Functional selectivity of interhemispheric connections in cat visual cortex.

The functional specificity of callosal connections was investigated in visual areas 17 and 18 of adult cats, by combining in vivo optical imaging of intrinsic signals with labeling of callosal axons. Local injections of neuronal tracers were performed in one hemisphere and eight single callosal axons were reconstructed in the opposite hemisphere. The distributions of injection sites and callosal axon terminals were analyzed with respect to functional maps in both hemispheres. Typically, each callosal axon displayed 2 or 3 clusters of synaptic boutons in layer II/III and the upper part of layer IV. These clusters were preferentially distributed in regions representing the same orientation and the same visuotopic location as that at the corresponding injection sites in the opposite hemisphere. The spatial distribution of these clusters was elongated and its main axis correlated well with the preferred orientation at the injection site. These results demonstrate a specific organization of interhemispheric axons that link cortical regions representing the same orientation and the same location of visual stimuli. Visual callosal connections are thus likely involved in the processing of coherent information in terms of shape and position along the midline of the visual field, which may facilitate the fusion of both hemifields into the percept of a single visual scene.

Layout of transcallosal activity in cat visual cortex revealed by optical imaging.

The contribution of interhemispheric connections to functional maps in cat visual cortex was investigated by using optical imaging of intrinsic signals. In order to isolate the functional inputs arriving via the corpus callosum (CC) from other inputs, we used the split-chiasm preparation. The regions activated through the CC in visual areas 17 (A17) and 18 (A18) were localized and characterized by stimulating monocularly split-chiasm cats with moving, high contrast oriented gratings. We found that the CC mediates the activation of orientation selective domains in the transition zone (TZ) between A17 and A18 and occasionally within portions of both of these areas. We observed transcallosally activated orientation domains all along the TZ without any obvious interruption, and these domains were arranged around "pinwheel" centers. Interestingly, the TZ was divided in two parallel regions, which resemble A17 and A18 in their preferred temporal and spatial frequencies. Finally, we demonstrated that orientation maps evoked through the transcallosal and geniculo-cortical pathways were similar within the TZ, indicating a convergence of inputs of matching orientations in this region. These results contribute to a better understanding of the role of the CC in visual perception of orientations and shapes, at the level of the visual cortex.

Axonal topography of cortical basket cells in relation to orientation, direction, and ocular dominance maps.

The axonal (bouton) distributions of a layer 4 clutch cell (CC), two layer 3 medium-sized basket cells (MBC), and a layer 3 large basket cell (LBC) to orientation, direction, and ocular dominance maps were studied quantitatively. 1) The CC provided exclusively local projections (<380 microm from the soma) and contacted a narrow "niche" of functional representations. 2) The two MBCs emitted local projections (75% and 79% of all boutons), which were engaged with isoorientations (61% and 48%) and isodirections, and long-range projections (25% and 21%, >313 microm and >418 microm), which encountered cross-orientation sites (14% and 12%) and isoorientation sites (7% and 5%). Their direction preferences were mainly perpendicular to or opposite those of local projections. 3) The LBC provided the majority (60%) of its boutons to long-range distances (>437 microm). Locally, LBC boutons showed a rather balanced contribution to isoorientations (19%) and cross-orientations (12%) and preferred isodirections. Remotely, however, cross-orientation sites were preferred (31% vs. 23%) and the directional output was balanced. 4) Monte Carlo simulations revealed that the differences between the orientation specificity of local and long-range projections cannot be explained by a homogeneous lateral distribution of the boutons. 5) There was a similar eye preference in the local and long-range projection fields of the MBCs. The LBC contacted both contra- and ipsilateral eye domains. 6) The basket axons showed little laminar difference in orientation and direction topography. The results suggest that an individual basket cell can mediate a wide range of effects depending on the size and termination pattern of the axonal field.

Local lateral connectivity of inhibitory clutch cells in layer 4 of cat visual cortex (area 17).

To characterise spatially a major component of the anatomical basis of local lateral inhibition in layer 4 of cat visual cortex (area 17), we analysed the lateral distribution of neuronal somata postsynaptic to electrophysiologically characterised GABAergic clutch (basket) cell axons (CC1 and CC2). We report two main results. First, the clutch cell axons appear to show isotropic lateral connectivity near their cell body (less than 50 microm radius), but beyond this core region they show anisotropic lateral connectivity, preferring particular angular sectors around their cell body. Second, we estimated the probability of lateral connection for each axon arbor as a function of radial distance from the parent soma. We found that this radial function has a brief rising phase, to a peak at 30-45 microm, and a longer, exponential decaying phase, with a space constant of around 50 microm. The shape of the radial connection probability function suggests that most lateral inhibitory connections of clutch cells are formed with neurons in nearest-neighbour cortical columns. Taken together, the results suggest that these individual layer-4 clutch cell axons may inhibit all (isotropic) nearest-neighbour cortical columns with a relatively high probability of connection, but outside this core region may provide a type of anisotropic lateral inhibition of cortical columns with a radially decreasing probability of connection.

Topography of orientation centre connections in the primary visual cortex of the cat.

The functional topography of lateral connections to orientation-centre zones was studied by optical imaging of intrinsic signals in combination with tracer injections (fluorescent beads and biocytin) and electrophysiological recordings. Three-dimensional reconstruction of anterogradely labelled axon terminals and retrogradely labelled somata revealed a uniform distribution across all orientations in a non-patchy manner. The overall lateral extent of the labelling was 3-4 mm in layer 3, that is about half of the extent observed for orientation domain connections in the same layer. These bulk injection data are in contrast with the reportedly sharp orientation tuning of neurons of centre zones and suggest that orientation specificity here does not require highly specific connections. Nonetheless, another plausible scenario is that orientation centre connections are orientation specific but their specificity present at the single cell level cannot be revealed by bulk labelling due to their large spatial overlap.

Calculating direction maps from intrinsic signals revealed by optical imaging.

Previous optical imaging studies used the vector-summation (VS) method for calculating direction and orientation preference maps. However, for direction maps it often resulted in direction vectors which showed a steep angle to that of orientation vectors violating the 'aperture rule'. The present report provides a simple procedure for calculating direction preference maps using the 'electro- physiologist's ear' approach. This approach takes into account the strongest directional response component (vector-maximum, VM) in each pixel of the optical image, reminiscent of how electro- physiologists determine direction preference by audio-monitoring of the firing rate of neurons. The major advantage of this method is that the orthogonal relationship between orientation and direction preference vectors is preserved and that for most image pixels direction preference can be faithfully described by a single vector parameter. Here we used the VM method for calculating direction and the VS method for calculating orientation preference maps and quantified their spatial relationship. The results showed that, typically, an iso-orientation domain contained a pair of patches that preferred opposite directions orthogonal to the orientation. Rate-of-change maps for direction revealed that virtually all direction discontinuity lines linked orientation centres. Close to orientation centres, direction discontinuity lines ran chiefly parallel with iso-orientation lines, whereas more remotely they had either parallel or perpendicular courses.

Comparison of orientation maps obtained with different number of stimulus orientations.

The structure of orientation maps computed from a different number of stimulus orientations was studied in visual cortical area 18 of the cat. Single condition maps (SCMs) were obtained to 16 stimulus orientations, of which angle maps were generated using 4, 8, and 16 SCMs corresponding to multiples of 45, 22.5, and 11.25 degrees, respectively. The overall orientation distribution of the three types of maps was compared on a pixel-by-pixel basis. Twenty percent of the pixels of the 4-orientations maps differed by more than +/-17 degrees from those produced by 16 orientations. Maps of 8 orientations differed by 6.4 and 5.8% from those of 4 and 16 orientations, respectively. Structural differences between the maps were mainly found at locations displaying high rate of change in orientation preference, i.e., orientation centers and adjoining short, fracture-like zones. These changes included lateral shifts up to 155 microm (average: 38.7 microm) in the position of orientation centers and appearance/disappearance of orientation centers when compared between different conditions. In general, these changes were three times more frequent between maps of 4/8 and 4/16 orientations than 8/16 orientations. It is concluded that orientation maps should be calculated from activity maps representing 8 or more stimulus orientations.

Combined physiological-anatomical approaches to study lateral inhibition.

In the visual cortex, large basket cells form the cellular basis of long-range lateral inhibition. The present paper focuses on combinations of methods with which large basket cells can be studied in the context of extensive neuronal representations. In the first approach, the topographic relationship between large basket axons and known functional representations such as orientation, direction, and ocular dominance is analysed. Functional mapping is carried out using extracellular electrode recordings or optical imaging of intrinsic signals followed by 3-dimensional anatomical reconstruction of biocytin stained large basket cells in the same regions. In the second approach, the contribution of lateral inhibition to orientation and direction selectivity is assessed using the GABA inactivation paradigm and direct inhibitory projections from the inactivation to recording sites are demonstrated with biocytin staining and injections of [3H]nipecotic acid, a radioactive marker for GABAergic cells. The limitation of these approaches is that they can only be used in cortical regions which lie on the surface of the brain.

Orientation topography of layer 4 lateral networks revealed by optical imaging in cat visual cortex (area 18).

The functional specificity of corticocortical connections with respect to the topography of orientation selectivity was studied by optical imaging of intrinsic signals and bulk injections of fluorescent latex beads (green and red) and biocytin into layer 4. The distributions of retrogradely labelled cells and anterogradely labelled axon terminals were histologically reconstructed from all cortical laminae, and the resulting anatomical maps compared with the optically imaged functional maps. Layer 4 injections produced extensive horizontal labelling up to 2-3 mm from the injection centres albeit without the clear patchy pattern described after layer 2/3 injections (Gilbert & Wiesel 1989, J. Neurosci., 9, 2432-2442; Kisvárday et al. 1997, Cerebral Cortex, 7, 605-618). The functional (orientation) distribution of the labelled projections was analysed according to laminar location and lateral spread. With regard to the former, no major difference in the orientation topography between supragranular- (upper tier), granular- (middle tier) and infragranular (lower tier) layers was seen. Laterally, proximal and distal projections were distinguished and further dissected into three orientation categories, iso- (+/- 30 degrees ), oblique- (+/- 30-60 degrees ) and cross-orientations (+/- 60-90 degrees ) with respect to the orientation preference at the injection sites. The majority of distal connections (retrograde and anterograde) was equally distributed across orientations (35.4% iso-, 33.7% oblique-, and 30.9% cross-orientations) that are equivalent with a preponderance to dissimilar orientations (oblique- and cross-orientations, 64.6%). In one case, distal excitatory and inhibitory connections could be morphologically distinguished. For both categories, a marked bias to dissimilar orientations was found (excitatory, 63.7%; inhibitory, 86.6%). Taken together, these results suggest that the long-range layer 4 circuitry has a different functional role from that of the iso-orientation biased (52.9%, Kisvárday et al. 1997, Cerebral Cortex, 7, 605-618) layer 2/3 circuitry, and is perhaps involved in feature difference-based mechanisms, e.g. figure ground segregation.

Functional topography of single cortical cells: an intracellular approach combined with optical imaging.

Pyramidal cells mediating long-range corticocortical connections have been assumed to play an important role in visual perceptual mechanisms [C.D. Gilbert, Horizontal integration and cortical dynamics, Neuron 9 (1992) 1-13]. However, no information is available as yet on the specificity of individual pyramidal cells with respect to functional maps, e.g., orientation map. Here, we show a combination of techniques with which the functional topography of single pyramidal neurons can be explored in utmost detail. To this end, we used optical imaging of intrinsic signals followed by intracellular recording and staining with biocytin in vivo. The axonal and dendritic trees of the labelled neurons were reconstructed in three dimensions and aligned with corresponding functional orientation maps. The results indicate that, contrary to the sharp orientation tuning of neurons shown by the recorded spike activity, the efferent connections (axon terminal distribution) of the same pyramidal cells were found to terminate at a much broader range of orientations.

Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques.

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.

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 was studied in relation to orientation maps obtained in areas 17 and 18. Small iontophoretic injections of biocytin were delivered to the superficial layers in regions where orientation selectivity had been mapped using electrode recordings of single- and multi-unit activity from various cortical depths. Biocytin revealed extensive patchy axonal projections of up to 3.5 mm in both areas while labelled somata occurred chiefly at the injection site, indicating that the labelling was primarily anterograde. Two types of boutons could be clearly distinguished: (i) putative excitatory 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 the excitatory and the inhibitory networks had a distinctively different relationship to orientation maps. The overall distribution of connections showed that 53-59% of excitatory and 46-48% of inhibitory connections were at 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% of inhibitory connections. Although excitatory patches occupied mainly iso-orientation locations, interpatch regions representing chiefly non-iso-orientations (oblique + cross orientation) were also innervated. There was considerable overlap between the excitatory and inhibitory network. Nonetheless, inhibitory connections were more common than excitatory connections with non-iso-orientation locations. There was no significant difference between the orientation topography of area 17 and area 18 projections. The results suggest that in general the lateral connectivity system is not orientation specific, but shows a moderate iso-orientation preference for excitation and an even weaker iso-orientation preference for inhibition. The broad orientation spectrum of lateral connections could provide the basis for mechanisms that requiring different orientations, as for example in detecting orientation discontinuities.

GABA-induced inactivation of functionally characterized sites in cat striate cortex: effects on orientation tuning and direction selectivity.

Microiontophoresis of gamma-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 approximately 350-700 microns. 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.

GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): effects on direction selectivity.

1. Microiontophoresis of gamma-aminobutyric acid was used to reversibly inactivate small sites of defined orientation and direction specificity at a horizontal distance of 400-700 microns from single cells recorded in cat area 18. There was extensive or complete overlap between the receptive fields of cells at the recording and inactivation sites. A cell's directionality index [DI: 1 - (response to nonpreferred direction/response to preferred direction)], the response to the preferred direction, and orientation tuning width (measured at half the maximum response) were compared before and during inactivation of either iso-orientation sites (where the orientation preference was within 22.5 degrees) or cross-orientation sites (where it differed by 45-90 degrees). 2. During iso-orientation inactivation, 40 (73%) of 55 cells showed a significant (> 0.20) change in DI; the mean change in DI for these cells was 0.59. An additional cell showed a marked increase in response to the preferred direction that did not result in a change in DI. With one exception, the effects occurred in the absence of a significant (> 25%) change in orientation tuning width. 3. In most cases, the results were broadly predictable in the sense that iso-orientation inactivation predominantly affected a cell's response to the direction of motion of an optimally oriented bar that was closest to the preferred direction at the inactivation site: viz., a decrease in response to the preferred direction and an increase in response to the preferred or nonpreferred direction. 4. It is argued that the decreases in response were due to a reduction in the strength of intracortical iso-orientation excitatory connections made primarily between cells with similar direction preferences, whereas the increases in response involved a loss of iso-orientation inhibition. 5. In cases where remote inactivation caused an increase in response to the nonpreferred direction, comparable effects could be elicited when a mask left exposed only the excitatory subregion of the receptive field in S cells or the most responsive part of the excitatory discharge region in C cells. This implies extensive or complete spatial overlap between the profiles of excitation and inhibition in a cell's nonpreferred direction. 6. During cross-orientation inactivation, a significant change in DI was seen in only 14 (19%) of 73 cells and, with one exception, these changes were accompanied by increases in response to non-optimal orientations and significant broadening of orientation tuning. The effects of cross-orientation inactivation on directionality were presumably due to the loss of cross-orientation inhibition, which contributes primarily to orientation tuning. 7. Inactivation of the same site could cause an increase in response to the nonpreferred direction in cells recorded at iso-orientation sites and an increase in response to nonoptimal orientations and broadening of orientation tuning in cells recorded at cross-orientation sites. This is consistent with the notion that a single inhibitory neuron can contribute to the directionality or orientation tuning of different target cells depending on their location in the orientation map. 8. The results provide evidence for a major contribution of intrinsic mechanisms to the orientation tuning and direction selectivity of cells in cat area 18. It is proposed that two different intracortical processes are involved in the enhancement of orientation and direction selectivity: 1) suppression of responses to nonoptimal orientations and directions as a result of cross-orientation inhibition and iso-orientation inhibition; and 2) facilitation of responses to optimal orientations/directions via iso-orientation excitatory connections.

Relationship between lateral inhibitory connections and the topography of the orientation map in cat visual cortex.

The functional and structural topography of lateral inhibitory connections was investigated in visual cortical area 18 using a combination of optical imaging and anatomical tracing techniques in the same tissue. Orientation maps were obtained by recording intrinsic signals in regions of 8.4-19 mm2. To reveal the inhibitory connections provided by large basket cells, biocytin was iontophoretically injected at identified orientation sites guided by the pattern of surface blood vessels. The axonal and dendritic fields of two retrogradely labelled large basket cells were reconstructed in layer III. Their axonal fields extended up to 1360 microns from the parent somata. In addition to single basket cells, the population of labelled basket cell axons was also studied. For this analysis anterogradely labelled basket axons running horizontally over 460-1280 microns from the core of an injection site in layer III were taken into account. The distribution of large basket cell terminals according to orientation preferences of their target regions was quantitatively assessed. Using the same spatial resolution as the orientation map, a frequency distribution of basket cell terminals dependent on orientation specificity could be derived. For individual basket cells, the results showed that, on average, 43% of the terminals provided input to sites showing similar orientation preferences (+/- 30 degrees) to those of the parent somata. About 35% of the terminals were directed to sites representing oblique-orientation [+/- (30-60) degrees], and 22% of them terminated at cross-orientation sites [+/- (60-90) degrees]. Furthermore, the possible impact of large basket cells on target cells at different distances and orientation preferences was estimated by comparing the occurrence of orientation preferences with the occurrence of basket terminals on the distance scale. It was found that a basket cell could elicit iso-orientation inhibition with a high impact between 100-400 and 800-1200 microns, strong cross-orientation inhibition at approximately 400-800 microns, and oblique-orientation inhibition between 300-500 and 700-900 microns from the parent soma. The non-isotropic topography of large basket axons suggests a complex function for this cell class, possibly including inhibition related to orientation and direction selectivity depending on the location of the target cells and possible target selectivity.

Prevention of Ca(2+)-mediated action potentials in GABAergic local circuit neurones of rat thalamus by a transient K+ current.

1. Neurones enzymatically dissociated from the rat dorsal lateral geniculate nucleus (LGN) were identified as GABAergic local circuit interneurones and geniculocortical relay cells, based upon quantitative analysis of soma profiles, immunohistochemical detection of GABA or glutamic acid decarboxylase, and basic electrogenic behaviour. 2. During whole-cell current-clamp recording, isolated LGN neurones generated firing patterns resembling those in intact tissue, with the most striking difference relating to the presence in relay cells of a Ca2+ action potential with a low threshold of activation, capable of triggering fast spikes, and the absence of a regenerative Ca2+ response with a low threshold of activation in local circuit cells. 3. Whole-cell voltage-clamp experiments demonstrated that both classes of LGN neurones possess at least two voltage-dependent membrane currents which operate in a range of membrane potentials negative to the threshold for generation of Na(+)-K(+)-mediated spikes: the T-type Ca2+ current (IT) and an A-type K+ current (IA). Taking into account the differences in membrane surface area, the average size of IT was similar in the two types of neurones, and interneurones possessed a slightly larger A-conductance. 4. In local circuit neurones, the ranges of steady-state inactivation and activation of IT and IA were largely overlapping (VH = 81.1 vs. -82.8 mV), both currents activated at around -70 mV, and they rapidly increased in amplitude with further depolarization. In relay cells, the inactivation curve of IT was negatively shifted along the voltage axis by about 20 mV compared with that of IA (Vh = -86.1 vs. -69.2 mV), and the activation threshold for IT (at -80 mV) was 20 mV more negative than that for IA. In interneurones, the activation range of IT was shifted to values more positive than that in relay cells (Vh = -54.9 vs. -64.5 mV), whereas the activation range of IA was more negative (Vh = -25.2 vs. -14.5 mV). 5. Under whole-cell voltage-clamp conditions that allowed the combined activation of Ca2+ and K+ currents, depolarizing voltage steps from -110 mV evoked inward currents resembling IT in relay cells and small outward currents indicative of IA in local circuit neurones. After blockade of IA with 4-aminopyridine (4-AP), the same pulse protocol produced IT in both types of neurones. Under current clamp, 4-AP unmasked a regenerative membrane depolarization with a low threshold of activation capable of triggering fast spikes in local circuit neurones.(ABSTRACT TRUNCATED AT 400 WORDS)

Functional and structural topography of horizontal inhibitory connections in cat visual cortex.

The functional organization of long-horizontal inhibitory connections was studied in cat visual cortical area 17, using a combination of electrophysiological recording and anatomical tracing in the same tissue. Orientation maps were obtained by recording multiunit activity from layer III at regular intervals (100-300 microns) in a region of approximately 1.3 mm2 of cortex at a depth corresponding to the location of the basket cell axons reconstructed later. Before the physiological mapping, the neuronal tracer biocytin had been iontophoretically injected at one functionally characterized site. On the basis of light microscopic features a total of five biocytin-labelled large basket axons, BC1-BC5, were reconstructed from series of horizontal sections of two cats. The parent somata and dendritic fields of three axons (BC1, BC4 and BC5) could also be reconstructed. The axonal field of basket cell BC1 had an overall lateral spread of 1.8 mm. The axons of basket cells BC4 and BC5 spanned a distance of 3.05 and 2.85 mm, respectively. The distribution pattern of histologically reconstructed recording sites and of five labelled basket cell axons were directly compared in the same sections. The results show that a single large basket cell provides input to regions representing the whole range of orientations, i.e. iso-orientation (+/- 30 degrees), oblique orientation (+/- [30-60] degrees) and cross-orientation (+/- [60-90] degrees) to that at the basket cell's soma. Furthermore, the differential effect mediated by the same large basket cell at sites of different orientation preference was numerically estimated for two basket cells (BC4 and BC5) whose preferred orientations could be determined on the basis of recording sites adjacent to their parent somata. We counted the number of axonal terminals of these basket cells at iso-, oblique- and cross-orientation sites and found no significant difference in the average density of terminals at sites of either orientation preference. The functional topography of large basket cell axons indicates that the same basket cell can mediate iso-, oblique- and cross-orientation inhibition at different sites. Hence, we assume that large basket cells serve a complex physiological role depending on the location of target cells in the orientation map.

Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition.

Anatomical and immunohistochemical data indicate that, in addition to pyramidal neurons, nonpyramidal cells are exposed to perisomatic inhibition mediated by gamma-aminobutyric acid (GABA)-containing terminals. However, no direct information is available as yet for the origin of GABAergic inputs to morphologically identified GABAergic neurons. In the present paper, we studied the topographical and synaptic relationship between identified GABAergic large basket cells and their immunohistochemically characterized target neurons revealed by parvalbumin-(PV) and GABA immunostaining in the same material. Extracellularly applied biocytin labelled a total of 36 and 9 large basket cells in layers III and V, respectively. Of these, the axonal arborizations of two basket cells, BC1 and BC2, were reconstructed. The axon of BC1 occupied an area of about 2.3 x 2.2 mm2 in layer III, providing a total of 2,755 terminals. The axon of BC2 showed an overall extent of 3.8 x 1.7 mm2 in layer V elongated in the anteroposterior direction, and gave off 1,599 terminals. Immunostaining for PV was carried out to reveal putative nonpyramidal targets for BC1 and BC2. It was found that in addition to immunonegative cells, they established an average of 4-6 perisomatic contacts onto each of 58 (BC1) and 33 (BC2) PV-immunopositive neurons. For electron microscopic verification, 23 terminals apposing the somata of 12 PV-immunopositive neurons were selected. Each terminal was found to establish symmetrical (type II) contacts with its targeted cell. Furthermore, the distribution of soma area of the targeted PV-immunopositive cells and of identified large basket cells showed remarkable similarity, implying that the two populations were actually the same. In addition, the average horizontal distance between neighbouring PV-immunopositive target cells was found to be about 100 microns both in layers III and V. The results suggest that in area 18 the same large basket cell provides direct inhibition to certain pyramidal cells and facilitation to other pyramidal neurons, by inhibiting their presynaptic large basket cells at regular intervals.