Neuronal responsiveness in areas 19 and 21a,and the posteromedial lateral suprasylvian cortex of the cat

Responsiveness to slits and pattern stimuli was quantified in a total of 68 cells sampled in the posterior extreme of the lateral suprasylvian (PS) cortex as response indices. The cells were studied in relationship to their locations in several subareas of the PS cortex, including areas 19 (n=15) and 21a (n=32) and the posteromedial lateral suprasylvian cortex (PMLS; n=21). These subareas were identified based on retrograde labelling from area 17 and also supplemented with photic responsiveness. This analysis revealed that each cortical area contains cells expressing different combinations of stimulus features. Area 19 contained two major groups of cells: (1) those with strong end-stop selectivity combined with moderate orientation or direction selectivity, and (2) those with weak end-stop selectivity combined with strong orientation selectivity. The groups of cells with strong or moderate orientation selectivity showed a strong preference for stripe over visual noise patterns and relatively large modulatory responses to motion of individual stripes. The PMLS contained one major group of cells with strong end-stop and direction selectivities and with poor orientation selectivity. They also showed stronger preference for visual noise than cells in the other cortical areas and rather weak modulatory responses. Area 21a contained only one group of cells with strong orientation selectivity and length summation property rather than end-stop selectivity, and they also lacked direction selectivity. These cells exhibited a strong preference for stripe patterns and moderate or weak modulatory responses. Altogether, these findings indicate that each cortical area is specialized in expressing different stimulus features. The two groups of cells in area 19 may encode the position and motion of discontinuous visual elements such as corners and line ends and continuous elements such as lines and edges. PMLS cells may encode the motion of single elements or associated motion of multiple discontinuous elements such as textures and backgrounds. Area 21a cells may specifically encode the orientation of long, continuous elements such as lines and edges. In support of this view, two types of statistical analyses demonstrated that the combinations of the response properties expressed in individual PS cells are highly correlated with their locations in cortical areas and that the anatomical locations of individual PS cells are reliably predicted from the sets of response indices expressed in these cells.     

Responses of neurons in the cat posteromedial lateral suprasylvian cortex to moving texture patterns

The posteromedial lateral suprasylvian cortex represents a point of convergence between the geniculostriate and extrageniculostriate visual pathways. Given its purported role in motion analysis and the conflicting reports regarding the texture sensitivity of this area, we have investigated the response properties of cells in PMLS to moving texture patterns ("visual noise"). In contrast to previous reports, we have found that a large majority of cells (80.1%) responds to the motion of a texture pattern with sustained discharges. In general, responses to noise were more broadly tuned for direction compared to gratings; however, direction selectivity appeared more pronounced in response to noise. The majority of cells was selective for drift velocity of the noise pattern (mean optimal velocity: 26.7 degrees /s). Velocity tuning was comparable to that of its principal thalamic input, the lateral posterior pulvinar nucleus. In general, responsiveness of cells in the posteromedial lateral suprasylvian cortex increased with increasing texture element size, although some units were tuned to smaller element sizes than the largest presented. Finally, the magnitude of these noise responses was dependent on the area of the visual field stimulated. In general, a stimulus corresponding to roughly twice the size of the receptive field was required to elicit an equivalent half-maximal response to that for gratings.The results of this study indicate that the majority of cells in the posteromedial lateral suprasylvian cortex can be driven by the motion of a fine texture field, and highlight the importance of this area in motion analysis.     

Orientation tuning of cells in areas 17 and 18 of the cat's visual cortex

Summary Sharpness and symmetry of orientation tuning were quantitatively investigated and compared in ninety-seven cells from areas 17 and 18 of the lightly-anaesthetised feline visual cortex.Halfwidths of orientation tuning at half-height ranged between 5 ° and 73 ° for long stimuli, with an extreme exception at 111 ° (excluding untuned cells).There was a tendency for cells in area 18 to be more broadly tuned than those in area 17, due largely to the relatively sharp tuning of area 17 simple cells. Confirming previous work, simple cells were more sharply tuned than complex cells in area 17. In area 18, there was no clear distinction in sharpness of tuning between complex type 1 cells (equated with area 17 simple cells), complex type 2 cells (equated with area 17 complex cells), or hypercomplex cells.Approximately 60% of cells in both areas were asymmetrically tuned for orientation: ratios of half-widths to either side of the optimal orientation ranged from 1.0–3.0, exceptionally 5.8. Asymmetry of tuning was more marked in area 18 than in area 17, except that area 18 complex type 2 cells as a group were relatively symmetrically tuned for orientation.Occasional cells with different preferred orientations for opposite directions of motion, for each peak of a bimodal response to a single direction, or for each half of the receptive field were also observed. The latter are described in the following paper (Hammond and Andrews, 1978b).     

Lesion of areas 17/18/19: effects on the cat's performance in a binary detection task

Summary The ability of two cats to discriminate between two geometrical outline patterns in the presence of superimposed Gaussian visual noise — i.e. in a binary detection task — was tested before and after bilateral removal of cortical areas 17, 18 and 19. The detection probability P_D was measured as a function of the signal-to-noise ratio. After a lesion of areas 17, 18 and 19 both cats were unable to carry out the discrimination tasks. Their detection performance dropped to chance level, but after an extensive phase of retraining (3 months) they regained the ability to discriminate visual patterns. It was thus possible to obtain detection curves and to determine a measure of a performance which is predominantly bound to be mediated by extra-geniculo-cortical systems. The detection capacity was abnormally low with both large and small patterns. However, the detection of stationary small patterns was similar to the performance of cats with 17/18 lesions; the detection of stationary large patterns was only slightly better than the detection of small patterns and much worse than the comparable performance of cats with 17/18 lesions. Furthermore the cats with lesions of areas 17/18/19 were unable to discriminate moving patterns, their performances being at chance level, whereas for the cats with 17/18 lesions the detection of moving and stationary patterns was equal.Supported by the Deutsche Forschungsgesellschaft     

Afferent connections of columns of area 17 and 18 of the cerebral cortex formed by neurons of dorsal lateral geniculate bodies in cats

Horseradish peroxidase (HRP) was injected microiontophoretically into nine single area 17 columns and six area 18 columns of the cat's cerebral cortex. Within the dorsal lateral geniculate nucleus most of the labelled cells were found in the laminae A. The ratio of HRP-labelled cells in lamina A to those in lamina Al (A/A1) was estimated. After injection of HRP in area 17 columns this ratio varied from 0.5 to 2.5, while after HRP injection into area 18 columns it varied from 0.2 to 0.9. These data may indicate that in the areas studied contain the columns that receive afferents from both ipsilateral and contralateral eyes.     

Projections from visual cortical area 19, the posterior medial lateral suprasylvian area and the lateral posterior-pulvinar complex of the thalamus to areas 17 and 18 in young kittens

Retrogradely transported horseradish peroxidase (HRP) or HRP conjugated to wheat germ agglutinin was used to demonstrate projections from area 19, the posterior medial lateral suprasylvian area (PMLS) and the lateral posterior-pulvinar complex (LP-PC) of the thalamus to areas 17 and 18 of the visual cortex in young kittens. Areas 17 and 18 in kittens, as in adult cats, receive association fibres from cells lying mainly in deep cortical laminae in area 19 and PMLS, and projections from the LP-PC of the thalamus.     

Regressive changes among corticocortical neurons projecting from the lateral suprasylvian cortex to area 18 of the kitten's visual cortex

The postnatal development of corticocortical neurons projecting from the medial bank of the lateral suprasylvian cortex to area 18 of the kitten's visual cortex was examined using retrograde fluorescent tracers. Area 18 was injected in young kittens aged nine days or less and in older kittens aged 30 days or more. Many of the injected kittens were perfused with fixative four to five days later, but some of the youngest were killed after longer survival periods of 35-50 days (long-survival animals). Labelled neurons in the medial bank of the lateral suprasylvian cortex were densely distributed in both superficial layers (II and III) and deep layers (V and VI) in the kittens injected less than nine days postnatal, irrespective of whether survival was short or long, but they were found almost exclusively in layers V and VI in the old, short-survival animals. Only in the group of old kittens did we find a clear topographical arrangement of projections in the rostrocaudal direction and a correlation between the rostrocaudal lengths of the injection sites and labelled areas. In the other two groups, for a similarly sized injection site, the labelled areas were much longer rostrocaudally than in the old, short-survival kittens, and occupied roughly the posterior two-thirds of the medial bank of the lateral suprasylvian cortex, irrespective of the positions of the injections. In the frontal plane, topography was unclear in all groups. These findings demonstrate that there is considerable postnatal refinement of the projection from the medial bank of the lateral suprasylvian cortex to area 18. This involves a loss of connections originating from superficial layers and a decrease of convergence with the appearance of topography. Our results from long-survival kittens suggest that most of the early exuberant population of corticocortical neurons projecting from the medial bank of the lateral suprasylvian cortex to area 18 survive beyond the first postnatal month but undergo axonal elimination during this period.     

Thalamo-cortical connections and their correlation with receptive field properties in the cat's lateral suprasylvian visual cortex

Summary Areas PMLS and PLLS of the cat's lateral suprasylvian visual cortex display an interesting global organization of local features in their single unit response properties: direction preference is centrifugally organized and velocity preference increases with eccentricity. In addition it has previously been shown that binocular interactions are strongest around the visual field center. This characterizes the LS areas as apt for the analysis of optic flow fields and for visual processing in various kinds of visuomotor tasks (Rauschecker et al. 1987). In the present study we analysed the types of input to LS from the optic chiasm, the corpus callosum and from two thalamic relay nuclei (lateral posterior and lateral geniculate) that constitute important sources of afferent information to the LS areas. We were interested in learning how the afferent (and efferent) connections between LS and these structures relate to the response properties of LS neurons. Overlap of an RF into the ipsilateral hemifield was virtually always associated with callosal input. Latency differences between responses to electrical stimulation of the optic chiasm and the thalamic sites indicated almost exclusively fast-conducting Y-input to LS. Correlation of response latencies with receptive field properties revealed the following correspondences: A positive correlation was found between LP-latency and RF-size matching the dependence of RF size on laminar origin. The type of correlation found between LP-latency and directional tuning of LS cells suggests that an interaction between thalamic and other inputs may be responsible for direction selectivity in LS. Finally, correlation of LP-latencies with centrifugal direction preference suggests that this specific property is generated by intracortical wiring rather than by thalamic input.     

Increased oxidative metabolism in middle suprasylvian cortex following removal of areas 17 and 18 from newborn cats

We measured changes in metabolic activity in middle suprasylvian (MS) cortex of cats subjected to early or late removal of areas 17 and 18 to localize shifts in activity possibly indicative of regions within MS cortex that may receive expanded inputs and be involved in the sparing of some visual behaviors following early primary visual cortex damage. Cytochrome oxidase (CO) activity was measured in MS cortex of mature, intact cats and of others with areas 17 and 18 removed in adulthood (P180), or on postnatal day 28 (P28) or postnatal day 1 (P1). Not less than 9 months after the ablation, brain sections were prepared and reacted for the presence of CO. The density of CO reactivity in each of the six cortical layers in MS cortex was measured and standardized against densities from ventral periaqueductal gray or hypothalamus on the same section. Following lesions on P1, significant increases in CO activity occurred in deep layer III and in layer IV of the medial bank of the MS sulcus, including all of area PMLS and the posterior portion of AMLS. In contrast, there were no significant differences in the level of CO activity among P28, P180, or intact cats for any of the cortical layers, and all had lower levels than the P1 cats. This metabolic change provides an anatomical marker for localizing adjustments in MS cortex and can be linked to amplified projections into MS cortex from the thalamus (LPm and A and C laminae of the dorsal lateral geniculate nucleus) and ventral posterior suprasylvian cortex following P1 ablations. Furthermore, this neurochemical analysis implicates a distinct region of MS cortex as the cortical locus of some spared visual functions following early primary visual cortex damage.     

Spatial and temporal properties of neurons of the lateral suprasylvian cortex of the cat

Neurons in the posteromedial lateral suprasylvian cortex (PMLS) of cats were recorded extracellularly to investigate their response to stimulation by bars and by sinusoidal gratings. Two general types of cells were identified: those that modulated in synchrony with the passage of drifting bars and gratings and those that responded with an unmodulated increase in discharge. Both types responded to contrast reversed gratings with a modulation of activity: the cells that modulated to drifting gratings modulated to the first harmonic of contrast reversed gratings (at appropriate spatial phase and frequency), whereas those that did not modulate to drifting gratings always modulated to the second harmonic of contrast reversed gratings. No cell had a clear null point. Nearly all cells were selective for spatial frequency. The preferred frequency ranged from 0.1 to 1 cycles per degree (cpd), and selectivity bandwidths (full width at half height) were around two octaves. Preferred spatial frequency was not correlated with receptive field size, but bandwidth and receptive field size were positively correlated. Preferred spatial frequency decreased with eccentricity, at about 0.05 octaves/deg. The response of all cells increased as a function of grating contrast up to a saturation level. The contrast threshold for response to a grating of optimal parameters was approximately 1% for most cells and the saturation contrast approximately 10%. The contrast gain was approximately 25 spikes/s per log unit of contrast. All cells were tuned for temporal frequency, preferring frequencies from approximately 3 to 10 Hz, with a selectivity bandwidth approximately 2 octaves. For some cells, the spatial selectivity did not depend on the temporal frequency and vice versa. Others were spatiotemporally coupled, with the preferred temporal frequency being lower at high than at low spatial frequencies, and the preferred spatial frequency lower at high than at low temporal frequencies. Previous results showing broad velocity tuning to a bar were replicated and found to be predictable from the combined spatial and temporal tuning of PMLS cells and the Fourier spectrum of a bar. Preferred temporal frequency steadily decreased with eccentricity, at 0.025 octaves/deg. The results for PMLS cells are compared with those of other visual areas. Acuity and spatial preference and selectivity bandwidth is comparable to all areas except area 17, where they are a factor of about two higher. Temporal selectivity in PMLS is as fine as observed in other areas. The possibility that PMLS cells may be involved with motion detection and detection of motion in depth is discussed.     

Phase- and position-disparity coding in the posteromedial lateral suprasylvian area of the cat

The posteromedial lateral suprasylvian area of the cat is known to be involved in the analysis of motion and motion in depth. However, it remains unclear whether binocular cells in the posteromedial lateral suprasylvian area rely upon phase or positional offsets between their receptive fields in order to code binocular disparity. The present study aims at clarifying more precisely the neural mechanisms underlying stereoperception with two objectives in mind. First, to determine whether cells in the posteromedial lateral suprasylvian area code phase disparities. Secondly, to examine whether the cells sensitive to phase disparity are the same as those which code for position disparities or whether each group represent a different sub-population of disparity-sensitive neurons. We investigated this by testing both types of disparities on single neurons in this area. The results show that the vast majority of cells (74%), in the posteromedial lateral suprasylvian area, are sensitive to relative interocular phase disparities. These cells showed mostly facilitation (95%) and a few (5%) summation interactions. Moreover, most cells (81%) were sensitive to both position and phase disparities.The results of this study show that most binocular cells in the posteromedial lateral suprasylvian area are sensitive to both positional and phase offsets which demonstrate the importance of this area in stereopsis.     

Transient projections from the fronto-parietal and temporal cortex to areas 17, 18 and 19 in the kitten

Summary Using the retrograde tracers, fast blue and horseradish peroxidase we have shown the presence of projections from extensive regions of the frontoparietal and temporal cortex to areas 17, 18 and 19 in the newborn kitten. These projections are transitory as they do not exist in the adult cat. The anterograde transport of horseradish peroxidase conjugated with wheat germ agglutinin after injections in frontoparietal and temporal cortex revealed that these transitory projections terminate in the gray matter and that they could therefore play a functional role in the development of the visual cortex.     

Collinearity tolerance of cells in areas 17 and 18 of the cat's visual cortex: Relative sensitivity to straight lines and chevrons

Summary Collinearity tolerance and length dependence of orientation tuning were compared in cells recorded from areas 17 and 18 of the lightly anaesthetised cat's visual cortex. Orientation tuning and interaction between receptive field halves of the same cells are reported in the preceding paper and elsewhere (Hammond and Andrews, 1978a, b).In confirmation of previous work, increase in stimulus length was associated with sharper orientation tuning in all simple and hypercomplex cells, and in most complex cells even in the absence of length summation.Cells in areas 17 and 18 were more sharply tuned for straight lines than for chevrons bent symmetrically about the optimal orientation; tuning for chevrons was noticeably skewed compared with tuning for straight lines. In area 17, the best response was always obtained with a straight line of optimal orientation.The two halves of the receptive fields of some cells in area 18 had dissimilar preferred orientations. Even in cells whose receptive field halves were similarly tuned, broadly tuned, or apparently untuned for orientation, simultaneous stimulation of both halves of the receptive field led to substantial sharpening of tuning. In cells with dissimilarly tuned half fields, the skew in chevron tuning was predictable from the orientation tuning of each half of the receptive field. Two area 18 cells responded consistently better to a chevron stimulus than to a straight line of any orientation.     

The retinotopic distribution of visual callosal projections in the suprasylvian visual areas compared to the classical visual areas (17, 18, 19) in the cat

Summary The distribution of the interhemispheric projection from area 17 and 18 was studied using the anterograde degeneration technique. Besides the classical visual areas (17, 18, 19), area 21 and several visual areas in the middle suprasylvian sulcus also received visual callosal input. In the four terminal areas of the middle suprasylvian sulcus the projection was found to be focused on representations of the vertical meridian including the area centralis, as in the classical visual areas. An increase of the width of visual field represented in the zone of callosal terminations can be seen from area 17 through area 18 to area 19 and possibly this trend continues in the suprasylvian visual areas.     

Transgeniculate signal transmission to middle suprasylvian cortex in intact cats and following early removal of areas 17 and 18: a morphological study

 Removal of cat areas 17 and 18 early, but not late, in postnatal development results in the sparing of certain reflexive and nonreflexive visually guided behaviors. These spared behaviors are accompanied by an expansion of geniculocortical projections to middle suprasylvian (MS) cortex. However, little is known about the types of visual signals relayed along these pathways. The purpose of our study was to reveal the morphologies of the neurons participating in the rewired circuits and, by relating them to the morphologies of functionally characterized neurons described by others, infer the types of visual signals transmitted via the lateral geniculate nucleus (LGN) to MS cortex. To do this, we retrogradely labeled LGN neurons from MS cortex with fluorescent microspheres, and subsequently intracellularly filled them with Lucifer Yellow. We then classified well-filled neurons according to a battery of morphological parameters (such as soma size and shape, and dendritic field-form and specializations), and compared them with already defined structure/function relationships. By doing this, we found that the large majority of visual thalamic relay neurons to MS cortex of both normal cats and cats that incurred removal of areas 17 and 18 were types I and IV. These results indicate that visual Y and W signals, respectively, are relayed directly from LGN to MS cortex in both types of cats. Following the early lesions, some of the MS-projecting type I neurons were found in layers A and A1, where they are never found in intact cats. Thus, some layer A and A1 type I neurons redirect axons to MS cortex following early removal of areas 17 and 18. For the type IV MS-projecting neurons in early lesioned cats, the somas were hypertrophied and they had more profuse and broader dendritic arbors than equivalent neurons in intact cats. These results suggest that dynamic interactions take place between inputs and outputs of LGN neurons during development that influence final LGN neuron morphology. Moreover, they suggest that signals transferred to MS cortex by type IV neurons may be modified by early lesions of areas 17 and 18. Overall, these results contribute to our understanding of the types of behaviors that may be spared by early lesions of areas 17 and 18. Received: 22 May 1996 / Accepted: 3 September 1996     

Patterns of cytochrome oxidase activity in areas 17, 18 and 19 of the visual cortex of cats and kittens

Summary The laminar pattern of cytochrome oxidase activity was studied in visual cortical areas 17,18 and 19 in adult cats and kittens, following electrophysiological determination of the boundaries of these areas in all but the youngest animals. The patterns of cytochrome oxidase staining and the cytoarchitectonic appearances of areas 17, 18 and 19 were compared. At all ages activity was especially high in the region of layers IV and VI in areas 17 and 18, and was low in all laminae in area 19. The results suggest that the degree of cytochrome oxidase activity in these regions of the visual cortex may be related to the strength and type of projection that they receive from the lateral geniculate nucleus. The cytochrome oxidase technique is a useful means of defining the 18/19 border, and may help locate the boundary between areas 17 and 18, in both adult cats and kittens.