Effects of selective pressure block of Y-type optic nerve fibers on the receptive-field properties of neurons in the striate cortex of the cat

1992 ◽  
Vol 9 (1) ◽  
pp. 47-64 ◽  
Author(s):  
W. Burke ◽  
B. Dreher ◽  
A. Michalski ◽  
B. G. Cleland ◽  
M. H. Rowe

AbstractIn an aseptic operation under surgical anesthesia, one optic nerve of a cat was exposed and subjected to pressure by means of a special cuff. The conduction of impulses through the pressurized region was monitored by means of electrodes which remained in the animal after the operation. The pressure was adjusted to selectively eliminate conduction in the largest fibers (Y-type) but not in the medium-size fibers (X-type). The conduction block is probably due to a demyelination and remains complete for about 3 weeks. Within 2 weeks after the pressure-block operation, recordings were made from single neurons in the striate cortex (area 17, area VI) of the cat anesthetized with N2O/O2 mixture supplemented by continuous intravenous infusion of barbiturate. Neurons were activated visually via the normal eye and via the eye with the pressure-blocked optic nerve (“Y-blocked eye”). Several properties of the receptive fields of single neurons in area 17 such as S (simple) or C (complex) type of receptive-field organization, size of discharge fields, orientation tuning, direction-selectivity indices, and end-zone inhibition appear to be unaffected by removal of the Y-type input. On the other hand, the peak discharge rates to stimuli presented via the Y-blocked eye were significantly lower than those to stimuli presented via the normal eye. As a result, the eye-dominance histogram was shifted markedly towards the normal eye implying that there is a significant excitatory Y-type input to area 17. In a substantial proportion of area 17 neurons, this input converges onto the cells which receive also non-Y-type inputs. In one respect, velocity sensitivity, removal of the Y input had a weak but significant effect. In particular, C (but not S) cells when activated via the normal eye responded optimally at slightly higher stimulus velocities than when activated via the Y-blocked eye. These results suggest that the Y input makes a distinct contribution to velocity sensitivity in area 17 but only in C-type neurons. Overall, our results lead us to the conclusion that the Y-type input to the striate cortex of the cat makes a significant contribution to the strength of the excitatory response of many neurons in this area. However, the contributions of Y-type input to the mechanism(s) underlying many of the receptive-field properties of neurons in this area are not distinguishable from those of the non-Y-type visual inputs.

1992 ◽  
Vol 9 (1) ◽  
pp. 65-78 ◽  
Author(s):  
B. Dreher ◽  
A. Michalski ◽  
B. G. Cleland ◽  
W. Burke

AbstractRecordings were made from single neurons in area 18 of anesthetized cats (N2O/O2 mixture supplemented by continuous intravenous infusion of barbiturate) in which one optic nerve had been pressure blocked to selectively block conduction in the largest (Y-type) fibers. Cortical neurons were stimulated visually via the normal eye or via the eye with the pressure-blocked optic nerve (“Y-blocked eye”). Several properties of the receptive fields such as their spatial organization (S or C cells), orientation tuning, and the presence and strength of end-zone inhibition appear to be unaffected by removal of the Y input. By contrast, the removal of the Y input resulted in a small but significant reduction in the size of the discharge field and in the direction-selectivity index. In three respects, peak response discharge rate, eye dominance, and velocity sensitivity, removal of the Y input had strong and highly significant effects. Thus, the mean peak discharge frequency of responses evoked by the stimulation of binocular neurons via the Y-blocked eye was significantly lower than that of responses evoked by the stimulation via the normal eye. Accordingly, the eye-dominance histogram was shifted markedly towards the normal eye (more so than in the homologous experiment conducted on area 17 — Burke et al., 1992). Finally, the mean preferred velocity of responses of cells activated via the normal eye was in the vicinity of 145 deg/s, whereas for cells activated via the Y-blocked eye the value was about 35 deg/s. Overall, the results of the present study imply that (1) apart from Y-type excitatory input there are significant excitatory non-Y-inputs to area 18; these inputs at least partially consist of indirect X-type input relayed via area 17; (2) in neurons of area 18 that receive both Y-type and non-Y-type excitatory inputs, the Y-type input has a major influence on strength of the response and velocity sensitivity and a lesser influence on the direction selectivity and size of the discharge fields; and (3) area 18 contains mechanisms determining such receptive-field properties as S- or C-type organization, orientation tuning, and direction selectivity which can be accessed either by the Y input or by non-Y input.


1986 ◽  
Vol 56 (4) ◽  
pp. 1062-1073 ◽  
Author(s):  
J. G. Malpeli ◽  
C. Lee ◽  
H. D. Schwark ◽  
T. G. Weyand

Reversible inactivation of individual layers of the cat lateral geniculate and medial interlaminar nuclei was used to investigate the necessary and sufficient inputs for maintaining visually driven activity and receptive field properties in area 17. Neither orientation selectivity nor direction selectivity depends on any individual geniculate layer. We identified two groups of cortical layers on the basis of the pattern of thalamic inputs providing visual driving through the contralateral eye. One group, consisting of layers 4 and 6, has geniculate layer A as its only necessary and sufficient input. The other, consisting of supragranular layers, integrates at least two sufficient thalamic inputs, one of which is layer A. Several major receptive field properties are independently generated in these two groups of layers.


1997 ◽  
Vol 14 (1) ◽  
pp. 141-158 ◽  
Author(s):  
John M. Crook ◽  
Zoltan F. Kisvárday ◽  
Ulf T. Eysel

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


1992 ◽  
Vol 9 (6) ◽  
pp. 581-593 ◽  
Author(s):  
C. Casanova ◽  
Y. Michaud ◽  
C. Morin ◽  
P.A. McKinley ◽  
S. Molotchnikoff

AbstractWe have investigated the effects of inactivation of localized sites in area 17 on the visual responses of cells in visuotopically corresponding regions of area 18. Experiments were performed on adult normal cats. The striate cortex was inactivated by the injection of nanoliters of lidocaine hydrochloride or of γ-aminobutyric acid (GABA) dissolved in a staining solution. Responses of the simple and complex cells of area 18 to optimally oriented light and dark bars moving in the two directions of motion were recorded before, during, and after the drug injection. Two main effects are described.First, for a substantial number of cells, the drug injection provoked an overall reduction of the cell's visual responses. This nonspecific effect largely predominated in the complex cell family (76% of the units affected). This effect is consistent with the presence of long-range excitatory connections in the visual cortex.Second, the inactivation of area 17 could affect specific receptive-field properties of cells in area 18. The main specific effect was a loss of direction selectivity of a number of cells in area 18, mainly in the simple family (more than 53% of the units affected). The change in direction selectivity comes either from a disinhibitory effect in the nonpreferred direction or from a reduction of response in the preferred direction. It is proposed that the disinhibitory effects were mediated by inhibitory interneurones within area 18. In a very few cases, the change of directional preference was associated with a modification of the cell's response profile.These results showed that the signals from area 17 are necessary to drive a number of units in area 18, and that area 17 can contribute to, or at least modulate, the receptive-field properties of a large number of cells in the parastriate area.


1976 ◽  
Vol 39 (6) ◽  
pp. 1352-1361 ◽  
Author(s):  
B. L. Finlay ◽  
P. H. Schiller ◽  
S. F. Volman

1. The receptive-field properties of corticotectal cells in the monkey's striate cortex were studied using stationary and moving stimuli. These cells were identified by antidromic activation from the superior colliculus. 2. Corticotectal cells form a relatively homogeneous group. They are found primarily in layers 5 and 6. These cells can usually be classified as CX-type cells but show broader orientation tuning, larger receptive fields, higher spontaneous activity, and greater binocular activation than CX-type cells do in general. A third of the corticotectal cells were direction selective. 3. These results suggest that the cortical input to the superior colliculus is not directly responsible for the receptive-field properties of collicular cells. We propose that this input has a gating function in contributing to the control of the downflow of excitation from the superficial to the deep layers of the colliculus.


1991 ◽  
Vol 6 (1) ◽  
pp. 25-41 ◽  
Author(s):  
C. Distler ◽  
K.-P. Hoffmann

AbstractEvidence is presented that innate microstrabismus and abnormal cortical visual receptive-field properties can occur also in cats without any apparent involvement of the Siamese or albino genetic abnormalities in their visual system. A possible cause for microstrabismus in these cats may be sought in an abnormally large horizontal distance between blind spot and area centralis indicated by a temporal displacement of the most central receptive fields on both retinae.Depth perception was found to be impaired in cats with innate microstrabismus. Behavioral measurements using a Y-maze revealed in four such cats that the performance in recognizing the nearer of two random-dot patterns did not improve when they were allowed to use both eyes instead of only one. The ability of microstrabismic cats to perceive depth under binocular viewing conditions only corresponded to the monocular performance of five normal cats.Electrophysiological recordings were performed in the visual cortex (areas 17 and 18) of four awake cats, two normal, and two innate microstrabismic animals. Ocular dominance and orientation tuning of single neurons in area 17 and 18 were analyzed quantitatively.The percentage of neurons in area 17 and 18 which could be activated through either eye was significantly reduced to 49.7% in the microstrabismic animals when compared to the normal cats (74.8%). “True binocular cells,” which can only be activated by simultaneous stimulation of both eyes, were significantly less frequent (1.6%) in microstrabismic cats than in normal animals (10.4%). However, subthreshold binocular interactions were identical in both groups of animals. In the strabismic animals, long-term binocular stimulation of monocular neurons did not give a clear indication of alternating use of one or the other eye.The range of stimulus orientations leading to discharge rates above 50% of the maximal response, i.e. the half-width of the orientation tuning curves, was the same in the two groups of cats. However, orientation sensitivity, i.e. the alternation in discharge rate per degree change in stimulus orientation, was higher in cortical cells of normal cats than in those of microstrabismic cats.In normal and microstrabismic cats, no clear sign of an “oblique effect,” i.e. the preference of cortical neurons for vertical and horizontal orientations compared to oblique orientations, could be found neither in the incidence of cells with horizontal or vertical preferred orientation nor in the sharpness of orientation tuning and sensitivity of these neurons.In summary, the receptive-field properties reported here for awake innate microstrabismic cats are similar to those reported in the literature for anesthetized cats with varying degrees of albinism and for cats with artificial symmetrical strabismus surgically induced by sectioning the equivalent extraocular muscles in both eyes. Our innate microstrabismic cats may provide, however, an animal model for investigating the etiology of one form of naturally occurring strabismus.


1986 ◽  
Vol 56 (4) ◽  
pp. 1088-1101 ◽  
Author(s):  
T. G. Weyand ◽  
J. G. Malpeli ◽  
C. Lee ◽  
H. D. Schwark

The receptive field properties of antidromically identified corticotectal (CT) cells in area 17 were explored in the paralyzed, anesthetized cat. To compare these with another population of infragranular cells, we also examined the receptive field properties of cells in layer 6. Sixty percent of our sample of CT cells showed increased response to increased stimulus length (length summation) and were classified as standard complex cells. The other 40% showed little or no length summation, were generally end stopped, and were classified as special complex cells. Standard and special complex CT cells have complementary orientation anisotropies: the distribution of orientation preferences of standard complex cells is biased toward obliquely oriented stimuli, whereas special complex cells are biased toward horizontally and vertically oriented stimuli. The receptive fields of the cells in our sample were primarily along the horizontal meridian so we cannot determine if these anisotropies are defined relative to the vertical meridian or relative to the meridian passing through the receptive field. The effects of these anisotropies in preferred orientation are minimized by the broad orientation tuning of CT cells. There was no simple relationship between the direction bias of CT cells and the reported direction bias of tectal cells. In contrast to the heterogeneity of corticotectal cells, layer 6 cells uniformly showed strong length summation, tight orientation tuning, and little spontaneous activity.


Of the many possible functions of the macaque monkey primary visual cortex (striate cortex, area 17) two are now fairly well understood. First, the incoming information from the lateral geniculate bodies is rearranged so that most cells in the striate cortex respond to specifically oriented line segments, and, second, information originating from the two eyes converges upon single cells. The rearrangement and convergence do not take place immediately, however: in layer IVc, where the bulk of the afferents terminate, virtually all cells have fields with circular symmetry and are strictly monocular, driven from the left eye or from the right, but not both; at subsequent stages, in layers above and below IVc, most cells show orientation specificity, and about half are binocular. In a binocular cell the receptive fields in the two eyes are on corresponding regions in the two retinas and are identical in structure, but one eye is usually more effective than the other in influencing the cell; all shades of ocular dominance are seen. These two functions are strongly reflected in the architecture of the cortex, in that cells with common physiological properties are grouped together in vertically organized systems of columns. In an ocular dominance column all cells respond preferentially to the same eye. By four independent anatomical methods it has been shown that these columns have the form of vertically disposed alternating left-eye and right-eye slabs, which in horizontal section form alternating stripes about 400 μm thick, with occasional bifurcations and blind endings. Cells of like orientation specificity are known from physiological recordings to be similarly grouped in much narrower vertical sheeet-like aggregations, stacked in orderly sequences so that on traversing the cortex tangentially one normally encounters a succession of small shifts in orientation, clockwise or counterclockwise; a 1 mm traverse is usually accompanied by one or several full rotations through 180°, broken at times by reversals in direction of rotation and occasionally by large abrupt shifts. A full complement of columns, of either type, left-plus-right eye or a complete 180° sequence, is termed a hypercolumn. Columns (and hence hypercolumns) have roughly the same width throughout the binocular part of the cortex. The two independent systems of hypercolumns are engrafted upon the well known topographic representation of the visual field. The receptive fields mapped in a vertical penetration through cortex show a scatter in position roughly equal to the average size of the fields themselves, and the area thus covered, the aggregate receptive field, increases with distance from the fovea. A parallel increase is seen in reciprocal magnification (the number of degrees of visual field corresponding to 1 mm of cortex). Over most or all of the striate cortex a movement of 1-2 mm, traversing several hypercolumns, is accompanied by a movement through the visual field about equal in size to the local aggregate receptive field. Thus any 1-2 mm block of cortex contains roughly the machinery needed to subserve an aggregate receptive field. In the cortex the fall-off in detail with which the visual field is analysed, as one moves out from the foveal area, is accompanied not by a reduction in thickness of layers, as is found in the retina, but by a reduction in the area of cortex (and hence the number of columnar units) devoted to a given amount of visual field: unlike the retina, the striate cortex is virtually uniform morphologically but varies in magnification. In most respects the above description fits the newborn monkey just as well as the adult, suggesting that area 17 is largely genetically programmed. The ocular dominance columns, however, are not fully developed at birth, since the geniculate terminals belonging to one eye occupy layer IVc throughout its length, segregating out into separate columns only after about the first 6 weeks, whether or not the animal has visual experience. If one eye is sutured closed during this early period the columns belonging to that eye become shrunken and their companions correspondingly expanded. This would seem to be at least in part the result of interference with normal maturation, though sprouting and retraction of axon terminals are not excluded.


1976 ◽  
Vol 39 (3) ◽  
pp. 613-630 ◽  
Author(s):  
W. Singer ◽  
F. Tretter

An attempt was made to relate the alterations of cortical receptive fields as they result from binocular visual deprivation to changes in afferent, intrinsic, and efferent connections of the striate and parastriate cortex. The experiments were performed in cats aged at least 1 jr with their eyelids sutured closed from birth.The results of the receptive-field analysis in A17 confirmed the reduction of light-responsive cells, the occasional incongruity of receptive-field properties in the two eyes, and to some extent also the loss of orientation and direction selectivity as reported previously. Other properties common to numerous deprived receptive fields were the lack of sharp inhibitory sidebands and the sometimes exceedingly large size of the receptive fields. Qualitatively as well as quantitatively, similar alterations were observed in area 18. A rather high percentage of cells in both areas had, however, preserved at least some orientation preference, and a few receptive fields had tuning properties comparable to those in normal cats. The ability of area 18 cells in normal cats to respond to much higher stimulus velocities than area 17 cells was not influenced by deprivation.The results obtained with electrical stimulation suggest two main deprivation effects: 1) A marked decrease in the safety factor of retinothalamic and thalamocortical transmission. 2) A clear decrease in efficiency of intracortical inhibition. But the electrical stimulation data also show that none of the basic principles of afferent, intrinsic, and efferent connectivity is lost or changed by deprivation. The conduction velocities in the subcortical afferents and the differentiation of the afferents to areas 17 and 18 into slow- and fast-conducting projection systems remain unaltered. Intrinsic excitatory connections remain functional; this is also true for the disynaptic inhibitory pathways activated preferentially by the fast-conducting thalamocortical projection. The laminar distribution of cells with monosynaptic versus polsynaptic excitatory connections is similar to that in normal cats. Neurons with corticofugal axons remain functionally connected and show the same connectivity pattern as those in normal cats. The nonspecific activation system from the mesencephalic reticular formation also remains functioning both at the thalamic and the cortical level.We conclude from these and several other observations that most, if not all, afferent, intrinsic, and efferent connections of areas 17 and 18 are specified from birth and depend only little on visual experience. This predetermined structural plan, however, allows for some freedom in the domain of orientation tuning, binocular correspondence, and retinotopy which is specified only when visual experience is possible.


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