Pflfigers Archiv

Pflfigers Arch. 382, 1-5 (1979)

EuropeanJournal
of Physiology
9 by Springer-Verlag1979

Parameters of the Static Burst Discharge of Lingual Cold Receptors in the Cat
H. Bade, H. A. Braun, and H. Hensel
Physi01ogisches Institut der Universidit Marburg, Deutschhausstrasse 2, D-3550 Marburg, Federal Republic of Germany

Abstract. Thermal stimuli were applied to the upper

surface of the tongue of the cat. The stimuli ranged

fi'om 40~ to 10~ and were changed in cold steps of
5~C, each temperature lasting 2 min. Afferent impulses
of single specific cold fibers from the lingual nerve were
analysed by a computer program. About 90 % of the
fibers showed bursts under static conditions. The bursts
began as doublets at the temperature of maximal
average frequency. This temperature varied from 40 ~C
to 15~ in different fibers, the average being 30 ~C. The
parameters burst period, burst duration, pause duration, intraburst interval and spikes per burst increased monotonically from 30~ to 15~ The possible physiological significance of the burst pattern is
discussed.
Key words: Cold receptor -

Burst parameters Lingual nerve - Static discharge.

Introduction

Grouped discharges were first described for cold fibers

in the lingual nerve of the cat. These grouped discharges

were found to start at constant temperatures lower than

those at which the static activity of cold fibers began
(Hensel and Zotterman, 1951). At temperatures below
15~ the grouped pattern disappeared and the discharge of impulses became more regular again. Dodt
(1953) found an inverse relationship between group
frequency and constant temperature.
Iggo (1969) gave a more detailed analysis of the
grouped discharge in the skin of monkey and dog,
defining the term 'burst' as a pattern with an interburst
interval at least twice as long as the intraburst interval,
which is repeated in a regular manner. While the
Send offprh~t requests to

H. Hensel at the above address

average static frequency of cold fibers showed a

maximum at a certain temperature, most of the burst
parameters, such as burst frequency or number of
impulses per burst, increased monotonically with decreasing constant temperature in the bursting range
(Iggo, 1969; Poulos, 1971, 1975; Iggo and Young,
1975; Dykes, 1975; Dubner et al., 1975; Kenshalo and
Duclaux, 1977). The burst pattern appeared at temperatures near the maximal sensitivity of a cold receptor (Iggo, 1965; Poulos, 1975).
It was assumed that the burst pattern could constitute a code to give unambiguous information about
steady temperature from the starting temperature of
cold fiber activity down to low temperatures where the
burst pattern disappears again (Iggo and Young, 1975;
Dykes, 1975; Poulos and Molt, 1976).
The aim of our investigations was to compare the
burst parameters of cold fibers in the lingual nerve of
the cat at constant temperatures with the respective
parameters in the skin of monkey and dog. In contrast
to the skin, the cat's tongue, under natural conditions,
is never exposed to low static temperatures where the
burst discharge may become significant as additional
information parameter. A comparison of relative number and properties of cold fibers in the tongue and in the
external skin was expected to contribute to the discussion of the physiological significance of the burst
discharge. In addition, the tongue is particularly suited
for the study of cold receptors under externally and
internally controlled conditions, including intraarterial
administration of substances and artificial perfusion. It
seemed therefore desirable to obtain detailed information about the properties of the lingual cold receptor
population.
Methods

Cats were initially anesthetized with pentobarbital i.p. (25 mg/kg);

anesthesia was maintained by intravenous application. The trachea
was cannulated. The head of the animal was fixed and the tongue -

0031-6768/79/0382/0001/$01.00

2
upper side down - was placed on a metal thermode of 2.5cm
diameter covering the whole forepart of the tongue. The thermode
was alternatively circnlated with water from 7 thermostats kept at
constant temperatures. Stimulus temperatures were measured by a
thermocouple soldered to the bottom of the thermode, displayed on
an oscilloscope and recorded on tape and film.
The distal part of the lingual nerve was exposed and proximally
cut. After testing the receptive field by mechanical stimulation,
suitable bundles were chosen for single-fiber preparations of specific
cold fibers. Action potentials were recorded with Ringer-soaked wick
electrodes. The amplified action potentials were displayed on an
oscilloscope and recorded on tape and film. Single fibers responding
to mechanical stimulation were not used. Furthermore, a cold step of
25 ~ C to 20 ~C was applied in order to eliminate fibers with receptive
fields on the lower side of the tongue. These fibers give a delayed
response to the cold step (Hensel and Witt, 1959). Seven stimulus
temperatures from 40~ to 10~ in steps of 5~ were applied for
2 min each. In this time the discharge adapted to the static values.
After transforming the spikes by a window discriminator, data were
processed by means of a computer p r o g r a m for burst identification
and analysis on a PDP 12.

Pfl/igers Arch. 382 (1979)

IMPULSE DISCHARGE

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INSTANTANEOUS FREQUENCY

Thirty-four single cold fibers were investigated, of

which 27 could be tested over the whole temperature
range. Figure 1 shows the static activity of a single cold
fiber at various temperatures. At higher temperatures, a
regular sequence of single spikes is seen. When lowering
the constant temperature, sporadic bursts (doublets)
appear. At 30 ~C, a regular burst discharge occurs. With
further decrease in temperature, burst duration, pause
duration, intraburst interval, and number of spikes per
burst increase. Finally, the discharge becomes more
irregular.
The following definitions (see also Fig. 3) were used
for the classification of burst parameters: BD, burst
duration; PD, pause duration; BP, burst period (BD
+ PD); BI, intraburst interval; ABI, average intraburst
interval; SB, spikes/burst; AF, average impulse frequency; BB, beginning of the regular burst pattern.
Since the change from single spikes to regular bursting
was gradual, BB was defined as that state at which more
than 50 % of the spikes appeared in bursts.
In a population of 27 fibers the temperature of BB
was 40~ to 15~ with accumulation in the range
between 20~ to 35 ~C. The average temperature of BB
was 30~ A recruitment of bursting fibers occurred
when lowering the temperature from 40 ~C to 25 ~C. At
25~ 92.5 % of the population was bursting.
Fibers having the same temperature of BB were
grouped together and their A F was plotted as function
of temperature (Fig. 2). A correlation between BB and
maximal AF can be seen in fibers with BB at 35~
30 ~C, 25 ~C and 20 ~C, whereas this correlation does not
hold for BB at the more extreme temperatures of 40 ~C
and 15~
If, however, average values for the whole population of cold receptors are calculated, the maximal A F

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Fig. 1. Impulse discharge, instantaneous frequency and interval

histograms of a single cold fiber at various constant temperatures

and BB must not necessarily coincide. For a population

of 27 cold receptors, the mean temperature of BB was
30 ~C, while the temperature of maximal AF was 25 ~C.
However, at 30 ~C, AF was only slightly lower (97 %)
than the maximal value.
The parameters BP, BD and PD did not significantly differ in fibers of different temperatures of BB.
Therefore the values of all fiber groups in Fig. 3 were
put together. BP, BD and PD increased monotonically
with decreasing temperature, the variation of single
values becoming larger in the lower thermal range. In
contrast to these parameters, the average interval had a
minimum at 25~ This curve depicts the reciprocal
value of the bell-shaped frequency-temperature curve
of cold receptors.
When the static temperature was lowered, the
parameter SB increased monotonically (Fig. 4). For
fiber groups with BB other than 30 ~C, the curves run
parallel with that shown in Fig. 4.

Discussion

The burst pattern of cold fibers from the cat's tongue

shows a similar dependency on temperature to that of

0,5

H. Bade et al. : Burst Parameters of Lingual Cold Receptors

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Fig. 2

Average frequency of single cold fibers as function

of temperature. BB, beginning of bursts, n, number
of fibers in each group. Bars indicate S.E.M.

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Fig. 3. Averageburst parameters and mean spike interval as function

of constant temperature. BD, burst duration; PD, pause duration;
BP, burst period; BI, intraburst interval; ABI, average intraburst
interval, n, number of cold fibers. Bars indicate S.E.M.

Fig.4. Number of spikes/burst (SB) for a group of cold fibers with

beginning of bursts at 30~Cas function of temperature, n, number of
fibers

cold fibers in the monkey's skin, perioral units in the

dog and cold fibers in the scrotal skin of the rat. The
values for several burst parameters in various species
are given in Table 1.
For cold receptors in the monkey's skin, Poulos
(1975) mentioned a certain correlation between the
temperature of BB and that of the static maximum of
AF. In his sample of 7cold fibers, the maximal A F
occurs at 29~ and the burst pattern with SB = 2 at
33 ~C. Similar results were reported by Iggo and Young
(1975); in a sample of 12 cold fibers, the maximal A F
was found at 27 ~C, while the burst pattern with SB = 2
occurred at 31~ The corresponding values found by
Dykes (1975) were 24~ and 2 6 - 2 8 ~
respectively.

Although the average temperature of BB is higher than

the temperature of the maximal AF, the results of these
authors show a correlation between both parameters:
the higher the temperature of the maximal AF, the
higher the temperature at which the regular burst
pattern begins.
According to our measurements, the temperature of
the cat's tongue does not drop to constant levels below
35~ even at ambients as low as 5~ while the skin
temperature of the nose can easily reach constant levels
between 30~ and 15~ where the burst parameters
are highly dependent on temperature. For example, the
average nasal temperature of cats was found to be 15~
at ambients of 5~ (Hensel and gch~fer, 1979).

Pfliigers Arch. 382 (1979)

Table 1. Burst parameters of cold fibers in various species

Author

Nerve

Spikes/burst
(SB)

Burst duration
(BD)

Burst period
(BP)

ms

ms

Range
of regular
burst pattern
~C

Iggo (1969)"

Monkey, N. medianus

2-4

285--650

31-21

Poulos (1971) ~

Monkey, N. trigeminus

2-5

20-100

1 3 0 - 340

33-21

Dykes (1975)

Monkey, N. medianus

2-4

12-220

240--600

26-20

Hellon et al. (1975)

Rat, N. pudendus

2-4

Our data

Cat, N. lingualis

2-4

27--20
15-- 100

1 6 0 - 520

30-15

Partially extrapolated data

However, in contrast to the lingual cold receptors with

more than 90 % bursting units, only 28 % of the nasal
cold fibers were bursting at constant temperatures of
15~C. If the burst discharge is decisive for the detection
of low static temperatures, it is difficult to understand
why in a receptive field never exposed to such temperature levels nearly all cold fibers are bursting, whereas
only a relatively small fraction of bursting units is found
in a region which, under natural conditions, can
frequently reach low constant temperatures. In the
range below 20~C, additional thermal information may
be conveyed by recently discovered nasal receptors
activated at very low constant temperatures (Duclaux,
Sch/ifer and Hensel, unpublished).
The average temperature of the furred skin in the
cat changes from about 34~C at 25 ~C ambient temperature to 31~ at - 5 ~ ambient temperature (Hensel
and Banet, 1977). There is only limited information
available about cutaneous cold receptors in the trunk
and proximal parts of the extremities in cats (Witt and
Hensel, 1959; Hensel et al., 1960). Assuming that their
response characteristics are similar to those of the nasal
cold receptors, AF alone could give sufficient information for the thermoregulatory system in this temperature range.
The burst parameters of cold fibers from the
monkey's hand do not agree with static temperature
sensation in the human hand. According to Beste and
Hensel (1977), human subjects are not able to discriminate constant temperatures applied to the hand in the
range between 28~ and 22~ whereas the burst
parameters of cold receptors in the monkey's hand are
highly dependent on temperature particularly in this
range (Dykes, 1975). On the other hand, human
sensory discrimination improves at constant temperatures below 20~C, but in the monkey no regular burst
pattern is seen in this range.
There is no evidence that the burst pattern of cold
receptors is maintained through synaptic transmission
in the situation of convergence (Landgren, 1957, 1960;

Poulos, 1975; Iggo and Young, 1976; Iggo and

Ramsey, 1976; Schmidt, 1976; Dostrovsky and Hellon,
1978).
Neither is there any evidence of an indirect transmission of the burst parameters, the frequencytemperature characteristics of higher order neurons
showing a bell-shaped curve similar to that of peripheral cold receptors (Poulos, 1971; Poulos and Molt,
1976; Dostrovsky and Hellon, 1978). This does not
necessarily exclude any significance of the burst pattern
for synaptic transmission but such a function remains
to be demonstrated.
Acknowledgements. The authors are greatly indebted to Prof. H.
Fruhstorfer and his co-workers Dr. W. G. Schmidt and Mr. P.
Langanke for their valuable help in programming the PDP-12 and to
Mrs. H. Bestgen for technical assistance.
Supported by the Deutsche Forschungsgemeinschaft.

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Received April ll/Accepted July 10, 1979