Synapse clustering can drive simultaneous ON-OFF and ocular-dominance segregation in a model of area 17

Author(s):  
Martin Stetted ◽  
Elmar W. Lang ◽  
Klaus Obermayerl
Keyword(s):  
2002 ◽  
Vol 19 (1) ◽  
pp. 39-49 ◽  
Author(s):  
RALF ENGELMANN ◽  
JOHN M. CROOK ◽  
SIEGRID LÖWEL

Strabismus (or squint) is both a well-established model for developmental plasticity of the brain and a frequent clinical symptom. While the layout and topographic relationship of functional domains in area 17 of divergently squinting cats has been analyzed extensively in recent years (e.g. Löwel et al., 1998), functional maps in convergently squinting animals have so far not been visualized with comparable detail. We have therefore investigated the functional organization of area 17 in adult cats with a surgically induced convergent squint angle. In these animals, visual acuity was determined by both behavioral tests and recordings of visual evoked potentials, and animals with comparable acuities in both eyes were selected for further experiments. The functional layout of area 17 was visualized using optical imaging of intrinsic signals. Monocular iso-orientation domains had a patchy appearance and their layout was different for left and right eye stimulation, so that segregated ocular dominance domains could be visualized. Iso-orientation domains exhibited a pinwheel-like organization, as previously described for normal and divergently squinting cats. Mean pinwheel density was the same in the experimental and control animals (3.4 pinwheel centers per mm2 cortical surface), but significantly (P < 0.00001) higher than that reported previously for normal and divergently squinting cats (2.7/mm2). A comparison of orientation with ocular dominance maps revealed that iso-orientation domains were continuous across the borders of ocular dominance domains and tended to intersect these borders at steep angles. However, in contrast to previous reports in normally raised cats, orientation pinwheel centers showed no consistent topographical relationship to the peaks of ocular dominance domains. Taken together, these observations indicate an overall similarity between the functional layout of orientation and ocular dominance maps in area 17 of convergently and divergently squinting cats. The higher pinwheel densities compared with previous reports suggest that animals from different gene pools might generally differ in this parameter and therefore also in the space constants of their cortical orientation maps.


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.


1998 ◽  
Vol 10 (8) ◽  
pp. 2629-2643 ◽  
Author(s):  
Siegrid Löwel ◽  
Kerstin E. Schmidt ◽  
Dae-Shik Kim ◽  
Fred Wolf ◽  
Frank Hoffsümmer ◽  
...  
Keyword(s):  

1991 ◽  
Vol 7 (3) ◽  
pp. 259-281 ◽  
Author(s):  
Simon Grant ◽  
Nancy E. J. Berman

AbstractWe have examined the effects of rearing kittens with a unilateral convergent strabismus, induced surgically at 3 weeks of age, on the binocularity (ocular dominance) and receptive-field position of neurons in the motion-sensitive lateral suprasylvian (LS) area of cat extrastriate cortex. Data were compared to those obtained from area 17 in the same animals, and from the two areas of cortex in normal adult cats. Interocular alignment of the operated cats was assessed in alert adults using corneal reflex photography and during recording from the positions of retinal landmarks under paralysis. The strabismus magnitude in each operated cat was calculated by comparison with equivalent data from the normal animals.Strabismus always caused a major loss of binocularity in area 17. The remaining binocular neurons had receptive-field (RF) pairs arising from positions of normal correspondence in the two retinae and would thus have been responsive to different regions of visual space through the misaligned eyes in the alert animal. In area LS, the effects were dependent on the strabismus magnitude. In the group of four cats with pronounced strabismus (18–30 deg crossed), a loss of binocularity occurred in area LS equivalent in severity to that in area 17. The majority of the remaining binocular LS neurons possessed RF pairs in normal retinal correspondence and would thus, in the alert animal, have received spatially disparate visual input through the two eyes. This also occurred in three other cats with more moderate strabismus (11–15 deg crossed), although only a small breakdown in the binocularity of area LS was apparent. The group of cats with mild strabismus (≤10 deg crossed) had normal proportions of binocular neurons in area LS. In three of these cats, the maintenance of binocularity was accompanied by shifts in RF position, with visual inputs arising from anomalous retinal locations. These shifts compensated, in part, for the strabismus angle present in each cat, so that most of the binocular LS neurons would have received inputs from regions of visual correspondence through the misaligned eyes when the animal was alert.Similar mechanisms could afford a basis for the binocular visual compensations that occur in humans with small-angle strabismus of early onset. If so, anomalous retinal correspondence in such individuals would have as a locus areas of extrastriate cortex with a role in motion perception, and would involve alterations to the neural substrate underlying normal binocular vision.


1987 ◽  
Vol 58 (4) ◽  
pp. 795-815 ◽  
Author(s):  
Y. Trotter ◽  
Y. Fregnac ◽  
P. Buisseret

1. The electrophysiological effects of section of extraocular muscle proprioceptive afferents have been investigated in kitten area 17. Extraocular proprioceptive afferents were interrupted by cutting the ophthalmic branch of the fifth trigeminal nerve (V1 nerve) unilaterally in 15 normally reared kittens (NR) between 3 and 12 wk postnatal, in 3 NR adult cats, and in 7 dark-reared (DR) kittens at 6 wk postnatal. Bilateral sections of the V1 nerve were performed in two kittens at 6 wk postnatal. NR kittens were maintained in a normal environment after the section. DR kittens were returned to the darkroom until the recording session. Receptive-field properties of area 17 neurons were studied after a postsurgical delay of 4-7 wk in most NR kittens and of 4 days to 5 wk in DR kittens. In one NR kitten and in the operated adult cats, the delay was 1-2.5 yr. This study is based on a total sample of 1,190 visual cortical units. 2. When performed in NR kittens between 4 and 8 wk of age, the unilateral section of extraocular proprioceptive afferents significantly reduced the proportion of binocular cells: 1 mo after the section of the V1 nerve, half of the visual cortical cells were monocularly activated. A similar reduction in the proportion of binocular cells was also observed in DR kittens operated at 6 wk of age and then maintained in the dark for 5-7 wk. In contrast to the unilateral section, the bilateral section of the V1 nerve performed in 6-wk-old NR kittens did not disrupt cortical binocularity. 3. In 10 of the 22 kittens that had undergone unilateral sections, there was a strong asymmetry in the ocular dominance distribution in favor of one eye. This asymmetry was not related to the side of the section and was the same in both hemispheres for a given kitten. 4. The postsurgical delay played an important role in the appearance of the cortical deficit: binocularity loss was not found within the week following the section but was present 1 mo after the section. This functional impairment appeared to be permanent, since it was still observed 2.5 yr after the section. 5. Cortical cells were classified in two ways on the basis of their receptive-field organization: 1) into S- or C-types (38, 73), and 2) into small area slow (SAS), large area slow (LAS), or Fast (F)-types (42, 57).(ABSTRACT TRUNCATED AT 400 WORDS)


1989 ◽  
Vol 3 (3) ◽  
pp. 249-265 ◽  
Author(s):  
Helen Sherk

AbstractThe existence of multiple areas of extrastriate visual cortex raises the question of how the response properties of each area are derived from its visual input. This question was investigated for one such area in the cat, referred to here as the Clare-Bishop area (Hubel & Wiesel, 1969); it is the region of lateral suprasylvian cortex that receives input from area 17. A novel approach was used, in which kainic acid was injected locally into the Clare-Bishop area, making it possible to record directly from afferent inputs.The response properties of the great majority of a sample of 424 presumed afferents resembled cells in areas 17 and 18. Thus, a systematic comparison was made with cells from area 17's upper layers, the source of its projection to the Clare-Bishop area (Gilbert & Kelly, 1975), to see whether these afferents had distinctive properties that might distinguish them from cells projecting to areas 18 or 19. Some differences did emerge: (1) The smallest receptive fields typical of area 17 were relatively scarce among afferents. (2) Direction-selective afferents were more abundant than were such cells in area 17. (3) End-stopped afferents were extremely rare, although end-stopped cells were common in area 17's upper layers.Despite these differences, afferents were far more similar in their properties to cells in areas 17 and 18 than to cells in the Clare-Bishop area. Compared to the latter, afferents showed major discrepancies in receptive-field size, in direction selectivity, in end-stopping, and in ocular dominance distribution. These differences seem most likely to stem from circuitry intrinsic to the Clare-Bishop area.


1988 ◽  
Vol 59 (5) ◽  
pp. 1410-1429 ◽  
Author(s):  
K. R. Zahs ◽  
M. P. Stryker

1. ON-center and OFF-center cells are found in separate sublaminae of the ferret's lateral geniculate nucleus (LGN). The purpose of these experiments was to determine whether this segregation is maintained in the projection from the LGN to primary visual cortex (area 17). 2. The distribution of the geniculocortical afferents within area 17 was studied by recording in layer IV after cortical neurons were silenced with kainic acid. 3. In 28 radial penetrations made into layer IV of five kainate-treated ferrets, the center types of 289 single units with response characteristics identical to those of geniculate cells were noted. A Monte Carlo analysis of these data demonstrated that the geniculocortical afferents cluster according to center type. 4. There was no tendency for ON and OFF afferents to occupy separate sublayers within layer IV. 5. The organization of the afferents in the plane of layer IV was studied by making closely spaced electrode penetrations across the dorsal exposed surface of the cortex in three kainate-treated ferrets. A Monte Carlo analysis of these results demonstrated that afferents segregate on the basis of center type, as well as on the basis of ocular dominance, into patches in the plane of layer IV. 6. The surface-mapping results and the results of experiments in which electrode penetrations were made tangential to layer IV indicated that center-type patches can extend over several hundred micrometers. A Monte Carlo analysis of the sizes of the ocular dominance patches and center-type patches provided further support for this conclusion.


1990 ◽  
Vol 5 (1) ◽  
pp. 83-98 ◽  
Author(s):  
M.E. McCourt ◽  
J. Thalluri ◽  
G.H. Henry

AbstractIn a series of physiological experiments, a total of 203 neurons at the Area 17/18 border were recorded with a callosal link either demonstrated by antidromic or transsynaptic activation from stimulating electrodes located in the homotopic contralateral hemisphere (CH), or in the splenial segment of the corpus callosum (CC). Forty-four percent of the transcallosal cells could also be driven from stimulating electrodes in or just above the lateral geniculate nucleus (OR1). The majority (69%) of transcallosal neurons were classifiable as belonging to the complex family (B and C cells) and most of these were found in the supragranular laminae and in lamina 4A. The ocular dominance distribution of transcallosal cells was trimodal, consisting of roughly equal numbers of monocularly dominated and binocularly balanced neurons. Estimates of conduction time and synaptic delay were obtained for neurons driven from CH, CC, and from OR1, and in most instances the response latency was short enough to suggest a monosynaptic input from either the ipsi- or contra-lateral hemisphere. The distribution of transcallosal conduction times showed that S cells, as a class, had significantly faster conduction than cells of the complex family but otherwise there was no obvious signs of multimodality in the distribution curve. An analysis of the synaptic delays in transcallosal activation produced a mean of 0.6 to 0.7 ms but some were too short to be consistent with a transsynaptic drive, suggesting that some cells with an antidromic drive may have been included in the transsynaptic category. Results are interpreted in terms of the contribution made by the corpus callosum to stereoscopic vision.


1997 ◽  
Vol 14 (5) ◽  
pp. 929-938 ◽  
Author(s):  
Suzannah Bliss Tieman ◽  
Nina Tumosa

AbstractGoodhill (1993) has recently suggested that the spacing of ocularity domains in visual cortex is not solely an intrinsic property of cortex, but is determined, at least in part, by the degree of correlation in the activity of the two eyes. In support of this model, Löwel (1994) has shown that strabismus, which decorrelates the activity of the two eyes, increases the spacing of ocular dominance columns in area 17, but not area 18, of the cat. As a further test of Goodhill's model, in this paper we examine the effects of another rearing procedure that decorrelates the activity of the two eyes, namely alternating monocular exposure (AME). Cats were reared either normally (9 cats) or with AME (21 cats). We labeled their ocularity domains by one of three methods: ocular dominance columns by 2-deoxyglucose (14 cats), and ocular dominance patches by transneuronal transport (14 cats), or by injections of tracer into single layers of the lateral geniculate nucleus (LGN; 2 cats). The spacing of ocular dominance was 11% greater in the AME cats than in the normal cats (0.976 vs. 0.877 mm). These results are similar to those previously reported for strabismic cats, although the effect is less striking. We thus confirm that decorrelating the activity of the two eyes increases the spacing of cortical ocularity domains. Our results further suggest that the degree of decorrelation affects the extent of that increase.


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