Developmental Brain Research, 59 119911 23-29 23
Elsevier
BRESD 51230
Temporal limits of the susceptibility of depth perception to
proprioceptive deafferentations of extraocular muscles
Yves Trotter, Jean-Chrlstophe Beaux, Alexandre Pouget* and Michel Imbert
Instltut des Neurosctencer, Laboratotre des Neurosclences de la Vtston, Umversttd P e t M Curie, Paris (France)
(Accepted 13 November 1990)
Key words Depth perception, Binocular WSlOn, Extraocular propnoceptlon, Critical period, Behawor
In a prewous study, extraocular muscle propnoceptlon (E O M P ) was shown to play an important role in the postnatal development of
depth perception following unilateral or bdateral sections of the ophthalmic branch of the trlgemmal nerve (V:h nerve) performed at 6-8
weeks of age, the binocular thresholds were 2 to 3 times higher than m control animals Since the Vl-Sectlons produced no deficits when
performed m adults, the temporal hmlts of a period of susceptibility remained to be determined In order to assess the lower and upper hmlts
of the period during which these perceptual deficits could be induced, unilateral or bilateral V:secttons were performed in k~ttens at different
ages Depth perception thresholds were measured by using the lumping stand techmque Sections of the V 1 nerve only produced significant
impairments of the binocular depth thresholds when performed after 3 weeks of age They could be observed when umlateral sections were
performed at up to 13 weeks of age and with bdateral sections at up to 10 weeks of age These functional impairments appeared to remain
permanently through adult hfe
INTRODUCTION
Previous studies 3 5 27,28 have shown that extraocular
muscle proprloceptton (E O.M P) played an important
role m the development of area 17 cell properties All
these studies used dark reared kittens in which rapid
modifications of orientation selectivity or ocular domi-
nance were obtained following a brief period of visuo-
motor experience delayed until the middle of the period
of susceptibility of cortical cells to manipulations of visual
envtronmentt°; the section of the proprioceptlve afferents
performed just before the visual experience prevented or
slowed down these functtonal modifications In addition,
it was shown that m similar rearing conditions, kittens
were not able to acquire normal visually guided behavior
unless the E O M.P. afferents of at least one eye were
mtact during the visual exposure 13 Thus the main
hypothesis of the role of E O M P afferents, as revealed
by these experiments, is that they gate visual experience
dependent modifications of receptive fields and visuo-
motor coordination during postnatal development An-
other important role of E O M P_, specifically related to
binocular visual perception, was recently demonstrated in
the development of depth perception in kittens 11 the
E O.M_P deafferentatlons performed around 6-8 weeks
of age prevented the development of normal binocular
depth thresholds which remained close to monocular
levels of performance While deafferentations performed
in adult cats produced a deficit in some cases 8'9, In
others it they did not Thus the existence of a period of
susceptibility of depth perception to V 1 sections remained
to be determined The purpose of the present study was
to dehmtt the lower and upper temporal limits of this
period
MATERIALS AND METHODS
Ammals
Twelve kittens were used in this study Nine of them were
subjected to a undateral V:sectlon at 3 weeks of age (n = 3), 10-13
weeks (n = 3), 14 weeks (n = 2), an addlhonal kitten was operated
at 4 5 weeks of age The last 3 kittens were subjected to a bdateral
V:sectlon at 3weeks of age (n = 1), 95-115 weeks (n = 2) of
age (For the detaded surgical procedures, see ref_ 29 ) Briefly, the
surgery was performed under general anesthesia reduced by
intramuscular mlect~on of Althesln (Glaxo, 1 2 ml-kg 1, l e_ 10 8
mg kg ~ of alfaxolone and 3 6 mg kg ~ of alfadolone acetate) and
maintained by continuous rejection of mlthesln through a catheter
inserted m the radial vein A temporal approach was used to reach
the V~ nerve and a piece of it (2-3 ram) was removed near the
junction with the Gassenan ganglion After the surgery was
complete, antibiotics were apphed locally (soframycm) and by
intramuscular rejection (terramycin)
Behavtoural tests
The kittens were tramed to discriminate differences m depth using
the jumping stand technique 1~ 1~ They had to discriminate the
* Present address Computational Neuroblology Laboratory, Salk Institute, La Jolla, CA, U S A
Correspondence Y Trotter, Laboratolre de Neurosoences de la VLslon, Insmut des Neurosclences. Umverslt6 Pierre et Marie Curie, 9 Qual
Saint Bernard, 75005 Pans, France
0165-3806/91/$113 50 © 1991 Elsevier Science Publishers B V (Biomedical Division)