The Tactile System in the Frog and Toad
by David D. Olmsted (Copyright - 1998, 2006. Free to use for personal and
educational purposes)
Last Revised September 2, 2006
Types of Tactile Sensors
Figure 1
Cross-section of the Frog Skin Showing the Nerve Endings (Spray - 1976)
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Unlike the mesh-like tactile strategy of the tadpole (see
here) the nerves of frogs and toads run
deep under the skin. Only the ends of the nerve fibers rise towards the surface
to form receptive fields. With the exception of the pain sensing nerves, the nerve
fibers are now mylenated meaning that they have a fatty covering for the purpose
of increasing signal velocity. As shown in figure 1 these free nerve endings near
the skin show the beginnings of sensory specialization with the termination of the
fibers in different regions of the skin.
Those fibers ending in the epidermis are
activated by light touch and have the fastest signal velocities. If the epidermis
is removed by scraping with a scalpel these touch responses are abolished
from the dorsal cutaneous nerve leaving only a "continued discharge of slow impulses
indistinguishable from those produced by acid on the skin" (Adrian, Cattell,
and Hoagland - 1931, page 391). These slow impulses are from the fibers ending
in the dermis and they are responsible for sensing pain and temperature yet
these fibers were not actually seen and identified until 1955 by Whitear. The function
of those with expanded tip endings is unknown.
Figure 2
The Range of Neuron Fiber Diameters in a Single Dorsal Cutaneous Nerve (Spray and Chronister - 1974, scanned from Spray - 1976)
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These different tactile sensors
were initially discerned because each type had a different signal velocity
which in turn meant that each type had a different sized axon. As shown in figure
2 a single dorsal cutaneous nerve innervating a region on the backside of the frog Rana pipiens has approximately 63 axons of various diameters ranging from less
than 1 to 11 microns (micrometers). These axons can be clustered into four groupings.
The nerve itself has a diameter of approximately 105 microns (0.1 mm).
As one can see the divisions between fiber diameters are not absolute yet the groupings
do represent the nominal sensory types. The fastest fibers between 9 and 10
microns represent fast (phasic) touch, the next fastest between 5 and 6 microns
represent the slow (tonic) touch, the next between 2 and 3 microns represent
cold detection while the slowest between 0 and 1 microns represent pain detection.
As shown in figure 3 the backs of frogs are supplied by 4 to 8 pairs of dorsal cutaneous
nerves. Each nerve innervates approximately 20% of the dorsal (back) surface and
a smaller percentage of the ventral (stomach side) surface. (Spray - 1974, page
609)
Figure 3
Regions Innervated by Dorsal Cutaneous Nerves (Spray and Chronister - 1974, scanned from Spray - 1976)
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The signal velocities on these nerves are shown in figure 4. Graph "a" in
the figure represents the velocities recorded from stimulating the nerve endings
directly while
graph "b" represents stimulation from the skin. The four peaks correspond
to the four fiber diameter peaks of figure 2. The vertical lines in the crosses
of the main figure give the range of conduction velocities for the range of
fiber diameters
(horizontal lines) as determined by Catton (1958).
Properties of the Touch Receptors
Tactile stimulation in frogs (Rana pipiens) can produce either
prey capture actions or withdrawal actions. A soft brush or the edge of a pipe cleaner
stroked on a frog's skin produces prey capture actions as if some bug were
crawling on it. In contrast pokes result in a limb withdrawal or a turning
away from the stimulus (Comer and Grobstein - 1981, p143). A reasonable hypothesis
is that the fast touch receptors are responsible for triggering the prey capture
actions while the slow touch receptors are responsible for triggering the withdrawal
actions.
Figure 4
Signal Velocity is Greater for Larger Axon Diameters (Spray and Chronister - 1974, scanned from Spray - 1976)
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Supporting this hypothesis is the fact that some touch receptors (presumably
the slow touch) have much higher stimulus thresholds. A good description is
given by W.T. Catton - 1976, page 629.
"As one traverses a vibrating stylus
over the surface of the skin of a frog, whilst recording from a cutaneous
nerve, responses can be obtained from nearly every point. When responses in a single
fiber are examined, it is found that there are a number of discreet points at which
a response is evoked; the envelop of these points makes up the receptive field of
that fiber. Receptive fields overlap extensively."
"If the response at one point is
evoked by a brief stimulus, it consists usually of only one or two spikes, even
for markedly supraliminal (strong) stimuli. When longer pulses are used, there is
still in most cases only a very brief discharge at pulse onset, although when
the strength is raised another brief burst occurs at the end of the pulse.
Thus the majority of receptors are fast adapting and would be termed 'touch'
receptors; they give brief responses only at the beginning and end of prolonged
skin deflection."
"However, here and there, one encounters receptors of much higher
threshold, which continue to discharge during during sustained pressure of the stylus.
Such slowly adapting 'pressure' receptors are probably sited deeper in the skin
than the touch receptors but there is little positive evidence to confirm this.
They do not appear to discharge for very long periods and maximum spike trains in
the frog were found not to exceed about 16 spikes, however long the stimulus."
Figure 5
Close-up of a Single Touch Receptor Fiber (Catton - 1958)
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As mentioned in the top paragraph from Catton above the responses of a single fiber
show varying degrees of sensitivity within its receptive field. This is due to the
wide branching of its free fiber endings as shown in figure 5 so that it is
more sensitive to small stimuli near its endings than to stimuli further away. If
a weak (non-spike triggering) stimulus is applied to one free fiber ending
it affects the other free nerve endings because its charge moves down its own
branch and then up the others (called antidromic stimulation). The effect of this
is to raise the stimuli threshold of the other ends just as it does at its own end
since, as mentioned above, the fast touch receptors turn themselves off
to a degree proportional to their stimulation so that they only produce a few action
potentials per stimulus. This effect was measured in toads by Lindblom (1958)
who excluded other effects such as skin deformation. A typical skin deformation
was 100 microns deep and the skin pit it formed was not wide enough to affect other
free fiber endings. Upon the release of the stylus stroboscopic measurements
showed that the skin recovered its shape in 5 milliseconds.
Figure 6
Response of a Fast Touch Sensor in a Toad. (Lindblom - 1962)
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In addition to this
local antidromic effect about half the dorsal cutaneous nerves have fibers
exhibiting a non-local antidromic effect showing that some fibers innervate widely
different regions of the skin (Adrian, Cattell, and Hoagland - 1931). These fibers
were best activated by narrowly focused (0.2 mm) air blasts so most likely
they are the slow touch receptors responsible for general withdrawal or escape
actions and not the spatially localized prey acquisition actions. These fibers
always innervate the same side of the frog at approximately the same distance
from the head such that they are within their nerve's receptive field. The
receptive fields of these single fibers range from 4 to 100 square mm. Typical
measurements are 3 mm wide and 8-14 mm long. (This is the only description
of the receptive field of individual fibers in the literature)
Figure 7
Response of a Slow Touch Sensor in a Toad. (Lindblom - 1962)
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Using swift pokes
the depth threshold range for touch receptors in the frog is 2 to 20 microns
(Catton - 1961) which is 5 times smaller than the toad's 10
to 150 microns (Lindblom - 1958). The reason for this difference is not known
but one wonders if toads can react to bugs on their skin in a fashion similar to
frogs. If the rate of the poking is measured one can get the minimum rate required
to produce a response which is called the critical slope. The critical slopes in
the frog range from 0.1 to 11 mm/sec (Petoe - 1965, reported in Catton - 1967)
while those of the toad are only slightly higher ranging from 0.8 to 15 mm/sec
(Lindblom - 1958).
The poke response rates in the European toad Bufo bufo for the
fast touch receptors (called very rapidly adapting by Lindblom) and slow touch
receptors (called less rapidly adapting by Lindblom) are shown in figures 6 and
7 (from Lindblom - 1962). These represent the extreme ends in a range of the touch receptor types for many intermediate responses were found as well to correspond
to the many intermediate fiber diameters. The significant thing to notice is that
both the frequency and the number of the action potential spikes are modulated.
The frequency response is given by the line graph while the number of action
potential spikes is given by the histogram at the bottom with each dot representing
one spike. The fast touch receptors only produce a few action potentials while
the slow touch receptors produce a longer train at low poking rates. If the stimulus
is suddenly withdrawn from a slow touch receptor before its normal end of
action potential production the action potential production will cease (Lindblom
- 1963, page 417)
Figure 8
Fatigue Responses of Touch Receptors (Catton - 1976)
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Repeated stimulation of the touch receptors will produce habituation
even in the slow touch fibers as shown in figure 8. The effect is to raise the skin
depth threshold for any response although serious habituation does not seem
to occur until the poke rate is over 80 per second.
The fast touch sensors producing only a few action potentials are not strong enough to accomplish anything by themselves. Yet when combined over time they can indicated
a bug and trigger the prey acquistion action.
The Torus Semicirularis is the Generator of Tactually Triggered Actions
Leopard frogs (Rana pipiens) both blinded and intact will turn
and snap in response to light touch stimulation by a small camel hair brush in a
fashion similar to that triggered by visual food targets (Comer and Grobstein -
1981a). Both actions also retract the eye suggesting that both trigger the same
action generation circuitry in the spinal cord. In addition, tactile stimulation
can produce a forelimb scooping motion which seems to have the purpose of
forcing a bug into the mouth. Table 1 below summarizes the results of tactile
stimulation at the various locations shown in figure 9.
Figure 9
Stimulation Directions for Visual Cues (left) and Tactile Cues (right) (Comer and Grobstein - 1981a)
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Notice the variability in
responses to both tactile and visual stimuli as they occur further away from the
mouth. The further away the tactile stimulus is from the mouth the less the probability of a "turn and snap" and the greater probability of a simple "orienting turn".
Also notice the greater variation in the turn amount in the tactile response at
locations intermediate between full "Head Turn and Snap" and full "Orient
Turn" actions.
Since the tactile stimulation is only present for a brief initial
triggering time, the turns of both the head and the body must be the result of ballistic
motor actions and not the result of object tracking using a continuous feedback
signal to guide the animal towards the target. Since these actions are similar to
the visually triggered actions the visual actions should also be ballistic. Video
of these actions show that tactile based prey acquisition can be completed in only a few
hundred milliseconds which is about the latency of visually based decisions (Raybourn
- 1975).
The "orient turn" action seems to be different and independent from the head "turn
and snap action". Sperry (1944) found that frogs with rostal (nose-ward) lesions
in the tectum which blind them in the forward part of their visual field would
turn towards visual stimuli detected in the peripheral vision but never snapped.
| Tactile Responses to Stimuli at Various Locations in figure 9 |
| Stimulated Position | Turn In Degrees (Variation) | % Head Turn & Snap | % Orient Turn Only | % No Response |
| F | --- | 100% | 0% | 0% |
| 1 | 20 (5) | 100% | 0% | 0% |
| 2 | 70 (10) | 99% | 1% | 0% |
| 3 (toe) | 85 (15) | 74% | 26% | 0% |
| 4 (foot) | 85 (20) | 13% | 71% | 16% |
| 5 | 150 (10) | 0% | 100% | 0 |
Table 1
Combined results from two blind frogs, 30 trials at each position. (Comer and Grobstein - 1981a) |
| Visual Responses to Stimuli at Various Locations in figure 9 |
| Stimulated Position | % Head Turn & Snap | % Orient Turn Only | % Orient then Snap | % No Response |
| F | 90% | 10% | 0% | 0% |
| 1% | 67% | 20% | 10% | 4% |
| 2 | 48% | 33% | 18% | 0% |
| 3 (toe) | 32%) | 40% | 28% | 0% |
| 4 (foot) | 3% | 55% | 37% | 5% |
| 5 | 0 | 68% | 25% | 7 |
Table 2
Combined results from two blind frogs, 30 trials at each position. (Comer and Grobstein - 1981a) |
Figure 10
Three Lesions Involving the Tectum and Torus Semicircularis. (Comer and Grobstein - 1981b)
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Removal of the optic tectum in the frog Rana pipiens eliminates visually
triggered prey acquisition actions but not the tactually triggered actions. The
tactually triggered actions are impaired in proportion to the damage to the torus
semicircularis below the tectum (Comer and Grobstein - 1981b). Figure 10 shows the areas affected
in a series of cross-sections from caudal (tailward) to rostal (headward).
The top left illustration is the most caudal followed by the illustrations below
it and then back up to the top of the right side and down again to reach the
most rostal. The blackened area shows the extent of the largest unilateral
lesion which had no effect on tactually triggered behavior (frog no. 98). The vertically
shaded area is the lesion which produced some tactually triggered abnormalities
(frog no. 62) and the horizontally shaded area is the smallest lesion which
produced severe deficits in tactually triggered prey acquisition (frog no.
74).
ot = Optic tectum, ni= nucleus isthmi (a major target of axons from the tectum,
so much so that destruction of the tectum on both sides produces severe cellular
degeneration here), ts=torus semicircularis, dt=dorsal tegmental fields, vt=ventral
tegmental fields (the tegmental fields are cell dense regions in reticular
formation), pt=pretectal nucleus
| Tactile Responses After the Lesions in Figure 10 |
| Frog 98 | Frog 62 | Frog 74 |
| Side of Stimulation | Same as Lesion | Opposite from Lesion | Same as Lesion | Opposite from Lesion | Same as Lesion | Opposite from Lesion |
| Forelimb Response | 100% | 100% | 100% | 53% | 83% | 3% |
| Forelimb Motion in Degrees | 21 | 28 | 23 | 17 | 23 | 30 |
| Hindlimb Response | 100% | 100% | 100% | 27% | 87% | 0% |
| Hindlimb Motion in Degrees | 122 | 127 | 134 | 42 | 164 | ---- |
Table 3
(Data from table 2 of Comer and Grobstein - 1981b) |
Table 3 shows the results of the above lesions. Notice that the lesions mostly affect
tactile stimulation on the opposite side of the brain because most sensory fibers cross
over from the opposite side of the brain. Also notice that partial damage does not
eliminate a tactile response in one small skin region, instead the percentage of
responses is reduced and the response is no longer as accurate as it is in
a nondamaged frog such as frog number 98.
Pain Sensors
The slowest nerve fibers are located in the dermis of the skin and
are responsible for pain sensation. Unlike the other skin nerves they are
not myelinated. In the frog they have signal velocities of between 0.5 and
4 meters/sec with most being in the range of 1.5 to 3 meters/sec (Spray -
1976). These signals can be triggered by weak acid, intense mechanical stimuli,
and strong heating. The significant characteristic of these fibers is the long initial
latency of 500 to 700 milliseconds before the maximal response in the action potential
pulse (Hogg - 1935). The maximal response occurs near the beginning of the
pulse and is followed by slow decline in action potential frequency lasting up to
a second for severe pain stimulus.
Besides these slow responding pain sensors in
the frog skin another type of pain receptor has been found in the skin overlaying
the gastrocnemius muscle of toads (Maruhashi, et al - 1952). These pain fibers
had faster signal speeds being myelinated and having diameters between 6 to 9 micrometers.
They produced brief responses to pinch and pin prick and were excited by a weak
acid solution. Smaller fibers between 3 to 5 micrometers produced a more tonic
response and these were occasionally responsive to thermal stimulation. So what
one has here is a strategy similar to that used by the touch receptors and
one would expect this system to trigger a different set of behaviors from the frog.
Since the pain signal velocities in the frog are so slow and have such a long initial
latency they are not responsible for triggering any kind withdrawal action (the
fast pain system in the toad being the exception). This separation of fast
withdrawal from pain continues throughout vertebrate evolution. Since these pain
signals do not trigger an action they must be responsible for the reinforcement
signal in operant conditioning learning and should thus project to the reticular
formation (no studies have been done to track the pain fibers in frogs or
toads) and connect to the neurons differently and perhaps with different neurotransmitters
than the behavior triggering neurons. They also most likely project to the forebrain
region, especially to the amygdala to help characterize the environment of the animal.
The Cold Sensors
Figure 11
Cold Sensors Responses in Frogs Acclimated Different Temperatures (Spray - 1974, scanned from Spray - 1976)
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The frog and toad are cold blooded (ectothermic) meaning that they
cannot generate their own body heat. Consequently they change their posture
or move in order to maintain their body temperature within the desired range.
Different species also have different desired optimum temperatures (Lillywhite
- 1970). This behavior should also be of a released motivation type since
it involves a whole body strategy.
As shown in figure 11 the cold sensors in the
frog Rana pipiens are continuously active within a certain temperature range with
this activity peaking at the desired body temperature. The white dots show the response in cold acclimated frogs (9.5
degrees C) while the black dots show the response in warm acclimated frogs (23 degrees
C). Notice that the activity
level of these tonically active cold sensors is not as large as the more transient
touch sensors. This would seem to be a strategy to conserve energy. Also notice
that the peak occurs at the desired temperature when no action needs to take
place!
Figure 12
Dynamic Responses of Cold Sensors Showing Greater Sensitivity to Rapid Cooling (Spray - 1974, scanned from Spray - 1976)
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The fact that the cold sensor
peak occurs at the desired temperature indicates that these cold sensors are
used for some other purpose besides body temperature regulation. They may be used
to regulate reproductive behavior by signalling the optimum situation for that to
occur. This may be the reason why the responses of the cold sensor decrease in frogs
living in below normal temperatures also shown in figure 11 (the effect should be
even worse for chemical reactions slow in colder temperatures meaning that the actual
responses would be even lower than shown if the frog had been tested at 9.5 degrees
C).
Not only do the cold sensors have the static response rate described above but
they also have a dynamic response component as shown in figure 12. The top lines
give the temperature change rate. The solid line represents a change of 0.67 degrees
C per second, the dashed line represents a change of 0.5 degrees C per second,
and the dotted line represents a change of 0.25 degrees C per second. This means that
rapid temperature changes, even if the body temperature is near normal, are able
to trigger the same posture response as a situation in which the body is far from
the desired temperature. This a good example of a predicting strategy since
large changes in temperature will eventually produce a change in body temperature
sometime in the future.
The cold sensors in frogs (Rana pipiens) do not have symmetric
responses to changes in temperature. Their dynamic (phasic) response is more
sensitive to coldness. An increase in coldness increases the sensor's dynamic
response rate while an increase in hotness (decrease in coldness) decreases
the sensors dynamic response rate (Spray, 1976). This is why they are called
cold sensors instead of just temperature sensors.
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