Encyclopedia of Computational Neuroscience

Living Edition
| Editors: Dieter Jaeger, Ranu Jung

Somatosensory Neurons: Spike Timing

  • Hannes SaalEmail author
Living reference work entry
DOI: https://doi.org/10.1007/978-1-4614-7320-6_387-2

Synonyms

Definition

A long-standing controversy in neural coding has been about whether the timing of individual action potentials (spikes) conveys information and is behaviorally relevant or whether information is instead transmitted simply by neurons’ firing rates. Both peripheral and cortical somatosensory neurons in primates can exhibit precisely timed action potentials in response to tactile stimuli, and there is a growing consensus that not only is some tactile information exclusively represented by such temporal codes but also that spike timing can shape tactile perception.

Detailed Description

Precisely Timed Responses of Cutaneous Mechanoreceptors to Skin Vibrations

In primates, rapidly adapting (RA) and Pacinian (PC) afferents entrain to medium- and high-frequency vibrations, respectively, in that their action potentials occur precisely within a given phase of each stimulus cycle (Talbot et al. 1968). Such precise timing can also be seen in the responses to diharmonic and noise stimuli (Muniak et al. 2007, see Fig. 1). PC responses are generally more precise than RA responses. Slowly adapting type I (SA1) afferents only respond weakly to vibrations, and their spikes are not precisely timed. Finally, the temporal patterning has been shown to be behaviorally relevant at a fine temporal resolution, by presenting different stimuli that elicit similar or the same firing rates and then test whether those are perceptually discriminable (Mackevicius et al. 2012). One behavior where skin oscillations are especially relevant is texture perception, where RA and PC afferents respond with precise temporal spiking patterns to texture-elicited skin vibrations (Weber et al. 2013).
Fig. 1

Responses of a PC afferent to sinusoidal, diharmonic, and bandpass noise stimuli. In each of the three panels, the top trace shows the time-varying position of the vibratory stimulus (with the three amplitudes marked to the right). The raster plots show the responses of a PC afferent to five repeated presentations of the stimulus at the three stimulus amplitudes. The bars to the right indicate the spike counts evoked on each stimulus presentation. While spike counts tend to change with stimulus amplitude, temporal patterning in the afferent response is more consistent across amplitudes. (Adapted from Mackevicius et al. (2012))

Peripheral Responses During Object Manipulation

Another temporal code might be active during object manipulation. When grasping an object, one needs to rapidly adapt grip forces depending on object properties to prevent slip or overgrasping. Information about object curvature and similar properties is encoded mostly by SA1 and RA afferents. It has been shown that in addition to firing rates, the first-spike latencies of SA1 and RA afferents are highly informative about object features. A neural code based on first-spike latencies could explain how tactile feedback is rapidly integrated into motor commands (grip force adjustments can occur within 100 ms) (Johansson and Birznieks 2004; Saal et al. 2009).

Spike Timing in Somatosensory Cortex

Whether spike timing matters in primate somatosensory cortex is more controversial. It is often assumed that even though peripheral afferents might exhibit precisely timed spikes, such temporal information might be converted into a rate code on the way to cortex. Thus, most work on somatosensory cortical neurons has focused on characterizing the makeup and extent of spatial receptive fields using firing rates. A notable exception concerns flutter stimuli (low-frequency vibrations in the range of 5–50 Hz), in response to which cortical somatosensory neuron both exhibit entrainment (phase-locking) and modulate their firing rates. However, changes in the perception of flutter stimuli align more closely with changes in the firing rates of cortical neurons rather than changes in their temporal profile, which has led to the conclusion that spike timing plays no role in the perception of flutter stimuli (Luna et al. 2005; Salinas et al. 2000). For high-frequency texture-like vibrations, however, a different picture emerges. For such stimuli, their amplitude is signaled in the slowly time-varying firing rates of cortical neurons, while their frequency content is transmitted by precisely timed action potentials (Harvey et al. 2013, see Fig. 2). Such a code is an instance of multiplexing, where different kinds of information are transmitted by different aspects of the neural response. Interestingly, information about amplitude and frequency is separated so well by these two different codes that some frequencies would be impossible to tell apart without, providing a strong argument that spike timing is indeed behaviorally relevant.
Fig. 2

Temporal patterning in cortical responses to sinusoidal stimulation. (a) Autocorrelations (top) and interspike interval histograms (bottom) for one neuron in area 3b, whose responses are entrained with the stimulus up to 800 Hz. (b) Phase histograms along with vector strength (r) for the same neuron as in (a) showing action potentials tended to occur during a restricted phase of each stimulus cycle. (c) Spectrograms for the same neuron as in (a), with corresponding power spectral densities (PSD) in the insets to the right. Note that the temporal patterning begins almost immediately and lasts for the duration of the stimulus and that the fundamental frequency in the neural response reflects the frequency of the sinusoid. (Adapted from Harvey et al. (2013))

Spike Timing and Attention

Spike timing across a population of neurons can also carry information. Specifically, attention modulates the synchrony of spikes of cortical somatosensory neurons (Steinmetz et al. 2000). Such a mechanism might enhance the saliency of attended stimuli by increasing the number of coincident spikes across the neural population.

Cross-References/Related Terms

References

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Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Organismal Biology and AnatomyUniversity of ChicagoChicagoUSA