The functional roles of the major visuo-motor pathways were studied in
lamprey. Responses to eye illumination were video-recorded in intact
and chronically lesioned animals. Postural deficits during spontaneous
swimming were analyzed to elucidate the roles of the lesioned structu
res for steering and postural control. Eye illumination in intact lamp
reys evoked the dorsal light response, that is, a roll tilt toward the
Light, and negative phototaxis, that is a lateral turn away from ligh
t, and locomotion. Complete tectum-ablation enhanced both responses. D
uring swimming, a tendency for roll tilts and episodes of vertical upw
ard swimming were seen. The neuronal circuitries for dorsal light resp
onse and negative phototaxis are thus essentially extratectal. Respons
es to eye illumination were abolished by contralateral pretectum-ablat
ion but normal after the corresponding lesion on the ipsilateral side.
Contralateral pre tectum thus plays an important role for dorsal ligh
t response and negative phototaxis. To determine the roles of pretecta
l efferent pathways for the responses, animals with a midmesencephalic
hemisection were tested. Noncrossed pretecto-reticular fibers from th
e ipsilateral pretectum and crossed fibers from the contralateral side
were transected. Eye illumination on the lesioned side evoked negativ
e phototaxis but no dorsal light response. Eye illumination on the int
act side evoked an enhanced dorsal light response, whereas negative ph
ototaxis was replaced with straight locomotion or positive phototaxis.
The crossed pretecto-reticular projection is thus most important for
the dorsal light response, whereas the noncrossed projection presumabl
y plays the major role for negative phototaxis. Transection of the ven
tral rhombencephalic commis sure enhanced dorsal light response; negat
ive phototaxis was retained with smaller turning angles than normal. S
pontaneous locomotion showed episodes of backward swimming and deficie
nt roll control (tilting tendency). Transections of different spinal p
athways were performed immediately caudal to the brain stem. All spina
l lesions left dorsal light response in attached state unaffected; thi
s response presumably is mediated by the brain stem. Spinal hemisectio
n impaired all ipsiversive yaw turns; the animals spontaneously rolled
to the intact side. Bilateral transection of the lateral columns impa
ired all yaw turns, whereas roll control and dorsal light response wer
e normal. After transection of the medial spinal cord, yaw turns still
could be performed whereas dorsal light response was suppressed or ab
olished, and a roll tilting tendency during spontaneous locomotion was
seen. We conclude that the contralateral optic nerve projection to th
e pretectal region is necessary and sufficient for negative phototaxis
and dorsal light response. The crossed descending pretectal projectio
n is most important for dorsal light response, whereas the noncrossed
one is most important for negative phototaxis. In the most rostral spi
nal cord, fibers for lateral yaw turns travel mainly in the lateral co
lumns, whereas fibers for roll turns travel mainly in the medial spina
l cord.