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The Journal of Neuroscience, June 24, 2009, 29(25):8022-8031; doi:10.1523/JNEUROSCI.0665-09.2009

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Behavioral/Systems/Cognitive
Information about Complex Fingertip Parameters in Individual Human Tactile Afferent Neurons

Hannes P. Saal,¹ Sethu Vijayakumar,¹ and Roland S. Johansson²

¹Institute of Perception, Action and Behaviour, School of Informatics, University of Edinburgh, Edinburgh EH8 9AB, United Kingdom, and ²Physiology Section, Department of Integrative and Medical Biology, Umeå University, SE-901 87 Umeå, Sweden

Correspondence should be addressed to Hannes P. Saal, Institute of Perception, Action and Behaviour, School of Informatics, University of Edinburgh, Informatics Forum, 10 Crichton Street, Edinburgh EH8 9AB, UK. Email: h.saal{at}sms.ed.ac.uk

Although information in tactile afferent neurons represented by firing rates has been studied extensively over nearly a century, recent studies suggest that precise spike timing might be more important than firing rates. Here, we used information theory to compare the information content in the discharges of 92 tactile afferents distributed over the entire terminal segment of the fingertip when it was contacted by surfaces with different curvatures and force directions representative of everyday manipulations. Estimates of the information content with regard to curvature and force direction based on the precise timing of spikes were at least 2.2 times and 1.6 times, respectively, larger than that of spike counts during a 125 ms period of force increase. Moreover, the information regarding force direction based on the timing of the very first elicited spike was comparable with that provided by spike counts and more than twice as large with respect to object shape. For all encoding schemes, afferents terminating close to the stimulation site tended to convey more information about surface curvature than more remote afferents that tended to convey more information about force direction. Finally, coding schemes based on spike timing and spike counts overall contributed mostly independent information. We conclude that information about tactile stimuli in timing of spikes in primary afferents, even if limited to the first spikes, surpasses that contained in firing rates and that these measures of afferents' responses might capture different aspects of the stimulus.

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Received Feb. 9, 2009; revised May 14, 2009; accepted May 26, 2009.

Correspondence should be addressed to Hannes P. Saal, Institute of Perception, Action and Behaviour, School of Informatics, University of Edinburgh, Informatics Forum, 10 Crichton Street, Edinburgh EH8 9AB, UK. Email: h.saal{at}sms.ed.ac.uk

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