EXPERIMENTAL NEUROLOGY 61, 84-95 (1978)

Acupuncture Reduces the Trigeminal Evoked Response

in Decerebrate Cats

FREDERICK W. L. KERR, PETER R. WILSON, AND

DANIEL E. NIJENSOHN 1

Departrncnt of Nczwologic Surgery, Mayo Clinic and Foundation,

Rochester, Minnesota 55901

Received December lb,1977

Electroacupuncture was administered to 52 decerebrate, unanesthetized

cats in which the trigeminal electrically evoked response was recorded from
the surface of the brain stem. In 15 of these, the first negative wave of the
evoked potential was reliably depressed by 20 to 80% after electroacu-
puncture, and spontaneous recovery of the responses occurred in 3 to 15 min.
This is a previously unreported finding and is discussed in the light of
current theories of acupuncture and analgesia.

INTRODUCTION
Acupuncture with mechanical or electrical stimulation of the needles
has been shown to have behavioral and physiological effects in animals (4,
5, 11, 12, 20, 24, 30) and man (1, 2, 7-10, 16, 18, 21, 22, 28). However,
there have been comparatively few electrophysiological studies of this
phenomenon (5, 15, 17), and these have not reached agreement on the
criteria for an acupuncture effect. For example, the duration of electro-
physiologic changes was variously reported in animals to range from less
than 800 ms (4) to more than 2 h (14)) and there is no unanimity on the
methods or sites of stimulation [see, for example, Ref. (lo)].
Faced with these inconsistencies, it was decided to investigate the
phenomenon in a preparation in which cerebral cortical, pharmacological,
and political factors could be controlled. An electrically evoked potential

1 This work was supported by National Institutes of Health Grant GM 21981. We

thank Mr. Patrick Bowron for skilled technical assistance. Dr. Wilson’s present
address is Department of Anaesthesia, Flinders University, South Australia 5042.
Abbreviations : CRO-cathode-ray oscillograph ; GABA-y-aminobutyric acid.

84

0014~4886/78/0611-0084$02.00/O
Copyright 0 1978 by Academic Press, Inc.
All rights of reproduction in any form reserved
 ACUPUiYCTL?RE AND TRIGEMINAL EVOKED RESPONSE 8.5

was chosen as the electrophysiologic event for study, and our own criteria
for the acupuncture effect were arbitrarily defined in the absence of any
published guidelines. Similarly, an arbitrary method of acupuncture was
chosen, based on anecdotal evidence that clinical analgesia/hypalgesia
requires 15 to 20 min of acupuncture stimulation.

IMETHODS
Data were acquired from 52 experiments in which the preparation was
successful. Unselected adult cats were anesthetized with ether for the initial
surgery. Tracheal, femoral arterial, and venous cannulae were inserted,
and the animal’s head was placed in a standard stereotaxic holder. A
pretentorial intercollicular decerebration was carried out with a fine spatula
under microscopic control through a left parietal craniectomy. The ether
was then discontinued, and the experiment continued only if the
decerebration was successful, determined by the following criteria :
maximally constricted pupils, unchanged spontaneous respiration, and no
brain edema or hematomas. Laminectomy of the first two cervical vertebrae
was carried out, and enough occipital bone was removed to allow access to
the brain stem a few millimeters above and lateral to the ohex. The infra-
orbital nerve on one side was dissected, freeing the three to five major
branches from the foramen as far distally as convenient (at least 10 mm).
In some cases the greater auricular nerve of the same side was also freed
for 10 cm of its course. Exposed neural tissue was protected with warm
vegetable oil. The animal was paralyzed (gallamine triethiodide j and
ventilated, and an open pneumothorax created on each side. Physiologic
variables (blood pressure, end-tidal CO-, body temperature ) were main-
tained within normal limits.
A branch of the infraorbital nerve was placed on silver hook electrodes
for isolated stimulation (Grass S&3, Grass SIU-5). Evoked potentials
were recorded from the surface of the ipsilateral trigeminal spinal tract
and nucleus caudalis at points between 3 mm above the uppermost Cl
rootlet and the middle of the Cl segment with a small silver ball electrode.
After conventional amplification these potentials were displayed on a
cathode-ray oscillograph (CR0 ; negative upwards) and photographed
(Grass kymograph camera) for later analysis. Threshold for electrical
stimulation was determined for the infraorbital branches (A fibers only).
i\lthough C-fiber activation could be readily obtained from the infraorbital
nerve with high currents, no potentials at appropriate latencies could be
recorded from the surface of the spinal tract of the trigeminal nerve below
the obex. We therefore measured only the early components of the tri-
geminal potential evoked hy stimulation (duration, 0.1 ms) of the infra-
orbital nerve branches at five times threshold at 0.3 to 1.0 shock per second,
86 KERR, WILSON, AND NIJENS~HN

Acupuncture was administered by inserting an uninsulated stainless-steel

needle (28 SWG) into the dorsum of the ipsilateral forepaw and stimulat-
ing 20 min with square pulses of 9 V, 1 ms, 60 Hz. The first intermetacarpal
space, which in animals and man is referred to as the Hoku point, was
the initial site of such stimulation; the needle was moved systematically
from one intermetacarpal space to the next, and to the other side in
attempts to elicit an acupuncture effect. In some cases, the skin of the
dorsum of the paw was reflected, and the needle inserted into the inter-
metacarpal space, avoiding large branches of cutaneous nerves. Peripheral
nerves themselves were not deliberately stimulated.
In some cases, the greater auricular nerve was stimulated simultaneously
at five times its threshold (duration, 0.1 ms) , and potentials were recorded
from the surface of the dorsal horn in the Cl-C2 region with another
silver ball electrode and displayed on a second channel of the CRO.
An acupuncture effect was arbitrarily defined as a significant, prolonged,
spontaneously reversible, and reproducible depression of the first negative
wave of the trigeminal evoked response recorded at, or just above, Cl.
Because on occasion a variation in the amplitude of the control evoked
response of as much as 10% may occur during a recording session, we

Nl

JL A
S

CONTROL
P
N2

&
S

POST
Nl

ACU I5 s
L 30 s

L
4/L
4 ILL

7 min

FIG. 1. Trigeminalevokedpotentialsrecordedfrom the surfaceof the spinalnucleus

caudalisafter electrically stimulatingthe ipsilateralinfraorbital nerve, shownbefore
(control) and after electroacupuncture of 20-minduration. Control showsthe follow-
ing components : A = stimulusartifact; S = tract spike; Nl = first negativewave;
P = positivewave; N2 = secondnegativewave. Post acu is the first evokedresponse
after acupuncture.The other responses are 15 s, 30 s, and 1, 2, 4, and 7 min after
cessationof acupuncture.Calibrations: 5 ms; 200 pV.
 ACtX’lJNCTURE AND TRIGEMINAL EVOKED RESPONSE 85

defined a significant depression as one of at least 20$,. We required this

change to be present consistently for at least three successive evoked
responses, to exceed a 20% reduction for at least 1 min, to return spon-
taneously to the control amplitude within 30 min, and to occur reliably
after electroacupuncture, but not after similar control periods without
electroacupuncture. Unless all these criteria were met, changes in the
evoked potential were not included in the results presented here.

RESULTS
The normal response recorded from the surface of the brain stem at
or just above Cl after electrical stimulation of the ipsilateral infraorbital
nerve is shown as the control response in Fig. 1 (control). The stimulus
artifact (A) is followed by the tract spike (S), a variable positive deflection
followed by a consistent negative spike, with a delay of approximately 1
ms, representing a conduction velocity of about 50 m/s. This spike is able
to follow stimulus rates of 500 Hz and is the component most resistant to
hypoxia. It is followed within 1 ms by a negative wave (Nl), which is
progressively reduced in amplitude at stimulus rates above 10 Hz and is
the most sensitive to hypoxia. ,4 small, positive wave (P) and a small
negative wave (N2) follow the first negative wave, with latencies of about
4 and 6 ms, respectively.

CONiROL POST ACU 30 s 1 min

I-

2 3 4 6 min

FIG. 2. Trigeminal evoked responses from another experiment, before (control) and
immediately after (post acu) 20-min acupuncture, showing recovery of the depressed
Nl wave during the succeeding 6 min. Calibrations: 5 ms, 200 pV.
88 KERR, WILSON, AND NIJENSOHN

In 15 of the 52 animals, the acupuncture effect defined above was

obtained. Figure 1 illustrates an acupuncture effect and its recovery. The
baseline trigeminal evoked potential recorded near the obex is shown as
control, and the response with unchanged stimulating and recording
conditions after 20 min of acupuncture is shown as post acu. The S spike
is depressed to 80% of control and the Nl wave is reduced to about 30%
of its control value. The P and N2 waves are virtually abolished. Spon-
taneous recovery of all components occurs within 7 min, most recovery
(to 75% of control) occurring in the first minute after cessation of electro-
acupuncture. Figure 2 shows another example from a different experiment.
In this case, the Nl wave is reduced to about 35% of control, and recovery
occurs in 6 min. The S spike is unaffected in this case.
This type of response could be obtained by electroacupuncture of adja-
cent intermetacarpal spaces and was reproducible time after time in the
same experiment, as shown in Fig. 3. The first row shows a control
response evoked by infraorbital nerve stimulation and recorded at the
level of mid-Cl. Note that the configuration of the evoked potential

I hr

2 hr

4 hr

CONTROL POST ACU 1 min 2 min 3min

FIG. 3. Top row-Trigeminal evoked responses recorded for the first time in an
experiment from the nucleus caudalis-Cl region, showing its configuration before
(control, first column) and immediately after ZO-min electroacupuncture (post acu,
second column), and recovery at 1, 2, and 3 min (third, fourth, and fifth columns).
Second row-One hour later; third row-2 h later; fourth row4 h later. Calibra-
tions 5 ms, 200 ,uV.
 ACUPUNCTURE AND TRIGEMINAI. EVOKED RESPOSSE 89

CONTROL POST ACU

1 2 3 min

FIG. 4. Responses from the spinal nucleus caudalis evoked after electrical stimula-
tion of the infraorbital nerve (INF, upper trace) and the Cl-C2 dorsal column region
after simultaneous electrical stimulation of the greater auricular nerve (GAN),
before (control) and immediately after (post acu) ZO-min electroacupuncture.
Recovery is shown at 30 s and 1, 2, and 3 min. Calibrations: 5 ms, 200 pV.

recorded here is somewhat different from that recorded nrore rostrally.

The Nl wave is reduced to about 50% of its initial value, and recovery
is shown at 1, 2, and 3 min. The N2 wave is abolished, but also recovers in
the same time. The second row shows the response after identical condi-
tions 1 h later. The degree of depression of the evoked response is similar,
and recovery occurs with the sanle time course. The third row is 2 h after
the first, but with electroacupuncture applied to the second interlnetacarpal
space. Again, there is a similar depression of the trigetninal evoked
response for a similar duration. The bottom row shows the evoked response
from a different branch of the infraorbital nerve, 4 h after the first
example. Acupuncture was at the second intermetacarpal space and record-
ing conditions were unchanged. The depression of the components of the
evoked potential and their rates of recovery are again similar.
In another experiment, evoked potentials were recorded from the
region of the obex and C2 after sinlultaneous stinnilation of the infra-
orbital and greater auricular nerves. Figure 4 shows the evoked responses
of infraorbital (INF) and greater auricular (GAN) nerves. The responses
are similar in shape, but of different latency. 130th Nl waves are depressed
after electroacupuncture.
The results of the 15 experinlents iii which the effect was obtained
 KERR, WILSON, AND NIJENSOHN

--=
=z-

,_--

I 1 1 I I ---
O1\
0 1 2 3 4 5
Time (min) after completion of acupuncture

FIG. 5. Graph summarizing one example of an acupuncture effect from each of the
successful experiments, expressed as percentage of the preacupuncture amplitude of
the evoked negative potential (control = 100%). Immediately after acupuncture (time
= 0), the amplitudes were depressed to 80 to 20% of the control values, and recovery
occurred within 3 to 15 min. No comment can be made on the rate of onset of the
effect from these experiments.

are summarized in Fig. 5, using one result from each experiment. The
Nl waves were depressedby at least 20 (by definition) to 80% of their
control values. The maximum depression seen was 80% (to 20% of the
control amplitude), with most being depressed by 30 to 70%. The degree
of depression was constant within an experiment. Recovery to control
values was measured and occurred with a delay of 3 to 15 min. Most ( 11)
recovered within 5 min, and most of each recovery occurred in the first
minute. In other experiments there was an apparent depression of the
evoked response after electroacupuncture but with no recovery, or
recovery to less than control amplitudes. Such observations were regarded
as unreliable and therefore discarded.
If an acupuncture effect was obtained, the animal remained unstimulated
by the electroacupuncture or infraorbital nerve at least 20 min, and evoked
responseswere recorded at the end of that time. In all casesthe responses
were identical to the control tracings.
 In twn animals the effect was abolished after spinal cord transection at
Cl-C2. The effect was not seen in a preliminary series of experiments
with harbiturate anesthesia, but the effects of barbiturates were not tested
in successful experiments. Also, the effects of narcotics and their antag-
onists, or other analgesics, were not systematically studied.

DISCUSSION
Before discussing the observations made in this study, some comments
on technique are necessary. The first issue to be considered concerns the
definition of acupuncture stimulation and its relationship to the stimulation
method used in this study. Because acupuncture is an empirically devised
therapeutic method, it necessarily follows that the methods used by its
successful practitioners should be followed as closely as possible. These
methods, however, vary widely (10). At one extreme, traditional prac-
titioners insert sharpened bamboo needles into conventional “acupuncture
points” and twirl the needle with a rapid to and fro rolling movement. At
the other extreme, uninsulated steel needles are introduced into “acupunc-
ture points” and electrical stimulation is delivered. The stimulus parameters
vary widely from one institution to another, even in China, as observed
by one of us ]F. 117. L. Kerr, Ref. (2) 1. Tl le voltages, pulse duration, and
frequency, as well as the needles, used in our study were well within the
range of techniques used for inducing surgical analgesia in China (2, IO).
Thus, insofar as acupuncture can be defined as a method, we believe that
the requirements have been fulfilled.
Another issue that requires consideration is the relationship, if any, of
this study to nociception. This question is, of course, equally apropos in
other studies in which direct evidence of pain modulation is not available.
Thus, unless behavioral correlates are an integral part of the study, only
indirect inferences can he made. Even when single units responding to
high-threshold peripheral receptors are modulated, there is no guarantee
that such cells are in the pathway to consciousness of pain. They may well
be in a nociceptive reflex arc, for example, and their responses only very
indirectly related to pain.
Insofar as this study is concerned, the region from which trigeminal
evoked responses were recorded corresponds to that part of the nuclear
complex in which the relay of nociceptive input occurs. However, it is
necessarly to note that this is not a pure nociceptive relay region, because
numerous mechanoreceptor interneurons are also present. For this reason,
it was clearly specified that what has been modified is the trigeminal
evoked response : whether and to what degree nociceptive relay was
modified cannot be inferred.
A third issue is that of the inconsistency with which depression of the
92 KERR, WILSON, AND NIJENSOHN

evoked response was obtained. Thus, only in approximately one of

every three experiments was a positive result obtained. Interestingly, the
most striking effect was obtained in the first experiment carried out ; the
depression of the Nl response lasted longer ( 15 min) than in any subse-
quent experiment. Although the response could be obtained time and again
in that experiment, no result was obtained in subsequent experiments
until the seventh attempt ! This unpredictability was characteristic through-
out the study and we have been unable to account for it. However, it may
represent an interesting experimental parallel to the notorious unpredict-
ability of acupuncture analgesia for surgery. Pomeranz and Chiu (25) and
Pomeranz et al. (24) described prolonged changes after electroacupunc-
ture comparable to those reported here. The former paper described an
increase in latency to squeak in mice subjected to a noxious heat stimulus.
Such mice showed a significant increase in latency after electroacupunc-
ture, but not after acupuncture plus naloxone. However, the latency was
shown to increase for 20 min after cessation of acupuncture, an effect we
were unable to demonstrate. In the latter paper [ (24)) completed first],
they examined spinal cord lamina V cells in 14 cats anesthetized with
chloralose and stimulated with n,atural noxious and nonnoxious stimuli.
Electroacupuncture was administered for 30 min and caused a reduction
in the firing rate of 21 of 26 cells monitored. It was not stated in how many
animals these cells were recorded from. The depression was stated to last
from 10 to 30 min after the acupuncture was discontinued, but time to
complete recovery was not stated.
They also commented that they were unable to elicit the effects in cats
with a spinal cord transection (Cl ; six cats) or with a midcollicular
decerebration (four cats). Unfortunately, they do not say whether or not
these maneuvers abolished the effects of acupuncture in susceptible animals.
In two of our experiments in which the effect was obtained, spinal cord
transection at Cl did abolish the effect, corroborating their first finding.
In our series of experiments, however, it was not unusual to have four
or more consecutive experiments where no effect was obtained. This sug-
gests that their conclusions regarding decerebration may need revision
because the acupuncture effect may not be invariably obtained in this state.
Du and Chao (11) also described prolonged changes of a viscerosomatic
reflex after electroacupuncture. They described an inhibition lasting 1 to
5 min after 30-s electroacupuncture and lasting more than 30 min after
.5-min electroacupuncture. They noted that decerebration did not alter this
particular acupuncture effect.
Because of the infrequency of obtaining this phenomenon, we were
unable to make a systematic study of the threshold for acupuncture stim-
ulation, the effects of pharmacologic agents (naloxone, morphine, haclofen,
 ACUPUNCTURE AND TRIGEMINAL EVOKED RESPONSE 03

bicuculline, strychnine, anesthetics), or surgical interventions (peripheral

nerve section, rhizotomy, tractotomy, or rordotomy), which will be needed
to define the pathways and neurochemistry of this phenomenon.
Acupuncture in humans is an unreliable method of producing analgesia,
and refined psychophysical methods are often necessary to detect the effect
(6-9, 18). However, Mayer et al. (19) reported that in human volunteers
under certain conditions (electrical tooth stimulation), acupuncture anal-
gesia can be obtained, and such analgesia can be antagonized by naloxone
(0.8 mgj, This suggests that endogenous opiates may have a role in this
analgesia. This view has received support from the preliminary report of
Sjijlund et al. (27) that endorphin concentrations in lumbar cerebrospinal
fluids were increased in four patients whose lumbar pain was relieved by
electroacupuncture. (Four patients with thoracic or trigeminal pain relieved
by electroacupuncture did not have increased endorphin values in their
lumbar cerebrospinal fluid.) However, serotonin may also play a role in
acupuncture analgesia (26), possibly as a transmitter in a spinal cord
system mediating analgesia (29)) and other putative transmitters (GABA
and glycine) must also be considered (20).
Indirect evidence of the possibility of endogenous opiate involvement
was presented by Ng et nl. (23). Morphine-dependent rats were reported
to have less severe naloxone-precipitated withdrawal signs if treated with
electroacupuncture for 30 min before the naloxone, suggesting that there
may have been an increase in endogenous opioid compounds. Peripheral
mechnisms may also play a role in the development of analgesia after
acupuncture. Lee et a,l. (14) reported in anesthetized dogs a sympathetic
response to acupuncture, but did not test for analgesia. Garcia Leme and
Lice (13) showed in rats that cortical potentials evoked by electrical
stimulation of tooth pulp were depressed as long as 180 min following
electrical stimulation of the cut end of a saphenous nerve. They suggested
that this effect was mediated by a peripheral humoral factor. Although
they showed recovery of the evoked potential in one illustration, their
graphs did not show that full recovery occurred (their Fig. Z), so their
results must be interpreted with caution. The phenomenon we have
described is not that of animal hypnosis (3), which is able to suppress
some behavioral reactions to noxious stimuli.
In smiimary, this report has demonstrated a prolonged effect of elec-
troacupuncture on brain stem trigeminal and somatic evoked responses.
The effect was present in decerebrate animals, but was suppressed by cord
transection at Cl, suggesting that the mechanism is in the brain stem and
requires efferent connections.
When an acupuncture effect, as defined here, was obtained, it was
reproducible as long as the condition of the animal remained stable. The
94 KERR, WILSON, AND NIJENSOHN

location of the acupuncture needle was not critical; thus, when the effect
was obtained, the needle could be inserted in adjacent intermetacarpal
spaces and an equivalent acupuncture response elicited. This observation
gives little support for the concept of specific meridians, which is central
to traditional acupuncture lore. On two occasions, when an effect of good
amplitude was obtained by stimulation of the ipsilateral Hoku point,
stimulation of the contralateral Hoku point produced a smaller effect, and
stimulation of points on either lower extemity was without effect, This
suggests only that proximity of the acupuncture to the test region is of
importance and thus is in accord with the greater effectiveness of
peripheral nerve stimulation when the stimulated nerve is close to the
region of pain being treated. In turn, this may relate to the greater prob-
ability of central convergence between closely related systems.

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