Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat

The topography of lateral excitatory and lateral inhibitory connections wasstudied in relation to orientation maps obtained in areas 17 and 18. Smalliontophoretic injections of biocytin were delivered to the superficiallayers in regions where orientation selectivity had been mapped usingelectrode recordings of single- and multi-unit activity from variouscortical depths. Biocytin revealed extensive patchy axonal projections ofup to 3.5 mm in both areas while labelled somata occurred chiefly at theinjection site, indicating that the labelling was primarily anterograde.Two types of boutons could be clearly distinguished: (i) putativeexcitatory boutons either en passant or having a short stalk and (ii)inhibitory boutons which were invariably of the basket-type.Three-dimensional reconstructions of all labelled boutons showed that theexcitatory and the inhibitory networks had a distinctively differentrelationship to orientation maps. The overall distribution of connectionsshowed that 53-59% of excitatory and 46-48% of inhibitory connections wereat iso-orientation, +/-30 degrees; oblique-orientation, +/-(30-60) degrees,was shown by 30% of excitatory and 28-39% of inhibitory connections;cross-orientation was shown by 11- 17% of excitatory and 15-24% ofinhibitory connections. Although excitatory patches occupied mainlyiso-orientation locations, interpatch regions representing chieflynon-iso-orientations (oblique + cross orientation) were also innervated.There was considerable overlap between the excitatory and inhibitorynetwork. Nonetheless, inhibitory connections were more common thanexcitatory connections with non-iso- orientation locations. There was nosignificant difference between the orientation topography of area 17 andarea 18 projections. The results suggest that in general the lateralconnectivity system is not orientation specific, but shows a moderateiso-orientation preference for excitation and an even weakeriso-orientation preference for inhibition. The broad orientation spectrumof lateral connections could provide the basis for mechanisms thatrequiring different orientations, as for example in detecting orientationdiscontinuities.