Translaminar differentiation of visually guided behaviors revealed by restricted cerebral cooling deactivation

The purpose of the present study was to test the hypothesis that superficial and deep layers within a single cerebral region influence cerebral functions and behaviors in different ways. For this test, we selected posterior middle suprasylvian (pMS) sulcal cortex of the cat, a suspected homolog of the area V5 complex of primates, because the region has been implicated in several visually guided behaviors. Cats were trained on three tasks: (1) discrimination of direction of motion; (2) discrimination of static patterns partially obscured by static or moving masks: and (3) visual detection and orienting. Cooling of cryoloops in contact with pMS sulcal cortex to 8 +/- 1 degreesC selectively and completely impaired performance on the two motion discrimination tasks (1 and 2), while leaving the detection and orienting task (task 3) unimpaired. Further cooling to 3 degreesC resulted in an additional complete impairment of task 3. The 8 degreesC temperature resulted in silencing of neuronal activity in the supragranular layers (I-III) and the 3 degreesC temperature silenced activity throughout the thickness of pMS sulcal cortex. The variation in behavioral performance with covariation of cryoloop temperature and vertical, but not lateral, spread of deactivation shows that deactivation of superficial cerebral layers alone was sufficient to completely impair performance on the two motion discrimination tasks, whereas additional deactivation of the deep layers was essential to block performance on the detection and orienting task. Thus, these results show a functional bipartite division of labor between upper and lower cortical layers that is supported by efferent connectional anatomy. Similar bipartite division into upper and lower layers may be a general feature of cerebral cortical architecture, signal processing and guidance of behavior.