Deciphering the spike train of a sensory neuron: counts and temporal patterns in the rat whisker pathway

Abstract

Rats achieve remarkable texture discriminations by sweeping their facial whiskers along surfaces. This work explores how neurons at two levels of the sensory pathway, trigeminal ganglion and barrel cortex, carry information about such stimuli. We identified two biologically plausible coding mechanisms, spike counts and patterns, and used "mutual information" to quantify how reliably neurons in anesthetized rats reported texture when "decoded" according to these candidate mechanisms. For discriminations between surfaces of different coarseness, spike counts could be decoded reliably and rapidly (within 30 ms after stimulus onset in cortex). Information increased as responses were considered as spike patterns with progressively finer temporal precision. At highest temporal resolution (spike sequences across six bins of 4 ms), the quantity of "information" in patterns rose 150% for ganglion neurons and 110% for cortical neurons above that in spike counts. In some cases, patterns permitted discriminations not supported by spike counts alone.

Figure 1.

Texture stimuli and neuronal responses. A, Stimuli consisted of whisker trajectories previously recorded during free whisking and contact with five different surfaces. B, Simplified scheme of the sensory pathway. The primary afferent neuron has a cell body in the ganglion (1) and projects into the brainstem trigeminal nuclei (2). The second-order neuron projects to the contralateral thalamus (3). The thalamic neuron projects to barrel cortex (4). The data consist of ganglion and cortical activity. C, Spike trains recorded from ganglion (top row) and cortex (bottom row) in response to 10 randomly selected whisker sweeps along the CD surface (left column) and P280 sandpaper (right column). PSTHs below the raster plots represent summated activity across all 100 trials. The timescale corresponds to the two phases, protraction and retraction, of a 125 ms whisk cycle. Note that the cortical cluster responded during both phases of whisker movement and the ganglion cell only during retraction.

Figure 2.

Texture-specific spike counts. A, Cortical activity during five successive trials on two textures, CD (black) and P280 (gray). The scale under the bottom panel indicates the time from stimulus onset until T over which cumulative spike counts can be computed. B, Left, Distribution of whole-whisk spike counts measured from 100 presentations of CD (black) and P280 (gray). Right, Conditional probabilities of the two stimuli of interest given an observed value of spike count.

Figure 3.

Spike count information. A, Cumulative information carried by the cortical cluster during presentation of stimulus pair CD–P280 (left) and the total stimulus set (right). To highlight information accumulation in relation to the whisk cycle, the protraction phase is shaded. In this and all figures, time steps were 1 ms. B, Cumulative information carried by the ganglion cell during presentation of stimulus pair CD–P280 (left) and the total stimulus set (right, solid line). During the protraction phase (shaded), the cell carried no information. A second ganglion cell carried information only during whisker protraction (right, dashed line). C, Correlation between ganglion and cortex spike times (top trace), and correlation between the rate of ganglion and cortex information flow (bottom trace). D, Matrix of all pairwise information values for ganglion (top left) and cortex (bottom right). Circles indicate the stimulus pair P400–P1200. Note the different information scales for the two plots.

Figure 4.

Texture-specific spike patterns. A, Left, Ganglion activity during five successive trials on two textures, P1200 (black) and P400 (gray). The box outlines a 24 ms sliding window spanning 92 to 116 ms along the whisk cycle (see time axis below spike trains). The window is in turn subdivided into six bins of 4 ms. Middle, Spike counts during the indicated window did not distinguish between the stimuli. Right, Spike patterns during the same window, in which binary values indicate the presence or absence of a spike in each bin, discriminated between the stimuli. B, Distribution of observed spike patterns from 100 presentations of P1200 (black) and P400 (gray). “pattern #” refers to binary value of the 64 possible spike patterns. For each stimulus, the three patterns with the highest number of occurrences are illustrated with their corresponding conditional probabilities.

Figure 5.

Spike pattern information. A, Time course of spike pattern information about stimulus pair P1200–P400 (left) and the total stimulus set (right) for the ganglion cell. Each point reports information in the 24 ms window (6 bins of 4 ms) preceding the point. The horizontal arrow indicates the whole-whisk spike count information. B, Time course of spike pattern information about the stimulus pair P1200–P400 (left) and the total stimulus set (right) for the cortical cell cluster. Conventions as in A. C, For each stimulus pair, peak spike pattern information is indicated for the ganglion cell (top left) and the cortical cluster (bottom right). Stimulus pair P1200–P400, illustrated in A and B, is indicated by the circles. The ganglion cell carried errorless information about this and all stimulus pairs. The cortical cluster carried ∼0.7 bits. D, The gain in information available from the spike pattern compared with the whole-whisk spike count, for the ganglion cell (top left) and the cortical cluster (bottom right). These values result from the subtraction of the values in Figure 3D from those in C.

Figure 6.

Effect of internal clock precision on available information. A, Time course of the ganglion cell pattern information about stimulus pair P1200–P400 (left) and the total stimulus set (middle). Each plot refers to a different degree of internal clock precision; ΔT_internal is indicated simply as ΔT. Right, Peak spike pattern information about the total stimulus set as a function of internal clock precision (ΔT). B, Time course of the cortical cell cluster pattern information about the stimulus pair P1200–P400 (left) and the total stimulus set (middle). Conventions are the same as in A. Right, Peak spike pattern information about the total stimulus set as a function of internal clock precision (ΔT).

Figure 7.

Effect of external clock precision on available information. A, Time course of the ganglion cell pattern information about stimulus pair P1200–P400 (left) and the total stimulus set (middle). Each plot refers to a different degree of external clock precision; ΔT_external is indicated simply as ΔT. Right, Peak spike pattern information about the total stimulus set as a function of external clock precision (ΔT). B, Time course of the cortical cell cluster pattern information about stimulus pair P1200–P400 (left) and the total stimulus set (middle). Conventions are the same as in A. Right, Peak spike pattern information about the total stimulus set as a function of external clock precision (ΔT). To prevent the expanded time window (widened by the amount ΔT_external) from including spike patterns corresponding to the preceding stimulus, the analysis of the external clock precision was performed on the second whisk responses (see Materials and Methods). Information values corresponding to the first 24 ms of the whisk cycle are also excluded because they partially correspond to the late retraction phase of the preceding whisk cycle and are not specific to the second whisk. Slight differences with Figure 5, A and B, and the black traces of Figure 6 result from the fact that different whisks are analyzed.

Figure 8.

Count and pattern information for the full set of recorded neurons. A, Scatter plot of the whole-whisk spike count information versus peak spike pattern information about the full stimulus set for 10 ganglion single units (left) and 10 cortical clusters (right). The neurons analyzed in the preceding sections are indicated by arrows. Although they carried more information than average (red points), their ratio of pattern to count information was comparable with the rest of the dataset. B, Effect of both external clock precision (ΔT_external) and internal clock precision (ΔT_internal) on spike pattern information, averaged for the full set of ganglion (left) and cortical (right) neurons. From the surface plots, the interaction between the two clocks can be discerned.