G. Broton
Abstract
1. Introduction

B. Calancie t al. /Electroencephalography nd clinical Neurophysiology 101 (1996) 304-315 305
velopment of these reflexes post-injury. Our evidence to
date leads us to conclude that these reflexes are due to the
establishment of new synaptic onnections made by sen-
sory afferents of lower extremity origin onto cervical
motoneurons, caudal to the level of a severe cervical spi-
nal cord injury. While of no apparent functional benefit o
the individual, establishment of such connections does
serve as an example of plasticity and the capacity for new
growth within the adult human spinal cord, and helps
account for the 'spread' of involuntary movements from
lower to upper limb muscles during a typical spasm in
such a subject. Preliminary findings have been presented
in abstract form (Calancie and Broton, 1992; Calancie,
1995).
2. Methods and materials
Computerscope) and simultaneously processed through
two 6-channel audio mixers (Rane RM 26) connected to a
loudspeaker for audio feedback.
Typically, 12 channels of EMG activity were recorded,
at least 8 of which were from upper limb muscles, includ-
ing different combinations of the wrist flexors (flexor
carpi radialis; FCR), wrist extensors (extensor carpi ra-
dialis; ECR), flexor pollicis longus (FPL), extensor polli-
cis longus (EPL), abductor digiti minimi (ADM), abduc-
tor pollicis brevis (APB, including adductor pollicis), and
different interosseous (INT) muscles, bilaterally. We also
recorded EMG from soleus and abductor hallucis (AbH;
an intrinsic foot muscle) on the side of the lower extrem-
ity being stimulated, for which the presence or absence of
the M-wave or H-reflex served as a means of localizing
the tibial or posterior tibial nerves for stimulation.
2.1. Subjects 2.3. Stimulation
Responses in upper limb muscles to stimulation of
lower extremity cutaneous receptive fields (i.e. areas
within which cutaneous stimulation could evoke re-
sponses from an identified motor unit in an upper limb
muscle) were obtained from 15 subjects with motor-
complete injury to the cervical spinal cord. All subjects
had sustained their spinal cord injury more than 1 year
prior to examination (i.e. their injury status was consid-
ered to be chronic for the sake of this study). Subjects
included 11 men and 4 women, whose ages ranged be-
tween 21 and 46 years. All subjects gave informed con-
sent for their participation in this protocol, which was
approved by the Institutional Review Board of this Uni-
versity.
2.2. EMG recording
Muscle electromyogram (EMG) was recorded with
pairs of gross EMG electrodes. These were either surface
Ag/AgCI electrodes (1 cm diameter; 5-7 cm spacing) or
non-insulated EEG-type subdermal wire electrodes (1 cm
length). The recording characteristics (impedance, muscle
volume sampled, frequency response) of the wire pairs
did not differ appreciably from the surface electrodes
used (Hugon, 1973). Because interlimb reflexes often in-
volved recruitment of only one or two single motor units
in a particular upper limb muscle, in many cases it was
possible to clearly distinguish the action potential of that
motor unit with such electrodes. However, in some cases
for which multiple motor units were recruited by sensory
stimulation to a lower limb, a concentric bipolar needle
electrode was also used, in order to achieve more selec-
tive single motor unit recordings. EMG signals were pre-
amplified close to the source, filtered and amplified
(100Hz-5 kHz; 1K or 10K gain), and stored on VHS
tape after being digitized (Vetter 4000AS). EMG signals
were displayed on a computer monitor (RC Electronics
All stimuli were delivered to the lower limbs at or dis-
tal to the knee. Stimuli included: (1) square-wave, con-
stant voltage electrical shocks delivered transcutaneously
via surface lectrodes or subcutaneously via non-insulated
needle electrodes to either mixed nerves (tibial or poste-
rior tibial) or to patches of skin within identified cutane-
ous receptive fields; (2) light stroking of the skin with a
blunt probe; (3) controlled cutaneous indentation via
Semmes-Weinstein monofilaments (equivalent o 'Von
Frey hairs'); (4) application of cold via either a controlled
thermal device (Peltier device; Thermal Devices Inc.) or
with ice, and radiant heat from a small lamp focused to a
5 mm spot; (5) pulling and bending of single hairs on
the toe, foot or leg using a needle micro-holder; and (6)
vibration of cutaneous receptive fields with varying
frequency and displacement, using a Ling 203 linear mo-
tor.
Electrical stimuli were delivered from a Grass $88
stimulator via an SIU5 stimulus isolation unit. Stimulus
rates, intensities and durations were varied and are re-
ported in Section 3. The influence of temporal summation
was investigated by comparing the response to single
shocks (typically 0.2-0.5 Hz) to those of brief trains of
shocks at high frequency (2 or 3 pulses at 500 Hz). Stim-
ulus rates of between 0.1 and 1 Hz were used to investi-
gate the phenomenon of 'wind-up' (increasing neuronal
discharge intensity to repeated stimuli at low frequencies)
(Mendell, 1966; Xu et al., 1995) of the upper limb motor
response.
2.4. Procedure
Subjects were given single-channel auditory feedback
of EMG and asked to attempt voluntary, isolated contrac-
tions of each muscle in turn to confirm whether or not it
was under some degree of volitional control. Electrical
stimulus pulses were then applied to the tibial nerve at the