
  • JE Gale et al.

    An intrinsic frequency limit of the cochlear amplifier

    Nature

    (1997)
  • J Zheng et al.

    Prestin is the motor protein of cochlear outer hair cells

    Nature

    (2000)
  • G Frank et al.

    Limiting dynamics of high-frequency electromechanical transduction of outer hair cells

    Proc Natl Acad Sci USA

    (1999)
  • P Dallos et al.

    High-frequency motility of outer hair cells and the cochlear amplifier

    Science

    (1995)
  • GK Yates et al.

    Cochlear electrically evoked emissions modulated by mechanical transduction channels

    J Neurosci

    (1998)
  • ME Benser et al.

    Rapid, active hair-bundle movements in hair cells from the bullfrog’s sacculus

    J Neurosci

    (1996)
  • P Martin et al.

    Active hair-bundle movements can amplify a hair cell’s response to oscillatory mechanical stimuli

    Proc Natl Acad Sci USA

    (1999)
  • S Nikonov et al.

    Kinetics of recovery of the dark-adapted salamander rod photoresponse

    J Gen Physiol

    (1998)
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