Exp Brain Res (1991) 84:461-464
Experimental
Research Note
Participation of Ia reciprocal inhibitory neurons
in the spinal circuitry of the tonic neck reflex
Y. Yamagata, B.J. Yates, and V.J. Wilson
Rockefeller University, 1230 York Avenue, New York, NY 10021, USA
Received October 5, 1990 / Accepted November 16, 1990
Summary. As p a r t o f our studies o f the spinal circuitry
o f the tonic neck reflex, we have recorded extracellularly
f r o m Ia reciprocal inhibitory n e u r o n s o f the decerebrate,
labyrinthectomized cat. The activity o f a majority o f
neurons driven by stimulation o f the quadriceps nerve
was m o d u l a t e d by sinusoidal r o t a t i o n o f the neck; such
m o d u l a t i o n was m u c h less frequent in the case o f neurons
driven by stimulation o f nerves to m o r e distal muscles.
The results suggest that some o f the inhibition which is
part o f the tonic neck reflex is mediated by Ia reciprocal
inhibitory neurons, but that other p a t h w a y s m u s t also
play an i m p o r t a n t role.
Key words: Tonic neck reflex - Ia inhibitory n e u r o n s -
Neck receptors Cat
Introduction
N a t u r a l stimulation o f neck receptors, which evokes the
tonic neck reflex, modulates the activity o f m a n y spinal
neurons. Some, in the u p p e r cervical and u p p e r l u m b a r
cord, have been identified as short or long propriospinal
neurons projecting as far as the cervical or lumbosacral
enlargement (Brink et al. 1985). The activity o f neurons
in the cervical and l u m b a r enlargements, typically locat-
ed medially in laminae 7 or 8, is also m o d u l a t e d by neck
rotation (Wilson et al. 1984; J. Kasper, V.J. Wilson and
B.J. Yates, unpublished observations). So far, however,
none o f the m o d u l a t e d n e u r o n s in the enlargements have
been identified as to projection or function.
M o s t studies o f m o d u l a t i o n o f E M G during neck and
vestibular reflexes have been p e r f o r m e d on forelimb ex-
tensor muscles o f decerebrate cats (e.g. L i n d s a y et al.
1976; M a n z o n i et al. 1983; Wilson et al. 1986). Flexor
muscles are also involved in the reflex ( C o n w a y and
Rosenberg 1984), apparently being actively inhibited
while extensors are excited. In the l u m b a r cord, where
Off))rint requests to ." V.J. Wilson (address see above)
BrainResearch
9 Springer-Verlag 1991
neck and vestibular reflexes are also present, such inhibi-
tion could be p r o d u c e d by propriospinal neurons in L4
whose axons extend to the lumbosacral enlargement; the
activity o f some o f these neurons is m o d u l a t e d by neck
r o t a t i o n (Brink et al. 1985), and some m a k e inhibitory
connections with hindlimb m o t o n e u r o n s (Cavallari et al.
1987). A n alternate route for inhibition o f m o t o n e u r o n s
is v i a segmental inhibitory neurons. F o r an initial inves-
tigation o f identified interneurons participating in the
tonic neck reflex, we have n o w studied the response o f Ia
reciprocal inhibitory neurons (henceforth called Ia in-
hibitory neurons) to natural stimulation o f neck recep-
tors.
Methods
Experiments were performed on 16 cats, initially anesthetized with
2-3 % halothane vaporized in nitrous oxide and oxygen. After bilat-
eral labyrinthectomy, the animals were decerebrated intercollicular-
ly, and the anesthesia was discontinued. In order to stimulate neck
receptors, the cat's head was attached to a head rotator which was
computer-driven to generate roll and pitch stimuli (Suzuki et al.
1985). The animal was suspended from hip pins and by a clamp on
the dorsal process of an upper lumbar vertebra. Spinal cord seg-
ments L2- or L3-Sl were exposed by dorsal laminectomy. Ventral
roots L6-S1 (and sometimes L5) were cut, and their central ends
placed on bipolar platinum stimulating electrodes. Some or all of
the following hindlimb muscle nerves were prepared for stimulation
of their cut central ends with 150 gs rectangular stimuli : quadriceps
(Q), gastrocnemius-soleus (GS), plantaris (PL), flexor digitorum
longus (FDL), and biceps posterior-semitendinosus (BST). Q was
stimulated by means of a buried cuffelectrode, the other nerves were
placed on bipolar electrodes. Afferent volleys were recorded with a
ball electrode placed at the dorsal root entry zone, and stimuli were
expressed in terms of the threshold of the largest fibers in the nerve
(T). In some experiments we stimulated the area of the contralateral
ventral spinocerebellar tract (VSCT) with either a pair of ball
electrodes placed on the ventrolateral surface of the spinal cord at
L2, or with a pair of floating electrodes inserted into the spinal cord
at this level.
Extracellular unit activity was recorded from the L6 and L7
segments with glass micropipettes containing 2M NaC1 saturated
with Fast Green dye, and having resistances of 1-2 MfL Many
recording locations were marked by dye ejection (Thomas and
462
Wilson, 1965), whereas stimulating electrode locations within the
spinal cord were marked by electrolytic lesions.
Procedures for head rotation in vertical planes and data analysis
have been described in detail previously (Suzuki et al. 1985). In
brief, we determined whether the firing rate of a spontaneously
active unit was modulated by neck rotation using a combined roll
and pitch "wobble" stimulus (Schor et al. 1984), typically at fre-
quencies in the range 0.05-0.5 Hz and with an amplitude of 7.5 ~
Neurons were considered modulated if significant responses were
obtained at 2 or more frequencies, and not modulated if they were
tested and failed to respond at 2 or more frequencies. In instances
where only 1 frequency could be tested, or only one of several test
frequencies evoked a significant response, the neuron's response
was classified as questionable. For modulated neurons, the wobble
stimulus allows determination of the most effective direction of
stimulation, the response vector orientation. Bode plots of the
responses of modulated neurons were sometimes obtained using
sinusoidal stimuli oriented within 7.5 ~ of the response vector.
Results and discussion
In order to be certain that modulation was present in a
given preparation, experiments were begun, and ended,
by searching for responses to neck rotation in the medial
grey matter of L4, where they have been described
previously (Suzuki et al. 1985). In 2 preparations modu-
lation was initially weak or absent, but appeared after an
injection of 4-aminopyridine (1 mg/kg, iv) was given to
increase excitability (Jankowska et al. 1977). Once the
presence of modulation was established, we looked for
spontaneously active Ia inhibitory neurons which were
A B
Ires
g-,
C D
to
0.1
m Neuron threshold was < 1.4T. Thick
9O
"~ 60
30
0 i i i r
0.05 O.l 0.2 0.5 1 2ram
Stimulus Frequency (Hz)
identified by the usual criteria (Baldissera et al. 1981):
monosynaptic Ia input from a muscle nerve and presence
of recurrent inhibition. Because a small fraction of VSCT
neurons in the rostral part of the lumbosacral enlarge-
ment may also receive recurrent inhibition (Lindstr6m
and Schomburg 1973), some of the neurons we studied
in L6 were tested for a rostral projection in the contralat-
eral spinal cord.
We particularly studied the behavior of Q Ia inhibito-
ry neurons for two reasons. First, tonic neck reflexes are
known to be pronounced in proximal muscles. Second,
Lundberg and Bruggencate (1974) showed that Q Ia
inhibitory neurons receive monosynaptic input from
Deiters' nucleus; since vestibular and neck inputs often
converge (e.g. Wilson et al. 1984; Suzuki et al. 1985), it
would be expected that a large fraction would receive
neck inputs as well. Fourteen Q Ia inhibitory neurons
were identified in L6. Eleven had thresholds < 1.4T of the
Q nerve, 3 were driven at < 1.6-1.9T. Central latency
from the positive peak of the Q afferent volley measured
in L6 ranged from 0.7 to 1.1 ms. All neurons were in-
hibited by stimulation of the L6 ventral root, and none
of 10 neurons tested responded antidromically to rostral
spinal cord stimulation. Ten Q Ia inhibitory neurons
including the one illustrated in Fig. 1 were modulated by
neck rotation (3 in a preparation given 4-aminopyridine),
while the results for one were questionable. It might have
been supposed that, for a presumably homogeneous pop-
ulation of neurons, spatial behavior would be similar and
response vector orientations narrowly distributed. In-
IIom s
Fig. 1A-D. Neck-evoked modulation of
a Q Ia inhibitory neuron firing
spontaneously about 14 spikes/s. A PST
histogram of firing evoked by a 2T
stimulus to the Q nerve (115 sweeps).
arrow indicates time of stimulus, thin
arrow arrival of Q Ia volley at cord
dorsum in L6. B Recurrent inhibition
produced by stimulation of L6 ventral
root at arrow (106 sweeps). C Bode plot
of response of neuron to sinusoidal neck
rotation. D Filled circle shows recording
location of the modulated cell, marked
I I I
by dye ejection. Open circle shows
location of an unmodulated neuron in
the same track

A B
~ 1
.5
~ 0.1
o~ 90
o 60
3O
~ 0 i i r i i la neurons
0.05 0.i 0.2 0.5 1
Stimulus Frequency (Hz)
stead, they were widely scattered, with 5 vectors in the
roll and 5 in the pitch quadrants. This is consistent with
the hypothesis that premotor neurons with very different
vectors converge on individual motoneurons (Wilson et
al. 1986; Wilson 1988). Figure 2A shows the mean Bode
plot for all 10 modulated neurons. Mean phase of neuron
responses is comparable to that of medial L4 neurons, as
is mean gain at low frequencies, but the slope of the gain
curve is much flatter (compare with Fig. 5 of Suzuki et
al. 1985). Recording locations of 8 modulated neurons
(Figure 2B) correspond to the lateral half of the distribu-
tion of Ia inhibitory neurons seen in L6 by Jankowska
and Lindstr6m (1972).
In addition to the neurons in L6, we also recorded
from 18 Ia inhibitory neurons in L7. A few were mod-
ulated by neck rotation: 2/12 GS, with 1 questionable;
3/4 PL, with 1 questionable (the questionable response
was obtained in a cat given 4-aminopyridine); 0/2 FDL.
Although the sample is small, the frequency of modula-
tion of neurons inhibiting ankle and toe motoneurons
(5/18, 2 questionable) seems lower than for neurons in-
hibiting knee flexors (10/14, 1 questionable). In this re-
gard it is of interest that the monosynaptic connections
made by the vestibulospinal tract with Ia neurons inhibit-
ing knee flexors appear to be lacking for Ia neurons
inhibiting ankle and toe flexors (cf Lundberg and Brug-
gencate 1974).
Several conclusions can be drawn from our results.
First natural stimulation of neck, and presumably ves-
tibular, receptors can influence not only neurons that are
located medially (e.g. Wilson et al. 1984, 1985), but also
others that are located more laterally in the grey matter.
Obviously, presence of modulation depends not only on
a cell's location, but also on its function. Second, activ-
ity originating in neck receptors reaches some Ia inhibi-
tory neurons, perhaps via propriospinal neurons, and
can be added to the many different inputs already known
to converge upon them (Baldissera et al. 1981). Finally,
and most important, the results provide further evidence
463
Fig. 2. A Dynamics of responses of Q
la inhibitory neurons to neck
stimulation. Points show mean
response + / - SE of 10 neurons
studied at 3 or more frequencies;
values were not necessarily available
at each frequency for every neuron.
i i N is 9 or 10 for 0.05-0.5 Hz, 3 for
I mm 1.0 Hz. B Recording locations of 8 Q
that inhibition plays an active role in the tonic neck
reflex, and show that it is mediated in part by Ia inhibi-
tory neurons. The relative scarcity of modulation among
Ia inhibitory neurons involved in control of more distal
muscles indicates that much of the inhibition is due to
pathways involving other segmental interneurons, or in-
hibitory propriospinal neurons.
Acknowledgements. We thank Dr. Robert Schor for his comments
on the manuscript. Supported in part by N.I,H. grants NS02619
and DC00693.
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