Stochastic resonance within the somatosensory system: effects of noise on evoked field potentials elicited by tactile stimuli

Abstract

Stochastic resonance (SR) is commonly understood to be the enhancement, by noise, of the response of a system to a weak input signal. The aim of this study was to demonstrate the occurrence of SR in spinal and cortical evoked field potentials (EFPs) elicited by periodic tactile stimuli in the anesthetized cat. The electrodes were positioned in spinal and cortical somatosensory regions in which the largest negative EFPs were detected. The periodic tactile stimuli consisted of local skin displacements on the central pad of the hindpaw. Two series of experiments were performed. First, periodic tactile stimuli and the noisy tactile stimuli were applied with the same indenter. Second, noisy tactile stimuli were applied with an additional indenter placed on the glabrous skin of the third hindpaw digit. This last protocol ensured that the signal and noise were mixed not in the skin but in the somatosensory regions of the CNS. All cats showed distinct SR behavior at the spinal and cortical stages of the sensory encoding. Such SR was abolished in the cortical but not in the spinal recording after sectioning of the dorsal columns and the ipsilateral dorsolateral funiculus. This suggests that the spinal neurons may also contribute to the SR observed at the cortical level. To the best of our knowledge, this is the first documented evidence that such a remarkable phenomenon embodies electrical processes of the spinocortical somatosensory system itself.

Fig. 1.

A, Scheme of the experimental arrangement. For the first protocol, the periodic and noisy tactile stimuli were applied with the same indenter. B, Records of the input signal and the spinal and cortical evoked potentials.C, Records with the same format as that inB: input noise alone and the simultaneously recorded spinal and cortical activity (output) for one level of noise, ς_n = 1.2 mN. D, Mean N-wave amplitude of the spinal cord dorsum potential versus test stimulus strength. E, Power spectrum of the input noise illustrated in C. The inset inE shows the amplitude distribution of the input noise.Ans, Ansate sulcus; au, arbitrary units;Cru, cruciate sulcus; Stim., stimulus;xT, times threshold.

Fig. 2.

A, Representative power spectra of the input periodic signal plus noise (traces inred) and noise alone (traces inblue) for three different levels of noise. In each case, ς_n indicates the SD of the input noise.B, C, Plots with the same format as that inA but for the simultaneously recorded spinal and cortical activity elicited by the stimuli illustrated in theinsets of 2A. Theinsets in A–C show typical recordings from which the power spectra were calculated. D, Formulas of SNR and R_info.S(f) corresponds to the power spectrum of the output neuronal activity (spinal or cortical) elicited by the periodic stimuli (2.5 Hz) plus noise. N(f) is the power spectrum of the output neuronal activity (spinal or cortical) elicited by noise alone. E, F, Output SNR (circles) and R_info(triangles) versus ς_n for one cat. E, Spinal (open symbols) output SNR and R_info versus ς_n. F, Cortical (filled symbols) output SNR andR_info versus ς_n. These results were obtained from experiments with the first protocol.au, Arbitrary units.

Fig. 3.

A, Scheme of the experimental arrangement. For the second protocol, the noise and signal stimuli arrive at the dorsal horn via separate pathways. This protocol ensured that the signal and noise were mixed not in the skin but in the somatosensory regions of the CNS. The electrodes were positioned in spinal and cortical somatosensory regions in which the largest EFPs were detected. Drawings in B andC are histological reconstructions of the electrode tracks within the dorsal horn at L6 and within the S1 somatosensory cortex. D–G, Averages (n = 32) of spinal and cortical EFPs recorded at intraspinal and intracortical depths, as indicated in B and C.D, Averages of spinal and cortical EFPs in control conditions (ς_n = 0). E–G, Averages of spinal and cortical EFPs for three different levels of noise (i.e., signal plus noise, ς_n = 0.75, ς_n = 2.01, ς_n = 4.7).H, Facilitation of spinal EFPs (amplitude) versus ς_n for one experiment. The dashed line represents the magnitude of a 95% confidence interval. Amplitude of EFPs was measured as indicated by thearrows in F. I, The same as H but for cortical EFPs. Ans, Ansate sulcus; Cru, cruciate sulcus.

Fig. 4.

Spinal (A) and cortical (B) output SNR versus ς_nfor three different cats (indicated by differentsymbols) in control conditions (before section).G, H, The same as A and B, but after section (at T12) of the DC and the IDLF illustrated inE and F. F,Drawings from the histological sections of the DC and IDLF at T12 obtained from three cats (indicated by differentsymbols). C and D andI and J are the same as Aand B and G and H but forR_info. Note that SR disappears in the cortical (filled symbols) but not in the spinal (open symbols) stages after section. These results were obtained from experiments with the second protocol.