Abstract
The correlation of neuronal activity with sensory input and behavioural output has revealed that information is often encoded in the activity of many neurons across a population, that is, a neural population code is used1,2. The possible algorithms that downstream networks use to read out this population code have been studied by manipulating the activity of a few neurons in a population3,4. We have used this approach to study population coding in a small network underlying the leech local bend, a body bend directed away from a touch stimulus5. Because of the small size of this network we are able to monitor and manipulate the complete set of sensory inputs to the network. We show here that the population vector6 formed by the spike counts of the active mechanosensory neurons is well correlated with bend direction. A model based on the known connectivity of the identified neurons in the local bend network can account for our experimental results, and is suitable for reading out the neural population vector. Thus, for the first time to our knowledge, it is possible to link a proposed algorithm for neural population coding with synaptic and network mechanisms in an experimental system.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
References
Sparks, D. L., Kristan, W. B. Jr & Shaw, B. K. in Neurons, Networks, and Motor Behavior (eds Stein, P. S. G., Grillner, S., Selverston, A. I. & Stuart, D. G.) 21–32 (MIT Press, Cambridge, MA, (1997)).
Geogopoulos, A. New concepts in generation of movement. Neuron 13, 257–268 (1994).
Lee, C., Rohrer, W. H. & Sparks, D. L. Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357–360 (1988).
Groh, J., Born, R. & Newsome, W. How is a sensory map read out? Effects of microstimulation in visual area MT on saccades and smooth pursuit eye movements. J. Neurosci. 17, 4312–4330 (1997).
Kristan, W. B. J, McGirr, S. J. & Simpson, G. V. Behavioural and mechanosensory neurone responses to skin stimulation in leeches. J. Exp. Biol. 96, 143–160 (1982).
Georgopoulos, A. P., Schwartz, A. B. & Kettner, R. E. Neuronal population coding of movement direction. Science 233, 1416–1419 (1986).
Kristan, W. B. J Sensory and motor neurones responsible for the local bending response in leeches. J. Exp. Biol. 96, 161–180 (1982).
Lockery, S. R. & Kristan, W. B. J Distributed processing of sensory information in the leech. II. Identification of interneurons contributing to the local bending reflex. J. Neurosci. 10, 1816–1829 (1990).
Lewis, J. E. From Touch Localization to Directed Behavior: Neural Computation in the LeechThesis (Univ. California, San Diego, San Diego, CA, (1997)).
Carlton, T. & McVean, A. The role of touch, pressure and nociceptive mechanoreceptors of the leech in unrestrained behaviour. J. Comp. Physiol. A 177, 781–791 (1995).
Lockery, S. R. & Kristan, W. B. J Distributed processing of sensory information in the leech. I. Input-output relations of the local bending reflex. J. Neurosci. 10, 1811–1815 (1990).
Salinas, E. & Abbott, L. F. Vector reconstruction from firing rates. J. Comp. Neurosci. 1, 89–107 (1994).
Miller, J. P., Jacobs, G. A. & Theunissen, F. E. Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons. J. Neurophyiol. 66, 1680–1689 (1991).
Abbott, L. F. Decoding neuronal firing and modeling neural networks. Q. Rev. Biophys. 27, 291–331 (1994).
Salzman, C. D. & Newsome, W. T. Neural mechanisms for forming a perceptual decision. Science 264, 231–237 (1994).
Lockery, S. R., Wittenberg, G., Kristan, W. B. J & Cottrell, G. W. Function of identified interneurons in the leech elucidated using neural networks trained by back-propagation. Nature 340, 468–471 (1989).
Salinas, E. & Abbott, L. F. Transfer of coded information from sensory to motor networks. J. Neurosci. 15, 6461–6474 (1995).
Gur, M., Beylin, A. & Snodderly, D. M. Response variability of neurons in primary visual cortex (V1) of alert monkeys. J. Neurosci. 17, 2914–2920 (1997).
Shaw, B. K. & Kristan, W. B. J The neuronal basis of the behavioral choice between swimming and shortening in the leech: control is not selectively exercised at higher circuit levels. J. Neurosci. 17, 786–795 (1997).
Muller, K. J., Nicholls, J. G. & Stent, G. S. Neurobiology of the Leech (Cold Spring Harbor Laboratory Press, New York, (1981)).
Batschelet, E. Circular Statistics in Biology (Academic, New York, (1981)).
Lockery, S. R. & Sejnowski, T. J. Distributed processing of sensory information in the leech. III. A dynamical neural network model of the local bending reflex. J. Neurosci. 12, 3877–3895 (1992).
Acknowledgements
We thank M. Courtemanche, S. Kealey, T. Lewis and K. Moortgat for comments on the manuscript. This work was supported by a research grant from NIMH to W.B.K. and a NRSA graduate fellowship from NIMH to J.E.L.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lewis, J., Kristan, W. A neuronal network for computing population vectors in the leech. Nature 391, 76–79 (1998). https://doi.org/10.1038/34172
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/34172
This article is cited by
-
Transcriptional profiling of identified neurons in leech
BMC Genomics (2021)
-
Synergistic population coding of natural communication stimuli by hindbrain electrosensory neurons
Scientific Reports (2021)
-
Behavioral analysis of substrate texture preference in a leech, Helobdella austinensis
Journal of Comparative Physiology A (2019)
-
Effects of Touch Location and Intensity on Interneurons of the Leech Local Bend Network
Scientific Reports (2018)
-
Neural Representations Observed
Minds and Machines (2018)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.