Exp. Brain Res. 28,457-467 (1977)
Experimental Brain Research @ Springer-Verlag 1977
Neurones in the Spinal Trigeminal Nucleus of the Cat Responding to Movement of the Vibrissae D.W. Young I and A. Iggo Somatosensory Research Group, Department of Physiology,Royal (Dick) School of Veterinary Studies, Universityof Edinburgh, Summerhall,Edinburgh EH9 1QH, England
Summary. 1. In chloralose anaesthetised cats the receptive field organisation and response properties of neurones of the spinal trigeminal nucleus were examined and compared with the discharge characteristics of afferent units from vibrissae. 2. The response properties of the primary afferent discharges were preserved in at least a proportion of the second order cells, 82 % of those which responded to movements of the maxillary vibrissae had phasic discharges and 18 % had tonic discharges. 3. The discharge characteristics of the two main types of primary afferent slowly-adapting units (St I and St II) were distinguishable in the tonically active cells of the nucleus. These two groups showed (i) substantially different interspike interval distributions, (ii) different adaptive properties and (iii) different directional sensitivity. The two categories were designated nuclear type I and type II in accordance with the classification of primary afferent slowly-adapting units. 4. A loss of stimulus information was deduced from a consistent increase in the variability of the second order discharges compared with their presumed afferent input, but this information loss may be important in allowing the linear summation of discharges at the level of the thalamus. Key words: Trigeminal Nucleus - Vibrissae - Slowly-adapting Neurones
Introduction The vibrissae (maxillary sinus hairs) form an array of mobile sensors which effectively extend the facial skin surface for several centimetres. This specialised hair group is used extensively in exploration and orientation behaviour and is particularly well-developed among nocturnal animals. Acting in addition to the touch receptors of the facial skin and fur, the sensory receptors in sinus hair 1 Presentaddress: The Brain Research Institute, Universityof California,Los Angeles, California, 90024. USA
458
D.W. Youngand A. Iggo
follicles provide information relation to the position, velocity, amplitude, duration and direction of vibrissal movement. Four main types of afferent response can be distinguished in axons dissected from the infraorbital nerve, two rapidly-adapting and two slowly-adapting (Gottschaldt, Iggo and Young, 1973). This array of receptors can accommodate a wide spectrum of mechanical stimuli ranging from low amplitude vibrations at frequencies over 1000 Hz, to large sustained deflections of the sinus hair. The functional organisation of the spinal trigeminal nucleus has been the subject of several investiga.tions (Wall and Taub, 1962; Kruger and Michel, 1962; Darian-Smith et al., 1963), and the present investigation was directed at the representation of specific vibrissal afferents in the spinal trigeminal nucleus, and in particular to the tonic responses which have the potential of transmitting to the central nervous system information about sustained mechanical stimulation. We have, therefore, compared the responses from trigeminal neurones with the afferent discharges from vibrissal afferent fibres under quantitatively controlled conditions. A preliminary account of this work has been published (Young, 1975).
Methods
Preparation Twenty cats weighing between 1.9 and 4.5 kg were used. In nine experiments anaesthesia was induced with ethyl chloride and ether, followed by chloralose 65 mg/kg i.v. In a further eleven experiments anaesthesia was induced by a mixture of nitrous oxide, oxygen (2:1) and halothane (1.5-3.5%) delivered via a face mask, and maintained by chloralose, 65 mg/kg i.v. Small doses of sodium pentobarbital (12 mg/kg) were given later in the experiments, as required. Arterial blood pressure was continuously monitored and electrophysiological recordings were taken only when the mean value exceeded 90 mm Hg. Expired air was sampled continuously and the end-tidal CO2 concentration recorded. A thermostatically-controlled electric blanket held the rectal temperature between 36 and 38 ~ C. The surface of the medulla was exposed by occipital craniotomy and cervical laminectomy. The head was fixed in a stereotaxic head-holder; a tilt of 15-20 ~ around the ear-bar axis was necessary to place the brain-stem recording area in the horizontal plane and, in addition in smaller animals the dorsal process of an upper thoracic vertebra was clamped to prevent distortion of the recording site. A recording pool was formed by sewing the skin margins to a metal ring and covering the surface of the medulla with warm mineral oil.
Stimulation and Recording Procedures Electrical stimuli of 1-18 volts and 50 ~ts duration were applied to the skin of the face at the base of individual vibrissae as required.
Vibrissae Input to the TrigeminalNucleus
459
Recordings were made in the medulla using glass micro-pipettes broken to a tip diameter of 1-3 ~tm, with impedances ranging from 2-5 Mfl. Action potentials were recorded and stored on a 7-channel tape recorder or processed on-line using a PDP-12 computer. In some experiments the position of the recording site was marked by the iontophoretic deposition of pontamine sky-blue from the dye-filled recording electrode (HeUon, 1971). These marked positions were subsequently identified on 40 gm sections of the brain-stem stained with cresyl violet and luxol blue. Care was taken to eliminate recordings made in the underlying lateral reticular nucleus, which also receives trigeminal input. Primary afferent fibres of the descending trigeminal tract may be recorded throughout the spinal nucleus, but these could be distinguished on the basis of latency, spike shape and the absence of injury discharge on further advancement of the electrode. The collision method was not used, however, to verify the separation of units on these subjective criteria. Recording in a region from 7 mm rostral to 3 mm caudal of the obex and from 2.5-5.5 lateral of the mid-line, the somatotopic organization of the spinal trigeminal nucleus under chloralose anaesthesia was found to correspond closely to that described by Darian-Smith et al. (1963). The methods by which single units were investigated using controlled angular displacement of sinus hairs and the statistical criteria by which different categories were distinguished, have been fully described in a previous publication (Gottschaldt et al., 1973). Additional information about the responses of vibrissal afferent units were required to supplement published information and cats prepared as described by Gottschaldt et al. (1973), were used for this purpose.
Results
Single Cell Activity One hundred and thirty two neurones responding to movements of the maxillary sinus hairs were recorded over the entire rostro-caudal and vertical extent of the spinal trigeminal nucleus. Contrary to the results of Mosso and Kruger (1973), who used barbiturate anaesthesia, 40% of recorded cells discharged continuously in the absence of any stimulus, and also responded to movements of the facial fur or the vibrissae. The rate of spontaneous activity varied from cell to cell and was clearly affected by the level of anaesthesia, often slowing appreciably following the administration of sodium pentobarbitone (12 mg/kg). In eleven units the appearance of spikes in time was random, or near random, and the inter-spike interval histogram (probability density function) was approximately exponential with a dead-time of 2-3 msec. The rate of discharge of some units could accelerate or decelerate abruptly over periods of several seconds. This instability in the firing frequency was not apparently related to any injury of the cells involved as it could be observed over several hours.
460
D.W. Youngand A. Iggo
Electrically Evoked Activity Electrical stimuli were applied through bipolar electrodes to the bases of vibrissal follicles. About 50 % of the cells responded to these stimuli with a burst of 3-6 impulses with a latency to the first spike of 3-5 msec (mean 5.14 msec, mode 3.5 msec) in agreement with Darian-Smith et al. (1963) and Mosso and Kruger (1973). The early burst or single spike was, in about 50% of these cells, followed by a later burst at a latency of 12-30 msec.
Responses to Movement of Vibrissae
Phasic Responses One hundred and thirty-two cells responded to movements of the maxillary vibrissae, and were classified using the criteria developed for the afferent vibrissal units (Gottschaldt et al., 1973). 82% gave only a phasic discharge, in contrast to the smaller proportion (33%) of the afferent unit population. Forty-eight (36%) of these phasic trigeminal neurones entrained for brief periods by high frequency (440 Hz) vibratory mechanical stimulation of a vibrissa, but not by low frequency vibration (< 10 Hz). The high frequency of vibration required to activate these cells and the absence of any directional preference of vibration, suggested that they were activated by axons supplying the Golgi-Mazzoni corpuscles in the sinus hair follicle (Gottschaldt et al., 1973). The remaining phasically responding cells showed a wide range of velocity thresholds, (20-100~ often responding with several impulses during the rising phase of a slow ramp movement applied to the hair.
Tonic Responses The discharge characteristics o f the two main classes of slowly-adapting afferent units (StI and StII) found in the infraorbital nerve were preserved in 24 cells (18%) of the sample of spinal trigeminal neurones. Two categories of tonically-responding neurones could be differentiated on the basis of (1) the interspike interval distributions of their discharges, (2) their adaptive properties and (3) their directional sensitivity. These correspond to similar differences between the two classes of slowly-adapting afferent units. The two categories were therefore designated nuclear type I and type I1. These patterns of discharge were clear-cut, despite the fact that units showed convergence from more than one vibrissa and the neurones could therefore not have been activated exclusively by single afferent fibres. The patterns of discharge in two typical units are shown in Figure 1 as sequential interval plots (A, B) and as interspike interval histograms (C, D). Figure 1A shows the sequential interval plot of the discharge of a nuclear type I cell to a sustained 10~ deflection of a maxillary sinus hair, recorded immediately after completion of the initial movement. Both long and short intervals appear
Vibrissae Input to the Trigeminal Nucleus
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Fig. 1. The discharge patterns of tonic cells in the spinal trigeminal nucleus. A, B Successive interval plots where each successive interval is plotted against its position in the spike train. A nuclear type I discharge. B nuclear type II discharge. C, D Interspike interval histograms of bin width 1 ms illustrating the distribution of interval lengths. C nuclear type I discharge with a superimposed exponential function (solid line) of the same parameters. D nuclear type II discharge with a superimposed Gaussian distribution of the same parameters. Note that the graphs are plotted on different scales
in the discharge, and although there is a progressive increase in the mean interspike interval, as revealed by the sloping regression line fitted to the histogram, the long and short intervals are nearly randomly distributed. In five similar units adaptation was present even in relatively small samples of data (100 intervals). The activity of the other unit plotted in a similar fashion (Fig. 1B), displays a characteristically uniform sequential interval plot (typical of class II units) with interspike intervals deviating only slightly from the mean over 100 intervals. Interspike interval distribution histograms Of the same cells are shown in Figure C and D. The probability density function for interspike interval lengths for the type I cell during a sustained rostral deflection of a single vibrissa is similar to a Poisson distribution of intervals, with a 2-3 msec dead-time. The probability density functions were calculated using parameters derived from the interspike interval histograms.
462
D.W. Youngand A. Iggo
The part of the curve between 3 and 150 msec does not, however, accurately fit an exponential function of the same parameters (~ (x) = )~e-ax) as would be expected of a truly random process, where )~ is the mean firing rate. In contrast to Figure 1C the interspike interval distribution for the nuclear type II neurone in Figure 1D is Gaussian, although deviations from the fitted normal probability density function are just significant at the 5 % level. The range of coefficients of variation (mean/standard deviation) in 5 nuclear type I units was from 0.92-1.71 and in 6 nuclear type II units was from 0.177-0.76, in both cases much wider than the equivalent values for the respective StI and StII afferent units (Gottschaldt et al., 1973). For the 11 trigeminal neurones tested in this way the increase in variability compared with that of the two groups of primary afferent slowly-adapting discharges was about 20 %.
Order-Dependent Properties of the Tonic Neuronal Discharges The presence of serial dependence in the tonically active trigeminal cells was estimated by the joint interval density and the serial correlation coefficient and compared with similar data obtained in separate experiments from primary afferent fibres of the infraorbital nerve in anaesthetized animals. Figures 2A and C shows the joint interval densities of the nuclear type I discharge (2A) and nuclear type II units (2C) respectively. The interspike interval (td has been plotted against the following interval (t~+1) in the spike train. The joint interval density therefore represents the degree of dependence of one interval on the previous interval (Rodieck et al., 1962; Perkel et al., 1967a). Where there is a completely random appearance of spikes in time the points would be scattered over the range of intervals plotted and this condition is met, at least partially, by the nuclear type I discharges (Fig. 2A), but is clearly not the case in the nuclear type II discharge (Fig. 2C), where a tight clustering of points around the common mean of both axes indicates that an interval of length t is followed by an interval which is very close in length to t. One parameter of this relationship is the serial correlation coefficient of order one (91, Cox and Lewis, 1966). The analysis was extended to nonadjacent intervals to test dependencies over a longer period of time. The serial correlogram of 200 intervals of a nuclear type II unit discharge for 50 orders of lag that is, the values of 91-9so, gave some evidence of cyclical activity with a period of about 15 intervals, but none of the 50 coefficients reached statistical significance at the 5 % level. The nuclear type ! discharge also shows signs of periodicity over 3-4 intervals, but again no deviations of the serial correlation coefficients from zero were significant at the 5 % level. Similar investigations of the properties of the slowly-adapting primary afferent discharges from sinus hair follicle StI and StII afferent units produced the results illustrated by joint interval plots in Figures 2B, D. The only clear difference between the peripheral and nuclear tonic discharges subjected to these tests was a cyclical change in the serial correlation of the sinus hair type II afferent activity which was highly significant for adjacent and alternate intervals (91 and 9z).
Vibrissae Input to the Trigeminal Nucleus
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Adaptation Behaviour of Nuclear Type I and H Neurones I n the p r i m a r y afferent units there is a clear distinction b e t w e e n the time constants of adaptation of the type I and the type II slowly-adapting m e c h a n o r e c e p t o r s (Iggo and Muir, 1969; C h a m b e r s et al., 1972; Gottschaldt et al., 1973). A d a p t a t i o n in the trigeminal n e u r o n e s was generally faster than in the p r i m a r y afferents. T h e nuclear type I discharge was even less sustained t h a n the nuclear type II, as in the periphery.
464
D.W. Young and A. Iggo
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Experimental Brain Research @ Springer-Verlag 1977
Neurones in the Spinal Trigeminal Nucleus of the Cat Responding to Movement of the Vibrissae D.W. Young I and A. Iggo Somatosensory Research Group, Department of Physiology,Royal (Dick) School of Veterinary Studies, Universityof Edinburgh, Summerhall,Edinburgh EH9 1QH, England
Summary. 1. In chloralose anaesthetised cats the receptive field organisation and response properties of neurones of the spinal trigeminal nucleus were examined and compared with the discharge characteristics of afferent units from vibrissae. 2. The response properties of the primary afferent discharges were preserved in at least a proportion of the second order cells, 82 % of those which responded to movements of the maxillary vibrissae had phasic discharges and 18 % had tonic discharges. 3. The discharge characteristics of the two main types of primary afferent slowly-adapting units (St I and St II) were distinguishable in the tonically active cells of the nucleus. These two groups showed (i) substantially different interspike interval distributions, (ii) different adaptive properties and (iii) different directional sensitivity. The two categories were designated nuclear type I and type II in accordance with the classification of primary afferent slowly-adapting units. 4. A loss of stimulus information was deduced from a consistent increase in the variability of the second order discharges compared with their presumed afferent input, but this information loss may be important in allowing the linear summation of discharges at the level of the thalamus. Key words: Trigeminal Nucleus - Vibrissae - Slowly-adapting Neurones
Introduction The vibrissae (maxillary sinus hairs) form an array of mobile sensors which effectively extend the facial skin surface for several centimetres. This specialised hair group is used extensively in exploration and orientation behaviour and is particularly well-developed among nocturnal animals. Acting in addition to the touch receptors of the facial skin and fur, the sensory receptors in sinus hair 1 Presentaddress: The Brain Research Institute, Universityof California,Los Angeles, California, 90024. USA
458
D.W. Youngand A. Iggo
follicles provide information relation to the position, velocity, amplitude, duration and direction of vibrissal movement. Four main types of afferent response can be distinguished in axons dissected from the infraorbital nerve, two rapidly-adapting and two slowly-adapting (Gottschaldt, Iggo and Young, 1973). This array of receptors can accommodate a wide spectrum of mechanical stimuli ranging from low amplitude vibrations at frequencies over 1000 Hz, to large sustained deflections of the sinus hair. The functional organisation of the spinal trigeminal nucleus has been the subject of several investiga.tions (Wall and Taub, 1962; Kruger and Michel, 1962; Darian-Smith et al., 1963), and the present investigation was directed at the representation of specific vibrissal afferents in the spinal trigeminal nucleus, and in particular to the tonic responses which have the potential of transmitting to the central nervous system information about sustained mechanical stimulation. We have, therefore, compared the responses from trigeminal neurones with the afferent discharges from vibrissal afferent fibres under quantitatively controlled conditions. A preliminary account of this work has been published (Young, 1975).
Methods
Preparation Twenty cats weighing between 1.9 and 4.5 kg were used. In nine experiments anaesthesia was induced with ethyl chloride and ether, followed by chloralose 65 mg/kg i.v. In a further eleven experiments anaesthesia was induced by a mixture of nitrous oxide, oxygen (2:1) and halothane (1.5-3.5%) delivered via a face mask, and maintained by chloralose, 65 mg/kg i.v. Small doses of sodium pentobarbital (12 mg/kg) were given later in the experiments, as required. Arterial blood pressure was continuously monitored and electrophysiological recordings were taken only when the mean value exceeded 90 mm Hg. Expired air was sampled continuously and the end-tidal CO2 concentration recorded. A thermostatically-controlled electric blanket held the rectal temperature between 36 and 38 ~ C. The surface of the medulla was exposed by occipital craniotomy and cervical laminectomy. The head was fixed in a stereotaxic head-holder; a tilt of 15-20 ~ around the ear-bar axis was necessary to place the brain-stem recording area in the horizontal plane and, in addition in smaller animals the dorsal process of an upper thoracic vertebra was clamped to prevent distortion of the recording site. A recording pool was formed by sewing the skin margins to a metal ring and covering the surface of the medulla with warm mineral oil.
Stimulation and Recording Procedures Electrical stimuli of 1-18 volts and 50 ~ts duration were applied to the skin of the face at the base of individual vibrissae as required.
Vibrissae Input to the TrigeminalNucleus
459
Recordings were made in the medulla using glass micro-pipettes broken to a tip diameter of 1-3 ~tm, with impedances ranging from 2-5 Mfl. Action potentials were recorded and stored on a 7-channel tape recorder or processed on-line using a PDP-12 computer. In some experiments the position of the recording site was marked by the iontophoretic deposition of pontamine sky-blue from the dye-filled recording electrode (HeUon, 1971). These marked positions were subsequently identified on 40 gm sections of the brain-stem stained with cresyl violet and luxol blue. Care was taken to eliminate recordings made in the underlying lateral reticular nucleus, which also receives trigeminal input. Primary afferent fibres of the descending trigeminal tract may be recorded throughout the spinal nucleus, but these could be distinguished on the basis of latency, spike shape and the absence of injury discharge on further advancement of the electrode. The collision method was not used, however, to verify the separation of units on these subjective criteria. Recording in a region from 7 mm rostral to 3 mm caudal of the obex and from 2.5-5.5 lateral of the mid-line, the somatotopic organization of the spinal trigeminal nucleus under chloralose anaesthesia was found to correspond closely to that described by Darian-Smith et al. (1963). The methods by which single units were investigated using controlled angular displacement of sinus hairs and the statistical criteria by which different categories were distinguished, have been fully described in a previous publication (Gottschaldt et al., 1973). Additional information about the responses of vibrissal afferent units were required to supplement published information and cats prepared as described by Gottschaldt et al. (1973), were used for this purpose.
Results
Single Cell Activity One hundred and thirty two neurones responding to movements of the maxillary sinus hairs were recorded over the entire rostro-caudal and vertical extent of the spinal trigeminal nucleus. Contrary to the results of Mosso and Kruger (1973), who used barbiturate anaesthesia, 40% of recorded cells discharged continuously in the absence of any stimulus, and also responded to movements of the facial fur or the vibrissae. The rate of spontaneous activity varied from cell to cell and was clearly affected by the level of anaesthesia, often slowing appreciably following the administration of sodium pentobarbitone (12 mg/kg). In eleven units the appearance of spikes in time was random, or near random, and the inter-spike interval histogram (probability density function) was approximately exponential with a dead-time of 2-3 msec. The rate of discharge of some units could accelerate or decelerate abruptly over periods of several seconds. This instability in the firing frequency was not apparently related to any injury of the cells involved as it could be observed over several hours.
460
D.W. Youngand A. Iggo
Electrically Evoked Activity Electrical stimuli were applied through bipolar electrodes to the bases of vibrissal follicles. About 50 % of the cells responded to these stimuli with a burst of 3-6 impulses with a latency to the first spike of 3-5 msec (mean 5.14 msec, mode 3.5 msec) in agreement with Darian-Smith et al. (1963) and Mosso and Kruger (1973). The early burst or single spike was, in about 50% of these cells, followed by a later burst at a latency of 12-30 msec.
Responses to Movement of Vibrissae
Phasic Responses One hundred and thirty-two cells responded to movements of the maxillary vibrissae, and were classified using the criteria developed for the afferent vibrissal units (Gottschaldt et al., 1973). 82% gave only a phasic discharge, in contrast to the smaller proportion (33%) of the afferent unit population. Forty-eight (36%) of these phasic trigeminal neurones entrained for brief periods by high frequency (440 Hz) vibratory mechanical stimulation of a vibrissa, but not by low frequency vibration (< 10 Hz). The high frequency of vibration required to activate these cells and the absence of any directional preference of vibration, suggested that they were activated by axons supplying the Golgi-Mazzoni corpuscles in the sinus hair follicle (Gottschaldt et al., 1973). The remaining phasically responding cells showed a wide range of velocity thresholds, (20-100~ often responding with several impulses during the rising phase of a slow ramp movement applied to the hair.
Tonic Responses The discharge characteristics o f the two main classes of slowly-adapting afferent units (StI and StII) found in the infraorbital nerve were preserved in 24 cells (18%) of the sample of spinal trigeminal neurones. Two categories of tonically-responding neurones could be differentiated on the basis of (1) the interspike interval distributions of their discharges, (2) their adaptive properties and (3) their directional sensitivity. These correspond to similar differences between the two classes of slowly-adapting afferent units. The two categories were therefore designated nuclear type I and type I1. These patterns of discharge were clear-cut, despite the fact that units showed convergence from more than one vibrissa and the neurones could therefore not have been activated exclusively by single afferent fibres. The patterns of discharge in two typical units are shown in Figure 1 as sequential interval plots (A, B) and as interspike interval histograms (C, D). Figure 1A shows the sequential interval plot of the discharge of a nuclear type I cell to a sustained 10~ deflection of a maxillary sinus hair, recorded immediately after completion of the initial movement. Both long and short intervals appear
Vibrissae Input to the Trigeminal Nucleus
461
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Fig. 1. The discharge patterns of tonic cells in the spinal trigeminal nucleus. A, B Successive interval plots where each successive interval is plotted against its position in the spike train. A nuclear type I discharge. B nuclear type II discharge. C, D Interspike interval histograms of bin width 1 ms illustrating the distribution of interval lengths. C nuclear type I discharge with a superimposed exponential function (solid line) of the same parameters. D nuclear type II discharge with a superimposed Gaussian distribution of the same parameters. Note that the graphs are plotted on different scales
in the discharge, and although there is a progressive increase in the mean interspike interval, as revealed by the sloping regression line fitted to the histogram, the long and short intervals are nearly randomly distributed. In five similar units adaptation was present even in relatively small samples of data (100 intervals). The activity of the other unit plotted in a similar fashion (Fig. 1B), displays a characteristically uniform sequential interval plot (typical of class II units) with interspike intervals deviating only slightly from the mean over 100 intervals. Interspike interval distribution histograms Of the same cells are shown in Figure C and D. The probability density function for interspike interval lengths for the type I cell during a sustained rostral deflection of a single vibrissa is similar to a Poisson distribution of intervals, with a 2-3 msec dead-time. The probability density functions were calculated using parameters derived from the interspike interval histograms.
462
D.W. Youngand A. Iggo
The part of the curve between 3 and 150 msec does not, however, accurately fit an exponential function of the same parameters (~ (x) = )~e-ax) as would be expected of a truly random process, where )~ is the mean firing rate. In contrast to Figure 1C the interspike interval distribution for the nuclear type II neurone in Figure 1D is Gaussian, although deviations from the fitted normal probability density function are just significant at the 5 % level. The range of coefficients of variation (mean/standard deviation) in 5 nuclear type I units was from 0.92-1.71 and in 6 nuclear type II units was from 0.177-0.76, in both cases much wider than the equivalent values for the respective StI and StII afferent units (Gottschaldt et al., 1973). For the 11 trigeminal neurones tested in this way the increase in variability compared with that of the two groups of primary afferent slowly-adapting discharges was about 20 %.
Order-Dependent Properties of the Tonic Neuronal Discharges The presence of serial dependence in the tonically active trigeminal cells was estimated by the joint interval density and the serial correlation coefficient and compared with similar data obtained in separate experiments from primary afferent fibres of the infraorbital nerve in anaesthetized animals. Figures 2A and C shows the joint interval densities of the nuclear type I discharge (2A) and nuclear type II units (2C) respectively. The interspike interval (td has been plotted against the following interval (t~+1) in the spike train. The joint interval density therefore represents the degree of dependence of one interval on the previous interval (Rodieck et al., 1962; Perkel et al., 1967a). Where there is a completely random appearance of spikes in time the points would be scattered over the range of intervals plotted and this condition is met, at least partially, by the nuclear type I discharges (Fig. 2A), but is clearly not the case in the nuclear type II discharge (Fig. 2C), where a tight clustering of points around the common mean of both axes indicates that an interval of length t is followed by an interval which is very close in length to t. One parameter of this relationship is the serial correlation coefficient of order one (91, Cox and Lewis, 1966). The analysis was extended to nonadjacent intervals to test dependencies over a longer period of time. The serial correlogram of 200 intervals of a nuclear type II unit discharge for 50 orders of lag that is, the values of 91-9so, gave some evidence of cyclical activity with a period of about 15 intervals, but none of the 50 coefficients reached statistical significance at the 5 % level. The nuclear type ! discharge also shows signs of periodicity over 3-4 intervals, but again no deviations of the serial correlation coefficients from zero were significant at the 5 % level. Similar investigations of the properties of the slowly-adapting primary afferent discharges from sinus hair follicle StI and StII afferent units produced the results illustrated by joint interval plots in Figures 2B, D. The only clear difference between the peripheral and nuclear tonic discharges subjected to these tests was a cyclical change in the serial correlation of the sinus hair type II afferent activity which was highly significant for adjacent and alternate intervals (91 and 9z).
Vibrissae Input to the Trigeminal Nucleus
463
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Ti ms Fig. 2. The order-dependent properties of the trigeminal slowly-adapting discharges, nuclear type I and II (A, C) and of slowly-adapting vibrissal ST I and ST II afferents (B, D) expressed as joint-interval density diagrams. Each interspike interval (Ti) is plotted against the succeeding interval to the spike train (Ti+l). A random scattering of points as in A and B indicate that there is no interaction between adjacent intervals. The close grouping of points in C and D indicates a highly ordered sequence of intervals
Adaptation Behaviour of Nuclear Type I and H Neurones I n the p r i m a r y afferent units there is a clear distinction b e t w e e n the time constants of adaptation of the type I and the type II slowly-adapting m e c h a n o r e c e p t o r s (Iggo and Muir, 1969; C h a m b e r s et al., 1972; Gottschaldt et al., 1973). A d a p t a t i o n in the trigeminal n e u r o n e s was generally faster than in the p r i m a r y afferents. T h e nuclear type I discharge was even less sustained t h a n the nuclear type II, as in the periphery.
464
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