Functional changes across the 17–18 border in the cat

Summary Changes in velocity sensitivity, receptive field (RF) position, and RF size were investigated in long oblique penetrations crossing the 17–18 border. The penetrations were histologically reconstructed and the border determined by cytoarchitectonics. In cortex subserving central and paracentral vision change in velocity sensitivity allowed a reasonable physiological identification of the 17–18 border. The physiological border correlates well with the histological border zone, best with its medial edge. Changes in RF position and RF size are of little use for physiological identification of the border in this region. In this cortical region area 18 representation of the vertical meridian (VM) has a high magnification factor. In cortex subserving peripheral vision, the change in velocity sensitivity was small and the change in RF position coincided with the cytoarchitectonics.Research Fellow of the National Research Council of Belgium     

Functional organization of the cortical 17/18 border region in the cat

The representation of the visual field in the 17/18 border region of the cat's visual cortex, and the layout of orientation and ocular dominance columns, were studied by making many closely spaced electrode penetrations into the superficial layers of the flattened dorsal region of the marginal gyrus and recording response properties at each location. The 17/18 border region was defined by measuring the change in the horizontal component of receptive field position within the gyrus: as the position of the recording electrode moved from medial to lateral, the receptive fields moved towards the vertical midline, indicating that the electrode was in area 17; as penetrations were made in increasingly lateral positions, the trend reversed, and receptive field positions moved away from the midline, indicating that the electrode was in area 18. The receptive fields of cells close to the border straddled, or lay within 2 degrees-3 degrees on either side of the vertical midline. In addition, patches of cortex were sometimes encountered in which cells had receptive field centers located up to 7 degrees in the ipsilateral visual field. Experiments in which maps were made in the left and right hemispheres of a single animal showed that these patches had a complementary distribution in the two hemispheres. Cells within the patches behaved as though driven by Y-cell inputs: they usually had large receptive fields and responded to rapidly-moving stimuli. They were broadly tuned for orientation and strongly dominated by the contralateral eye. Fourier spectral analysis of orientation selectivity maps showed that iso-orientation bands had an average spacing of 1.14 +/- 0.1 mm and tended to be elongated in a direction orthogonal to the 17/18 border. Individual bands crossed the border without obvious interruption, although singularities (points of discontinuity in the layout of orientations) were more frequently observed in the border region than in adjacent areas. Two dominant periodicities could be measured in the maps of ocular dominance, one at around 0.8 +/- 0.2 mm and a second at 2.0 +/- 0.3 mm. No constant direction of elongation was noted. These are close to the periods present within areas 17 and 18 respectively.     

Topographic relations between ocular dominance and orientation columns in the cat striate cortex

Summary In the visual cortex of four adult cats ocular dominance and orientation columns were visualized with (³H)proline and (¹⁴C)deoxyglucose autoradiography. The two columnar systems were reconstructed from serial horizontal sections or from flat-mount preparations and graphically superimposed. They share a number of characteristic features: In both systems the columns have a tendency to form regularly spaced parallel bands whose main trajectory is perpendicular to the border between areas 17 and 18. These bands frequently bifurcate or terminate in blind endings. The resulting irregularities are much more pronounced in the ocular dominance than in the orientation system. The periodicity of the columnar patterns was assessed along trajectories perpendicular to the main orientation of the bands and differed in the two columnar systems. The spacing of the ocular dominance stripes was significantly narrower than the spacing of orientation bands. The mean periodicity of a particular columnar system was virtually identical in the two hemispheres of the same animal but it differed substantially in different animals. However, the spacing of orientation columns covaried with that of the ocular dominance columns, the ratios of the mean spacings of the two columnar systems being similar in the four cats. The superposition of the two columnar systems revealed no obvious topographic relation between any of the organizational details such as the location of bifurcations, blind endings and intersections. We suggest the following conclusions: 1. The developmental processes generating the two columnar systems seem to obey the same algorithms but they act independently of each other. 2. The space constants of the two systems are rigorously specified and appear to depend on a common variable. 3. The main orientation of the bands in both columnar systems is related to a) the representation of the vertical meridian, b) the anisotropy of the cortical magnification factor, and c) the tangential spread of intracortical connections.     

Topographic organization of orientation columns in the cat visual cortex

Summary Three-dimensional reconstructions of the orientation column system were obtained from the visual cortex of four cats using the deoxyglucose technique. One cat had normal visual experience, one was monocularly deprived and two had selective experience with vertical and horizontal contours, respectively. In areas 17 and 18 orientation columns form a remarkably regular system of equally spaced parallel bands whose trajectory is orthogonal to the borderline between areas 17 and 18. This topographic organization is resistant to manipulations of early visual experience.     

The pattern of ocular dominance columns in flat-mounts of the cat visual cortex

Summary Ocular dominance (OD) columns in the cat visual cortex were visualized with autoradiography after intravitreal injection of (³H)proline. Extending previous studies, a flat-mount technique was applied that enabled the analysis of the distribution of label throughout extensive regions of the visual cortex without requiring reconstructions from serial sections. OD-columns were confined to layer IV and consisted of isolated patches and short bands. The latter were parallel to each other and regularly spaced, the main trajectory being orthogonal to the 17/18 border. This pattern of the geniculo-cortical terminals was similar in the hemispheres ipsi- and contralateral to the injected eye. The mean periodicities of the OD-bands were virtually identical in the two hemispheres of the same animal: 850 m and 830 m in cat D1 and 770 m and 800 m in cat D2. However, the ipsilateral OD-columns appeared smaller, more heavily labeled and more sharply delineated than the contralateral columns.     

Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18

Summary Orientation sensitivity was tested, using moving bars as stimuli, in 136 LGN cells in normal cats and 82 LGN cells in cats with areas 17 and 18 lesioned.The responses of most neurones showed some dependence on the orientation of the line stimulus. The orientation bias was more pronounced for long, narrow bars moving at rather slow velocities. Length-response curves revealed less end-inhibition along the optimum orientation than along the nonoptimum orientation. Thirty-two percent of the cells in the normal cats and 50% in the lesioned animals responded best to orientations within 10 ° of the vertical or horizontal. The oblique orientations were represented poorly in the lesioned group. Thus the corticogeniculate feedback may serve to confer a more uniform distribution of orientation preferences on the LGN.It is suggested that the orientation biases of LGN neurones may play a role in building orientation-selective cells in the visual cortex. Further, the preferences for horizontal and vertical orientations in the LGN may explain the preferences for these orientations reported for visual cortical cells.     

14C-Deoxyglucose mapping of orientation subunits in the cats visual cortical areas

Summary The orientation domain in the cortical visual areas of anesthetized cats has been investigated by employing the ¹⁴C-Deoxyglucose technique (Sokoloff et al., 1977).Orientation subunits (OS) are seen in the first (V1), the second (V2) and the third visual area (V3) as well as in the visual areas of the suprasylvian sulcus. In the latter regions OS are less elaborated than in V1, V2, and V3. The OS are continuous through all cortical layers; in V1 however, only weak label is detected in layer 4C. In V1, V2, and V3 the width of the OS is about 0.4 mm and the average distance between two OS centers is 0.9 mm. The spatial pattern of the OS seems to be more regular in the visual field periphery than in regions representing the vertical meridian.     

Orientational influences of layer V of visual area 18 upon cells in layer V of area 17 in the cat cortex

We examined the orientation tuning curves of 86 cells located in layer V of area 17, before, during, and after focal blockade of a small (300-m diameter) region of near-retinotopic register in layer V of area 18 of quantitatively established orientation preference. Such focal blockade revealed three distinct populations of area 17 layer V cells-cells with decreased responses to stimuli of some orientations (21%), cells with increased responses to stimuli of some orientations (43%), and cells unaffected by the focal blockade (36%). These effects were clearcut, reproducible, and generally directly related to the known receptive field properties of the cell recorded in area 18 at the center of the zone of blockade. These effects were also analyzed in terms of alterations in orientation bandwidth in the cells in area 17 as a result of the blockade-bandwidth increases (22%) and decreases (24%) were found; however, these changes were essentially unrelated to the measured receptive field properties. Inhibitory and excitatory effects were most pronounced when the regions in areas 17 and 18 were of like ocular dominance and were of similar orientation preference. Inhibitory effects (suggesting a normally excitatory input) were most dependent upon the similarity of receptive fields; excitatory effects (suggesting a normally inhibitory input) were less heavily dependent.     

Stimulus dependence of ocular dominance of complex cells in area 17 of the feline visual cortex

Summary Stimulus dependence of ocular dominance of 31 deep-layer complex cells was assessed from detailed monocular directional tuning curves for motion of bar stimuli or fields of static visual noise, in area 17 of normal adult cats, lightly anaesthetised with N₂O/O₂ supplemented with pentobarbitone. Virtually all cells were binocularly driven, with the anticipated ocular dominance distribution. Interocular differences in directional bias and sharpness of directional tuning for noise were observed in eleven cells, whereas preferred direction and sharpness of tuning for bar stimuli were similar for each eye. In the majority of cells (20/31), any differences between noise and bar tuning in one eye were replicated in the other. Ocular dominance of about half the cells (17/31) for noise and for bar motion was similar, or marginally shifted by up to one ocular dominance group. Substantial shifts in ocular dominance were seen in 14 cells — by up to two ocular dominance groups in 12 cells and by up to three ocular dominance groups in two cells. In three cases these shifts involved a reversal of eye dominance. Notwithstanding these changes, there were no obvious trends in shifts of ocular dominance in favour of the ipsilateral or contralateral eye, nor was there any tendency towards increased binocularity for noise.     

Directionality of cat striate cortical neurones: contribution of suppression

Summary Direction-selective or direction-biased striate cortical neurones were assessed for absence or incidence of suppression of firing, maximal at 90° or 180° (null suppression) to the optimal direction, in 327 neurones recorded from the striate cortex of cats anaesthetized with N₂O/O₂/halothane. Stimuli were light or dark bars moving over uniform or stationary textured back-grounds; or square-wave gratings of optimal spatial frequency and velocity. Five identified directionality groups were correlated with neuronal class and a range of other receptive field properties. Suppression maximal at 90° to optimum was common amongst direction-biased neurones, rare amongst direction-selective neurones. In the latter group, null suppression (maximal at 180° to optimum) was more prevalent than at 90°. Standard complex cells constituted the majority of complex neurones. They were more commonly direction-biased and less commonly showed suppression than special complex cells. The latter comprised the majority of direction-selective neurones with 180° suppression. Endstopping was seen more frequently in special complex cells, but for each functional class was similarly distributed between the different directionality groups. Based on the mean and mode of partially overlapping distributions, for all neuronal classes direction-selective neurones were more broadly tuned than direction-biased neurones. Special complex neurones were appreciably more broadly tuned than standard complex neurones; those with suppression at 180° were the most broadly tuned neurones in the cortex. Direction-biased neurones with suppression at 90° to optimum were more sharply tuned than those lacking such suppression. Direction-selective neurones had larger receptive fields than direction-biased neurones. In both groups receptive fields decreased in size in the sequence: intermediate complex > standard complex > special complex > simple. Resting discharge was highest amongst direction-selective neurones with 180° suppression, lower in those with 90° suppression or those lacking it, and lowest amongst direction-biased neurones. With the possible exception of the minority of neurones that were silent, low levels of resting discharge have not seriously prejudiced either neuronal categorization or comparisons of tuning selectivity. The pattern which emerges is that suppression maximal in directions orthogonal to the preferred direction/orientation is more commonly associated with sharp tuning and directionbias, whereas null suppression, in the direction opposite that preferred, is associated with broad tuning, direction-selectivity, high resting discharge levels and strong texture sensitivity.     

Rarity of luxotonic responses in cortical visual areas of the cat

Summary Neuronal responses to continuous, diffuse white light or darkness were studied in cortical visual areas 17, 18, 19 and Clare-Bishop of the unanesthetized cat. In contrast to squirrel monkeys and macaques in which about 40 or 25% of the units in striate cortex are luxotonic (response to continuous light or darkness sustained>2.0 min), all of the visual areas in the cat had fewer than 4.0% of the units exhibiting such luxotonic activity. The functional basis of this difference may be related to differences between the two species in the quantitative balance of antagonistic receptive field properties.This report is dedicated to the guidance and friendship of John R. Bartlett, deceased November 5, 1978 R. Bartlett, deceased November 5, 1978     

Non-stationarity of ocular dominance in cat striate cortex

Summary Interocular relationships, based on monocular directional tuning curves derived simultaneously for bar and for texture motion interleaved, are described for complex cells in the lightly-anaesthetised feline striate cortex. The results confirm earlier reports of stimulus-dependent differences in ocular dominance (Hammond 1979a, b) and demonstrate that ocular-dominance may be time-dependent and influenced by secondary stimulus characteristics including velocity of motion. Temporal and apparently spontaneous shifts in ocular dominance may take place other than in parallel for different classes of stimuli and may even occur simultaneously but in opposite directions. Thus absolute shifts in eye preference, as well as relative shifts between differing stimuli, must both occur with time, perhaps as the result of non-visual influences. The results present a challenge to strategies classically employed in defining cortical ocular dominance.     

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).     

A quantitative study of the classification and stability of ocular dominance in the cat's visual cortex

Summary We recorded from single cells in the cat's visual cortex to quantitatively evaluate (1) the reliability of subjective assessments of ocular dominance (101 cells) and (2) the stability of ocular dominance over time (25 cells). We found that the correlation between subjective and objective measures of this variable was poorer than expected, and was worst for cells with low overall response strengths. This result appears to reflect variability in the subjective assessment procedure. For the second part of the study, we recorded from single cortical cells of 5-week-old kittens, and made repeated objective measurements of ocular dominance over time. Twenty-four of the twenty-five cells examined were quite stable in ocular dominance for periods so long as 8 h. One unit was encountered which showed substantial progressive shifts in ocular dominance over time.Supported by grant EY01175 and Research Career Development Award EY00029 from the US National Eye Institute to R.D. Freeman     

A high probability of an orientation shift between layers 4 and 5 in central parts of the cat striate cortex

Summary On the postlateral gyrus of the cat striate cortex the cells' preferred orientation was measured as a function of cortical depth in penetrations as parallel as possible to the radial fibre bundles. According to the penetration angle and in agreement with the current model of orientation columns, there was a low orientation drift in layers 2–4. At the transition between layers 4 and 5 an orientation shift of 45–90 deg was found in most penetrations. The orientation differences between adjacent recording sites in lower layers was normally low too, but clearly higher than in upper layers. The results are discussed in terms of more independent orientation mechanisms in upper and lower layers.Supported by grant Ba 636/2-1 and Ho 450/14 from the Deutsche Forschungsgemeinschaft to R. Bauer and K. P. Hoffmann     

GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex

Summary We investigated the contributions of lateral intracortical connections to the orientation tuning of area 17 cells using micro-iontophoresis of the inhibitory transmitter gamma-aminobutyric acid (GABA) to inactivate small cortical sites in the vicinity of a recorded cell. GABA was ejected from an array of micropipettes each with an average horizontal distance of 500 m from the recording site. Of 54 cells tested, 33 showed a reduction and 3 a loss of orientation selectivity due to an increase in responses to non-optimal orientations during GABA inactivation. The response to the optimal orientation remained constant in more than half of the cells and increased or decreased in others. Given that a complete cycle of orientations occupies a tangential distance of 1000 m, the observed broadening of orientation tuning is presumably due to GABA-mediated inactivation of inhibitory interneurones with different preferred orientations from those of their target cell.     

Retinotopic organization of extra-retinal saccade-related input to the visual cortex in the cat

Summary Single unit activity of 842 cells has been recorded in cat visual cortex and analyzed with respect to vestibular induced, and spontaneous saccadic eye movements performed in the dark. This study has been done in awake, chronically implanted cats, subsequently placed in acute conditions to achieve the precise retinotopic mapping of the cortical areas previously investigated.In areas 17 and 18, respectively, 27% and 24% of the cells tested were influenced by horizontal saccadic eye movements in the dark (E. M. cells). In the Clare-Bishop area, the proportion of E. M. cells was 12%, while only 2% of such cells were found in areas 19 and 21.The distribution of E.M. cells in areas 17 and 18 with respect to retinotopy showed that E.M. cells were more numerous in the cortical zones devoted to the representation of the area centralis (38% in area 17, 27% in area 18) than in the zones subserving the periphery of the visual field (17% and 12%, respectively).Two of the characteristics of E. M. cell activations appear dependant on the retinotopic organization. First, a larger number of E.M. cells presenting an asymmetry in their responses to horizontal saccadic eye movements in opposite directions (directional E.M. cells) were encountered in the cortical representation of the peripheral visual field. 53% of E. M. cells recorded in area 17 and 71% in area 18 were directional in the cortex corresponding to the peripheral visual field. This percentage was of 23% and 25% respectively in the cortex devoted to area centralis. Second, E.M. cells were found to have a latency from the onset of the saccade systematically larger than 100 ms (i.e, they discharged at, or after the end of the eye movement) if they were located in the cortical representation of the area centralis, while E.M. cells related to the peripheral visual field displayed a wider range of latencies (0–240 ms).Results obtained in Clare Bishop area, although limited to the representation of the peripheral visual field, were quantitatively and qualitatively similar to those observed in the homologous retinotopic zones of areas 17 and 18.It is concluded that an extra-retinal input related to oculomotor activity is sent to the cat visual cortex and is organized, at least in areas 17 and 18, with respect to the retinotopic representation of the visual field. These data support the hypothesis of a functional duality between central and peripheral vision and are discussed in the context of visual-oculomotor integration.Supported by INSERM (C.R.L. 79-53336)     

Ocular dominance in striate cortex is altered by neonatal section of the posterior corpus callosum in the cat

Summary In adult cats that had previously undergone surgical section of the posterior corpus callosum at 13–18 days after birth, the striate cortex was examined using extracellular single unit recordings. The receptive fields of the cells examined were located from the vertical meridian to 39 ° peripherally, and ranged from above to below the horizontal meridian. Cells were classified according to type (simple, complex), ocular dominance, receptive field size and location. Callosum sectioned cats had 53% of striate cells activated monocularly as compared to 25% for control cats. This increase in monocularly activated units primarily occurred for receptive fields in the paracentral region of the visual field, from 4–39 °. The age at which the neonatal surgery had occurred was correlated with the individual cat's proportion of monocularly activated cells.Therefore, the increase in monocular activation of striate units occurred within a large portion of the normal binocular visual field. This physiological change was partially predicted by a previous behavioral study showing a substantial loss in the extent of the binocular visual field following neonatal corpus callosum section (Elberger 1979).Support for this research was received from Training Grant No. T-32 EY 07035-02 awarded to the University of Pennsylvania. Additional support was provided by the Department of Neurobiology and Anatomy, University of Texas Medical School at Houston, No. 1-11321-215001-10     

The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat

The responses of neurons in area 17 were tested as a function of various stimulus parameters. The thresholds of individual cortical neurons were at contrasts between 0.01 and 0.1 (increment of 0.5×10⁻¹ cd/m⁻² on a background of 3 cd/m⁻²), the dynamic ranges were 1.0–2.0 log units of increment, and all cells showed a response decrease at increments above a certain maximum (supersaturation response). The averaged contrast/response curve for all neurons was S-shaped in the logarithmic plot, had a dynamic range of 2.5 log units, reached its maximum at a contrast of 0.75 and supersaturated above this level. The contrast/ sensitivity curves changed their slope under different stimulus conditions. They became flatter when the non-dominant eye was stimuated as compared to dominant eye stimulation or when the stimulation was done at a non-optimal orientation or direction, and they became steeper when both eyes were stimulated. But the maximum was reached at the same contrast and supersaturation was seen above maximum contrast no matter whether a cell was stronlgy (e.g. binocular stimulation at optimal orientation) or weakly excited (non-dominant or non-optimal orientation stimulation). After normalization, the averaged population contrast/response curves were virtually identical at all stimulus conditions. It was concluded, that range as well as maximum and supersaturation of cortical contrast/response curves are determined before the input reaches the cortex, and that the cortical cells summate, essentially, linearly. The findings furthermore demonstrate that the supersaturation of the cortical input must be due to subtractive inhibition, and that the same is true for the orientation sensitive inhibition in the cortex itself. Both, the peripheral contrast and the cortical orientation dependant inhibition cannot be explained by multiplicative inhibition. The fact, that the responses of neurons depend on many variables relativates their significance for feature representation.     

Inactivation of the infragranular striate cortex broadens orientation tuning of supragranular visual neurons in the cat

Intracortical inhibition is believed to enhance the orientation tuning of striate cortical neurons, but the origin of this inhibition is unclear. To examine the possible influence of ascending inhibitory projections from the infragranular layers of striate cortex on the orientation selectivity of neurons in the supragranular layers, we measured the spatiotemporal response properties of 32 supragranular neurons in the cat before, during, and after neural activity in the infragranular layers beneath the recorded cells was inactivated by iontophoretic administration of GABA. During GABA iontophoresis, the orientation tuning bandwidth of 15 (46.9%) supragranular neurons broadened as a result of increases in response amplitude to stimuli oriented about ±20° away from the preferred stimulus angle. The mean (±SD) baseline orientation tuning bandwidth (half width at half height) of these neurons was 13.08±2.3°. Their mean tuning bandwidth during inactivation of the infragranular layers increased to 19.59±2.54°, an increase of 49.7%. The mean percentage increase in orientation tuning bandwidth of the individual neurons was 47.4%. Four neurons exhibited symmetrical changes in their orientation tuning functions, while 11 neurons displayed asymmetrical changes. The change in form of the orientation tuning functions appeared to depend on the relative vertical alignment of the recorded neuron and the infragranular region of inactivation. Neurons located in close vertical register with the inactivated infragranular tissue exhibited symmetric changes in their orientation tuning functions. The neurons exhibiting asymmetric changes in their orientation tuning functions were located just outside the vertical register. Eight of these 11 neurons also demonstrated a mean shift of 6.67±5.77° in their preferred stimulus orientation. The magnitude of change in the orientation tuning functions increased as the delivery of GABA was prolonged. Responses returned to normal approximately 30 min after the delivery of GABA was discontinued. We conclude that inhibitory projections from neurons within the infragranular layers of striate cortex in cats can enhance the orientation selectivity of supragranular striate cortical neurons.