RESPONSE VARIABILITY TO REPEATED MECHANICAL STIMULATION OF THE SKIN IN THE DORSAL COLUMN SYSTEM
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1 ACTA NEUROBIOL. EXP. 1986, 46: RESPONSE VARIABILITY TO REPEATED MECHANICAL STIMULATION OF THE SKIN IN THE DORSAL COLUMN SYSTEM Antti PERTOVAARA, Timo TUKEVA and Timo HUOPANIEMI Department of Physiology, University of Helsinki Siltavuorenpenger 20 J, Helsinki, Finland Key words: mechanoreceptor, periphery, cuneatus, response variability, cat Abstract. The response variability in the primary afferent fibers and in the post-synaptic neurons of the cuneatus was determined using repetitive mechanical stimulation of the skin in cat. The response variability was larger in the post-synaptic neurons. Of the two studied mechanoreceptor types, the RA (rapidly adapting) units had significantly more variability at the cuneate level than the PC (Pacinian) units, but at the peripheral level no such difference was found. The results suggest that the PC units transmit signals more securely through the cuneatus than the RA units. I I INTRODUCTION A repetitive application of a mechanical stimulus to the receptive field of a post-synaptic somatosensory neuron does not produce a constant response to each consecutive stimulus although the stimulus would remain constant. The response variability may be due to peripheral factors or to central factors. At the peripheral level the mechanical events at the skin (eg. incomplete creep recovery after the preceding stimulus) may cause changes in mechanorecelptor responsiveness during the course of closely spaced repeated stimulations (3, 10, 14, 15). At the central levels the transmission of impulses across the synaptic cleft is one source of variability, which may be especially important under anesthesia (5).
2 The aim of this study was to find out what is the contribution of peripheral and central factors to the response variability seen in the mechanoreceptive neurons of the dorsal column nuclei in the anesthetized cat. The second aim was to find out whether there are any differences in response variabilities of different mechanoreceptor types. A difference in response variability between separate post-synaptic neuron populations might indicate that the synaptic mechanislms in the ascending pathways are not identical; eg., under anesthesia, a larger response variability in one neuron population would suggest that a more complex temporal and spatial summation, possibly via interneurons, is needed to activate the post-synaptic neuron (1, 9). METHODS Experiments were performed in adult cats anesthetized with pentobarbital. The recordings of primary afferent fibers were made from the tibia1 nerve which innervates the glabrous foot pad of the hind leg. Fine strands were dissected from the nerve under the binocular microscope anld after cutting placed on a thin platinum-iridium wire for recording of unit activity (6). For the recordings of post-synaptic dorsal column system neurons, the cuneate nucleus was exposed by removing the atlas and a small part of the occipital region of the skull. A tracheotomy was performed and the animal was artificially ventilated as required to hold the end tidal PCoz at 3-4OIo. Extracellular impulse activity was recorded from individual neurons within the cuneate nucleus using glass- or lacquer-coated microelectrodes (0.5-5 M Q at 1 khz). Penetrations were made between 1 mm anterior and 3 mm posterior to the obex, and 1-3 mm lateral to the midline (13). Several criteria were used to identify post-synaptic cell discharge: tile distance along the penetration at which single spike could be recorded, the shape of the spike, a latency variation exceeding 150 ps, to brief electrical pulses applied at supraliminal intensities to the receptive field (13). All the primary afferent and post-synaptic neurons selected for the study had their receptive fields (or at least a prevailing part of it) positioned in the glabrous foot pad. The low threshmold mechanose~mitive units innervating the glabrous foot pad of the cat, can be classified into three groups according to the criteria used in earlier studies (4, 6): SA (slowly adapting) units (prolonged discharge to steady pressure), PC (Pacinian) units (large receptive fields with hard to define borders, response to remote tapping, entrainment by low-amplitude, high-frequency vibration), and RA (rapidly adapting) units (rapidly adapting units with small or medium size receptive fields and well defined bor-
3 ders). Only PC and RA units were included in the current sample of cells. None of the studied units gave prolonged responses to steady pressure. The stimulation procedure has been described in earlier studies (6, 13). The limb was fixed to the experimental table with pads facing up. The stimulus probe made of Perspex (diameter 2 mm) was,placed at the centre of the receptive field in the foot pad after determination of the unit type. The probe was adjusted to make a firm contact with the pad. The stimuli were short mechanical pulses (Fig. 1) delivered to the re- Fig. 1. Responses of a primary afferent neuron to a mechanical stimulus. The actual movement of the probe into the skin is depicted by the upward deflection from the base line. A, single stimulus; B, ten consecutive stimuli superimposed. The stimulus amplitude is 100 pm. The horizontal calibration bar represents 10 ms. ceptive field with the probe connected to an electromechanical vibrator (Bruel and Kjaer 4810). The vibrator was driven with single cycle sine waves from a function generator through a power amplifier. The frequency of the single cycle sine wave was 60 Hz. The actual movements of the probe were constantly monitored and measured with a piezoelectric accelerometer (Bruel and Icjaer 4371) positioned between the probe and the vibrator. The signals produced by the accelerometer were fed into a preamplifier with integrating circuits (Bruel and Kjaer 2635) for displacement measurements. The actual shape and amplitude of every stimulus could thus be controlled on a storage oscilloscope screen. The pulses were delivered to the skin at the frequency of 0.25 Hz, except when testing the effect of stimulus repetition rate. In these tests the stimulus repetition rate was varied between 0.25 and 0.5 Hz (cuneate neurons) or between 0.25 and 1.0 Hz (primary afferent neurons). The stimulus intensity was supraliminal for the tested neuron. The displacement value eliciting one or two impulses per stimulus, was chosen for further testing. After selection of the supraliminal stimulus value, this value was kept constant. The number of impulses elicited by each consecutive stimulus presentation was registered. Each test consisted of ten
4 consecutive stimulus presentations at the chosen repetition rate. The first few stimulus cycles of each test were not included in the analysis. Since the discharge frequency of the neurons may influence the response variability (17, 18, 19), a coefficient of variation (C.V.) derived from the mean impulse number per stimulus (2) and S.D. of the ten consecutive responses, was used als a measure olf the response variability: CV = SD/k The Mann-Whitney U-test was used in statistical comparisons. RESULTS Altogether 12 peripheral mechanoreceptive units were studied quantitatively. Of these 7 were PC units and 5 were RA units. The number of post-synaptic neurons recorded in the cuneatus was 10, of which 4 were PC units and 6 were &A units. All neurons had their receptive fields in the glabrous skin of the foot pad. The coefficient of variation (CV) in the post-synaptic neurons was significantly larger both in the PC unit population (P < 0.02) and in the RA unit population (P < 0.002) than in the respective primary afferent neuron populations (Fig. 2). When the two types of mechanoreceptor populations were compared to each other, it was found that at the peri- CUPiEATUS PERIPHERY Fig. 2. Variability coefficient (CV) in post-synaptic neurons of the cuneatus and in the primary afferent neurons. CV = SDJmean impulse number per stimulus.
5 PERIPHERY f CUNEATUS 0 RA Repetition rate [ HZ] Fig. 3. Effect of stimulus repetition rate (abscissae) on response variability (CV on ordinate) in post-synaptic neurons of the cuncatus and in the primary afferent neurons. pheral level there was no significant difference in CV between the two populations. However, at the cuneate level the postsynaptic RA neurons had significantly more response variability than the post-synaptic PC neurons (P < 0.005). An in'crease of stimulus repetition rate, from 0.25 to 0.50 Hz produced an increase in response variability in most post-synaptic neurons (Fig. 3). In contrast, most of the primary afferent neurons had response variability which was iadepe,ndent of the stimulus repetition rate, when the repetition rate was varied between 0.25 and 1.0 Hz. DISCUSSION The results of this study indicate that the response variability seen in the post-synaptic mechanoreceptive neurons of the cuneatus can be due both to peripheral factors (mechanical events at the skin; 14, 15) and to synaptic factors (5). The contribution of synaptic factors is greater. Interestingly, the two studied mechanoreceptor types (PC and RA) differed in the amount of response variability at the cuneate level but not at the peripheral level. Perhaps the activation of the post-synaptic RA units in the cuneatus requires more complex temporal and spatial
6 summation and a contribution of the cuneate interneurons, which under anesthesia could result i~n a larger response variability. It may also be that the studied RA neurons were third-order cells belonging to the dorsal column post-synaptic pathway (ll), and polysynaptically mediated signals are more variable. Previous recordings indicate that PC units are high-velocity sensitive mechanoreceptors (4, 6, 7, 9, 16). A recent psychophysical study indicated that different neural circuits are employed for coding the details of the stimulus waveform and indentation, and for signalling the occurrence of a rapid stimulus (8). It may be very important for an animal to know securely that a high-velocity stimulus has taken place. According to the present results PC units provide a secure pathway for signalling the occurrence of a stimulus with a steep onset. The response variability was increased with increasing stimulus repetition rate in moist post-synaptic neurons in contrast to primary afferent neurons. Interestingly, Armett and her co-workers (2) reported that the response variability of mechanoreceptor responses in the spinal dorsal horn was decreased with increasing repetition rate of the stimulus. However, the range of repetition rates in their study was between 1 and 10 Hz, whereas in the current study it was between 0.25 and 0.5 Hz (post-synaptic neurons) or between 0.25 and 1.0 Hz (primary afferents). Moreover, although some of the spinal dorsal horn neurons do project to the dorsal column nuclei (ll), it is not known whether the neurons described by Armett et al. (2) belonged to the dorsal column system. The marked progressive diminution of impul~se discharge in the primary afferent neurons during the first few cycles of stimulation (3, 7, 10, 12, 14, 15) did not contribute to the current results, since the first few cycles were not included in the data analysis. If the first few cycles had been included in the analysis, the response variability both in the primary afferent and cuneate neurons would have been somewhat larger. Werner and Mountcastle (17, 18), and Whitsel and his co-workers (19) in their extensive studies on the role of response variability in the coding of somatosensory information, used variance in impulse intervals as the studied parameter. In the present investigation the variance in the number of impulses per stimulus was used as the studied parameter, which makes comparisons to the results of Werner and Mountcastle (17, 18) and Whitsel et al. (19) difficult. Anyhow, their results and those of this study emphasize that the response variability is an important factor which should not be neglected in investigations on coding of somatosensory information. This investigation was supported by a grant from the Paulo Foundation, Hel. sinki, Finland.
7 REFERENCES 1. ANDERSEN, P., ECCLES, J. C., OSHIMA, T. and SCHMIDT, R. F Mechanisms of synaptic trarlsmission in the cuneate nucleus. J. Neurophysiol. 27: ARMETT, C. J., GRAY, J. A. B., HUNSPERGER, R. W. and LAL, S The transmission of information in primary receptor neurones and second-order neurones of a phasic system. J. Physiol. (Lond.) 164: BARKER, D. J., SHEPARD, P. D. and McDERMOTT, K. L Fatigue in cat facial mechanoreceptors. Neurosci. Lett. 30: DYKES, R. W Parallel processing of somatosensory information: a theory. Brain Res. Rev. 6: GALINDO, A Effects of procaine, pentobarbital and halothane on synaptic transmission in the central nervou's system. J. Pharmacol. Exp. Ther. 169: HAMALAINEN, H. and PERTOVAARA, A Liminal and supraliminal response characteristics of mechanoreceptors of the hairy and foot pad skin of cat determined with short tactile pulses. Quart. J. Exp. Physiol. 68: HAMALAINEN, H. and PERTOVAARA, A Vibrotactile thresholds in mechanoreceptive afferents innervating the foot pad of the cat. Acta Physiol. Scand. 120: HORCH, K. W., TUCKETT, R. P. and BURGESS, P. R Rapid displacements of th'e skin lack clear positional information. Brain Res. 309: JANIG, W., SCHULTZ, T. and SPENCER, W. A Temporal and spatial parameters of excitation and afferent inhibition in cuneothalamic relay neurons. J. Neurophysiol. 40: LINDBLOM, U Properties of touch rece,ptors in distal glabrous skin of the monkey. J. Neurophysiol. 28: LU, G.W., BENNETT, G. J., NISHIKAWA, N., HOFFERT, M. J. and DUBNER, R Extra- and intracellular recordings from dorsal column postsynaptic spinomedullary neurons in the cat. Exp. Neurol. 82: PERTOVURA, A. and HAMALAINEN, H. '1981.,Vibrotactile thresholds in non-pacinian mechanoreceptive afferents: the importance of temporal parameters. Acta Physiol. Scand. 113: PERTOVAARA, A., HUOPANIEMI, T. and TUKEVA, T Lirninal and supraliminal response characteristics of mechanoreceptive neurons in the cuneate nucleus of cat. Exp. Brain Res. 62: PUBOLS, Jr., B. H Factors affecting cutaneous mechanoreceptor response. I. Constant-force ver'sus constant-displacement stimulation. J. Neurophysiol. 47: PUBOLS, Jr., B. H Factors affecting cutaneous mechanoreceptor response. 11. Changes in mechanical properties of skin with repeated stimulation. J. Neurophysiol. 47: TALBOT, W. H., DARIAN-SMITH, I., KORNHUBER, H. H., MOUNTCASTLE, V. B The sense of flutter-vibration: comparison of the human capacity with res,pon,se patterns of mechanoreceptive afferents from the monkey hand. J. Neurophysiol. 31: WERNER, G. and MOUNTCASTLE, V. B The variability of central neural
8 activity in a sensory system, and its implications for the central reflection of sensory events. J. Neurophysiol. 26: WERNER, G. and MOUNTCASTLE, V. B Neural activity in mechanoreceptive cutaneous afferents: stimulus-response relations, Weber functions, and information transmission. J. Neurophysiol. 28: WHITSEL, B. L., SCHREINER, R. C. and ESSICK, G. K An analysis of variability in somatosensory cortical neuron discharge. J. Neurophysiol. 40: Accepted 12 March 1986
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