We have previously reported that cells in cat areas 17 and 18 can show increases in response to non-optimal orientations or directions, commensurate with a loss of inhibition, during inactivation of laterally remote, visuotopically corresponding sites by iontophoresis of gamma-aminobutyric acid (GABA). We now present anatomical evidence for inhibitory projections from inactivation sites to recording sites where 'disinhibitory' effects were elicited. We made microinjections of [3H]-nipecotic acid, which selectively exploits the GABA re-uptake mechanism, < 100 microm from recording sites where cells had shown either an increase in response to non-optimal orientations during inactivation of a cross-orientation site (n = 2) or an increase in response to the non-preferred direction during inactivation of an iso-orientation site with opposite direction preference (n = 5). Retrogradely labelled GABAergic neurons were detected autoradiographically and their distribution was reconstructed from series of horizontal sections. In every case, radiolabelled cells were found in the vicinity of the inactivation site (three to six within 150 microm). The injection and inactivation sites were located in layers II/III-IV and their horizontal separation ranged from 400 to 560 microm. In another experiment, iontophoresis of biocytin at an inactivation site in layer III labelled two large basket cells with terminals in close proximity to cross-orientation recording sites in layers II/III where disinhibitory effects on orientation tuning had been elicited. We argue that the inactivation of inhibitory projections from inactivation to recording sites made a major contribution to the observed effects by reducing the strength of inhibition during non-optimal stimulation in recurrently connected excitatory neurons presynaptic to a recorded cell. The results provide further evidence that cortical orientation tuning and direction selectivity are sharpened, respectively, by cross-orientation inhibition and iso-orientation inhibition between cells with opposite direction preferences.

SUMMARY1. The visual resolving ability of different types of macaque retinal ganglion cells was estimated at different retinal eccentricities, by measuring the amplitude of modulated responses to black-white gratings of spatial frequencies near the resolution limit for each cell.2. The resolving ability of tonic, spectrally opponent ganglion cells was usually similar to that of phasic, non-opponent ganglion cells at similar eccentricities, except that at eccentricities greater than 10 deg some tonic ganglion cells with remarkably high resolution (up to ca. 15 cycles/deg) were found. Our cell sample was limited within the central 2 deg of the visual field, however.3. Only a small proportion of phasic ganglion cells showed an increase of mean firing level to gratings near the resolution limit. The maintained firing of tonic ganglion cells was higher than that of phasic ganglion cells.4. With red-black or green-black gratings, the resolution of phasic ganglion cells was unaffected. For red or green on-centre ganglion cells. a marked deterioration of resolving ability occurred when the grating was of a colour to which a cell responded poorly (green-black gratings for red on-centre cells. and red-black gratings for green on-centre cells). A slight improvement in resolving ability occurred when the grating was of an excitatory colour.5. For a sub-sample of cells. we compared resolution limit with centre size as determined from area-threshold curves. For both phasic and tonic ganglion cells, resolution limit (the period length just resolved) was about half the centre diameter, as is the case for cat ganglion cells. This implies that the centre sizes of phasic and tonic monkey ganglion cells are similar at most eccentricities.6. We attempt to relate these results to primate retinal anatomy and visual resolution, determined behaviourally.

Microiontophoresis of γ-aminobutyric acid (GABA) was used to reversibly inactivate small sites of defined orientation/direction specificity in layers II-IV of cat area 17 while single cells were recorded in the same area at a horizontal distance of ~350–700 jam. We compared the effect of inactivating iso-orientation sites (where orientation preference was within 22.5 deg) and cross-orientation sites (where it differed by 45–90 deg) on orientation tuning and directionality. The influence of iso-orientation inactivation was tested in 33 cells, seven of which were subjected to alternate inactivation of two iso-orientation sites with opposite direction preference. Of the resulting 40 inactivations, only two (5%) caused significant changes in orientation tuning, whereas 26 (65%) elicited effects on directionality: namely, an increase or a decrease in response to a cell's preferred direction when its direction preference was the same as that at an inactivation site, and an increase in response to a cell's nonpreferred direction when its direction preference was opposite that at an inactivation site. It is argued that the decreases in response to the preferred direction reflected a reduction in the strength of intracortical iso-orientation excitatory connections, while the increases in response were due to the loss of iso-orientation inhibition. Of 35 cells subjected to cross-orientation inactivation, only six (17%) showed an effect on directionality, whereas 21 (60%) showed significant broadening of orientation tuning, with an increase in mean tuning width at half-height of 126%. The effects on orientation tuning were due to increases in response to nonoptimal orientations. Changes in directionality also resulted from increased responses (to preferred or nonpreferred directions) and were always accompanied by broadening of tuning. Thus, the effects of cross-orientation inactivation were presumably due to the loss of a cross-orientation inhibitory input that contributes mainly to orientation tuning by suppressing responses to nonoptimal orientations. Differential effects of iso-orientation and cross-orientation inactivation could be elicited in the same cell or in different cells from the same inactivation site. The results suggest the involvement of three different intracortical processes in the generation of orientation tuning and direction selectivity in area 17: (1) suppression of responses to nonoptimal orientations and directions as a result of cross-orientation inhibition and iso-orientation inhibition between cells with opposite direction preferences; (2) amplification of responses to optimal stimuli via iso-orientation excitatory connections; and (3) regulation of cortical amplification via iso-orientation inhibition.

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Microiontophoresis of the inhibitory transmitter GABA was used to reversibly inactivate small sites of defined orientation specificity at a horizontal distance of some 600 microns from single cells recorded in area 18 of cat visual cortex, and the effects on orientation tuning were studied. The receptive fields of cells at the recording and inactivation sites overlapped extensively. During the inactivation of sites where the orientation preference differed by 45 degrees or more from that of a recorded cell ("cross-orientation" sites), 65% of 54 cells tested showed significant broadening of orientation tuning, with a mean increase in tuning width (measured at half the maximum response) of 93%, and an almost fourfold increase in the relative response to the orientation orthogonal to the optimum, compared with the response to the optimum; four cells essentially lost their orientation tuning. Broadening of tuning reflected an increase in response to nonoptimal orientations and was reversible upon termination of GABA application. The effects on orientation tuning typically peaked within 10-15 min of the onset of GABA iontophoresis with 50-100 nA ejecting currents, and could not be replicated by inactivating sites where the orientation preference was similar to that of a recorded cell; when the orientation preference at the inactivation sites was within 22.5 degrees of that of a recorded cell ("iso-orientation" sites), only 3 of 22 cells showed significant broadening of tuning, and in these cases, the effects were relatively weak (mean increase in tuning width of 39% and a negligible change in the relative response to the orientation orthogonal to the optimum). The effect of inactivating "iso-orientation" sites consisted primarily in an increase in response magnitude. The difference in the magnitude of the effects on orientation tuning elicited by inactivating "cross-orientation" and "iso-orientation" sites was highly statistically significant. Additionally, inactivation of "cross-orientation" or "iso-orientation" sites elicited differential effects on orientation tuning in 10 of the 13 cells in which direct comparisons were made. It is argued that the observed broadening of tuning was due to the loss of a "cross-orientation" inhibitory input, which normally sharpens orientation tuning by suppressing responses to nonoptimal orientations.