Yawning
and Penile Erection induced in Rats by Cortical
Spreading Depression
Joseph Houston
Institute of Physiology,
Czeehosloyak Academy of Sciences,
Prague
Behaviour can be stimulated as well as
disrupted by cortical spreading depression (CSD)
the massive wave of neural depolarization and
subsequent EEG depression which can be induced
to spread slowly over a cortical hemisphere by
injection of KCl. Eating, drinking and locomotor
behaviour have been elicited in rats by
administering single waves of CSD (ref. 1).
Consummatory behaviour was most likely to be
elicited if an animal had extensive feeding
experience in the testing chamber.I wish to
describe two further effects of single waves of
CSD, the induction of penile erections and of
stretching and yawning responses.
Waves of spreading depression were generated
either by injecting K+ electrophoretically into
the occipital cortices of male hooded rats, or
by pressure injection of about 1 µl. of 6%
KCl solution. For electrophoresis, refillable
glass cannulae containing 25% KCl and a coiled
silver wire were implanted chronically. An
anodal current of 1 mA, passed between the wire
and an indifferent electrode over the cerebellum
for about 10s, released sufficient K + to
trigger one wave of CSD (ref. 2). For pressure
injection, steel cannulae were placed over the
occipital cortices, and KCI was injected from
smaller needles attached to flexible
polyethylene tubing. The corresponding steady
potential changes (SPCs) were recorded
bilaterally across Ag-AgCl electrodes placed 2
mm lateral to bregma. The reference electrode
was 10 mm anterior to bregma at the midline. The
animals were able to eat and drink freely inside
a box with one transparent wall. Waves of CSD
were administered at least 5 mn after any
manifestation of the behaviour we were
monitoring. Waves were separated by at least 15
mn.
Although much less consummatory behaviour
was elicited by CSD than when rats were
pretrained to drink, the rats yawned
frequently after a wave of CSD. Yawning was
never observed in the experimental chamber
except after CSD. Typically, the response
consists of stretching, with extension and
raising of a forepaw, accompanied by wide
opening of the mouth. Frequently chewing
movements preceded a yawning response by 1-30 s.
Yawning was observed in seventeen out of twenty
rats tested.
Fig. 2 (top) shows the distribution of onset
times of seventythree cases of elicited yawning
in six rats. Of these 25% were elicited by CSD
applied to both cortical hemispheres. This
histoggram shows the proportion of times yawning
commenced in any of the 1 mn intervals following
injection of K+. Onsets were measured from an
arbitrary synchronization point of maximal
depolarization at the anterior (frontal cortex)
recording electrode. Thus,whenever yawning
accompanied a wave of CSD, it was most likely to
occur first about 5 min after initiation of CSD.
The mean number of yawns elicited by each of the
seventythree CSDs was 4.3. Fig. 2 (bottom) shows
the distribution of all the 314 elicited yawns.
At least three waves of CSD usually necessary
before a rat yawned. On four occasions yawning
followed the first wave of CSD, but in each case
the animals had experience of CSD on the
previous day. Apparently facilitation of yawning
after CSD persists for some time. Drowsiness
generally coincided with yawning.
When yawning followed waves of CSD it was
often possible to elicit the
chewing-stretching-yawning sequence by startling
the animal with a sudden noise or by tapping on
the chamber.
Thus CSD has two effects, namely, repeated
waves induce a disposition to yawn, and
subsequently single waves can the yawning
response. The metabolic, hormonal, and
physiological changes which accompany CSD (ref.
3) may provide insight into the central
mechanism of yawning, of which little is
known.
The distribution of the onset of yawning
corresponds closely to the distribution of the
other behaviours elicited by CSP in slightly
different conditions. This fact, in conjunction
with the data on the induction of yawning in
startled animals, suggests that, given a
readiness to yawn, the yawning response occurs
an after effect of arousing stimulation,
possibly when arousal value of the stimulation
has dissipated (the lateencies of yawning
elicited by startling varied from 1to 20 s). ln
such scheme, a yawn could have some regulatory
function in reponse to a sudden mobilization of
neural resources.
During and between bouts of CSD which induced
yawning six rats frequently exhibited penile
erections. Typically they arched their backs,
trembled, reared up on their hind legs, and
exhibited a remarkable erection, often with
waving of the penis. This was followed by
licking and grooming of the genital area. The
relationship in these experiments between
yawning and sexual excitement is not clear, but
it is interesting in the light of recent reports
of yawning and sexual arousal induced
concurently by injection of adrenocorticotropin
into the brain of rats, rabbits and cats and by
the release of erections and yawning in monkeys
in response to their mirror images.
