Strobe Rearing Prevents the Convergence of Inputs With Different Response Timings Onto Area 17 Simple Cells

1998 ◽  
Vol 80 (6) ◽  
pp. 3005-3020 ◽  
Author(s):  
Allen L. Humphrey ◽  
Alan B. Saul ◽  
Jordan C. Feidler

Humphrey, Allen L., Alan B. Saul, and Jordan C. Feidler. Strobe rearing prevents the convergence of inputs with different response timings onto area 17 simple cells. J. Neurophysiol. 80: 3005–3020, 1998. The preceding paper showed that the loss of direction selectivity in simple cells induced by strobe rearing reflects the elimination of spatially ordered response timing differences across the receptive field that underlie spatiotemporal (S-T) inseparability. Here we addressed whether these changes reflected an elimination of certain timings or an alteration in how timings were associated in single cells. Timing in receptive fields was measured using stationary bars undergoing sinusoidal luminance modulation at different temporal frequencies (0.5–6 Hz). For each bar position, response phase versus temporal frequency data were fit by a line to obtain two measures: absolute phase and latency. In normal cats, many individual simple cells display a wide range of timings; in layer 4, the mean range for absolute phase and latency was 0.21 cycles and 39 ms, respectively. Strobe rearing compressed the mean timing ranges in single cells, to 0.08 cycles and 31 ms, respectively, and this compression accounted for the loss of inseparability. A similar compression was measured in layer 6 cells. In contrast, the range of timing values across the simple-cell population was relatively normal. Single cells merely sampled narrower than normal regions of the timing space. We sought to understand these cortical changes in terms of how inputs from the lateral geniculate nucleus (LGN) may have been affected by strobe rearing. In normal cats, a wide range of absolute phase and latency values exists among lagged and nonlagged LGN cells, and these thalamic timings account for most of the cortical timings. Also, S-T inseparability in many simple cells can be attributed to the convergence of lagged and/or nonlagged inputs. Strobe rearing did not change the sampling of lagged and nonlagged cells, and the geniculate timings continued to account for most of the cortical timings. However, strobe rearing virtually eliminated cortical receptive fields with mixed lagged and nonlagged timing, and it compressed the timing range in cells dominated by one or the other geniculate type. Thus strobe rearing did not eliminate certain timings in LGN or cortex, but prevented the convergence of different timings on single cells. To account for these results, we propose a developmental model in which strobe stimulation alters the correlational structure of inputs based on their response timing. Only inputs with similar timing become associated on single cortical cells, and this produces S-T separable receptive fields that lack the ability to confer a preferred direction of motion.

1993 ◽  
Vol 10 (1) ◽  
pp. 93-115 ◽  
Author(s):  
B. Dreher ◽  
A. Michalski ◽  
R. H. T. Ho ◽  
C. W. F. Lee ◽  
W. Burke

AbstractExtracellular recordings from single neurons have been made from presumed area 21a of the cerebral cortex of the cat, anesthetized with N2O/O2/sodium pentobarbitone mixture. Area 21a contains mainly a representation of a central horizontal strip of contralateral visual field about 5 deg above and below the horizontal meridian.Excitatory discharge fields of area 21a neurons were substantially (or slightly but significantly) larger than those of neurons at corresponding eccentricities in areas 17, 19, or 18, respectively. About 95% of area 21a neurons could be activated through either eye and the input from the ipsilateral eye was commonly dominant. Over 90% and less than 10% of neurons had, respectively, C-type and S-type receptive-field organization. Virtually all neurons were orientation-selective and the mean width at half-height of the orientation tuning curves at 52.9 deg was not significantly different from that of neurons in areas 17 and 18. About 30% of area 21a neurons had preferred orientations within 15 deg of the vertical.The mean direction-selectivity index (32.8%) of area 21a neurons was substantially lower than the indices for neurons in areas 17 or 18. Only a few neurons exhibited moderately strong end-zone inhibition. Area 21a neurons responded poorly to fast-moving stimuli and the mean preferred velocity at about 12.5 deg/s was not significantly different from that for area 17 neurons.Selective pressure block of Y fibers in contralateral optic nerve resulted in a small but significant reduction in the preferred velocities of neurons activated via the Y-blocked eye. By contrast, removal of the Y input did not produce significant changes in the spatial organization of receptive fields (S or C type), the size of the discharge fields, the width of orientation tuning curves, or direction-selectivity indices.Our results are consistent with the idea that area 21a receives its principal excitatory input from area 17 and is involved mainly in form rather than motion analysis.


1998 ◽  
Vol 80 (6) ◽  
pp. 2991-3004 ◽  
Author(s):  
Allen L. Humphrey ◽  
Alan B. Saul

Humphrey, Allen L. and Alan B. Saul. Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. J. Neurophysiol. 80: 2991–3004, 1998. Direction selectivity in simple cells of cat area 17 is linked to spatiotemporal (S-T) receptive-field structure. S-T inseparable receptive fields display gradients of response timing across the receptive field that confer a preferred direction of motion. Receptive fields that are not direction selective lack gradients; they are S-T separable, displaying uniform timing across the field. Here we further examine this link using a developmental paradigm that disrupts direction selectivity. Cats were reared from birth to 8 mo of age in 8-Hz stroboscopic illumination. Direction selectivity in simple cells was then measured using gratings drifting at different temporal frequencies (0.25–16 Hz). S-T structure was assessed using stationary bars presented at different receptive-field positions, with bar luminance being modulated sinusoidally at different temporal frequencies. For each cell, plots of response phase versus bar position were fit by lines to characterize S-T inseparability at each temporal frequency. Strobe rearing produced a profound loss of direction selectivity at all temporal frequencies; only 10% of cells were selective compared with 80% in normal cats. The few remaining directional cells were selective over a narrower than normal range of temporal frequencies and exhibited weaker than normal direction selectivity. Importantly, the directional loss was accompanied by a virtual elimination of S-T inseparability. Nearly all cells were S-T separable, like nondirectional cells in normal cats. The loss was clearest in layer 4. Normally, inseparability is greatest there, and it correlates well ( r = 0.77) with direction selectivity; strobe rearing reduced inseparability and direction selectivity to very low values. The few remaining directional cells were inseparable. In layer 6 of normal cats, most direction-selective cells are only weakly inseparable, and there is no consistent relationship between the two measures. However, after strobe rearing, even the weak inseparability was eliminated along with direction selectivity. The correlated changes in S-T structure and direction selectivity were confirmed using conventional linear predictions of directional tuning based on responses to counterphasing bars and white noise stimuli. The developmental changes were permanent, being observed up to 12 yr after strobe rearing. The deficits were remarkably specific; strobe rearing did not affect spatial receptive-field structure, orientation selectivity, spatial or temporal frequency tuning, or general responsiveness to visual stimuli. These results provide further support for a critical role of S-T structure in determining direction selectivity in simple cells. Strobe rearing eliminates directional tuning by altering the timing of responses within the receptive field.


1992 ◽  
Vol 68 (4) ◽  
pp. 1190-1208 ◽  
Author(s):  
A. B. Saul ◽  
A. L. Humphrey

1. The visual cortex receives several types of afferents from the lateral geniculate nucleus (LGN) of the thalamus. In the cat, previous work studied the ON/OFF and X/Y distinctions, investigating their convergence and segregation in cortex. Here we pursue the lagged/nonlagged dichotomy as it applies to simple cells in area 17. Lagged and nonlagged cells in the A-layers of the LGN can be distinguished by the timing of their responses to sinusoidally luminance-modulated stimuli. We therefore used similar stimuli in cortex to search for signs of lagged and nonlagged inputs to cortical cells. 2. Line-weighting functions were obtained from 37 simple cells. A bar was presented at a series of positions across the receptive field, with the luminance of the bar modulated sinusoidally at a series of temporal frequencies. First harmonic response amplitude and phase values for each position were plotted as a function of temporal frequency. Linear regression on the phase versus temporal frequency data provided estimates of latency (slope) and absolute phase (intercept) for each receptive-field position tested. These two parameters were previously shown to distinguish between lagged and nonlagged LGN cells. Lagged cells generally have latencies > 100 ms and absolute phase lags; nonlagged cells have latencies < 100 ms and absolute phase leads. With the use of these criteria, we classified responses at discrete positions inside cortical receptive fields as lagged-like and nonlagged-like. 3. Both lagged-like and nonlagged-like responses were observed. The majority of cortical cells had only or nearly only nonlagged-like zones. In 15 of the 37 cells, however, the receptive field consisted of > or = 20% lagged-like zones. For eight of these cells, lagged-like responses predominated. 4. The distribution of latency and absolute phase across the sample of cortical simple cell receptive fields resembled the distribution for LGN cells. The resemblance was especially striking when only cells in or adjacent to geniculate recipient layers were considered. Absolute phase lags were almost uniformly associated with long latencies. Absolute phase leads were generally associated with short latencies, although cortical cells responded with long latencies and absolute phase leads slightly more often than LGN cells. 5. Cells in which a high percentage of lagged-like responses were observed had a restricted laminar localization, with all but two being found in layer 4B or 5A. Cells with predominantly nonlagged-like responses were found in all layers. 6. Lagged-like zones can not be easily explained as a result of stimulating combinations of nonlagged inputs.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 81 (3) ◽  
pp. 1212-1224 ◽  
Author(s):  
Aditya Murthy ◽  
Allen L. Humphrey

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17. Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T–oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sinewave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified from fits to response temporal phase versus stimulus spatial phase data. Bicuculline reduced direction selectivity and S-T orientation in nearly all cells, and reductions in the two measures were well correlated ( r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well for absolute changes in the amplitude and phase of responses to gratings drifting in the preferred and nonpreferred direction. For each cell we also calculated an exponent used to estimate the static nonlinearity. Bicuculline reduced the exponent in most cells, but the changes were not correlated with reductions in direction selectivity. We conclude that GABAA-mediated inhibition influences directional tuning in layer 4 primarily by sculpting S-T receptive-field structure. The source of the inhibition is likely to be other simple cells with certain spatiotemporal relationships to their target. Despite reductions in the two measures, most receptive fields maintained some directional tuning and S-T orientation during BMI. This suggests that their excitatory inputs, arising from the lateral geniculate nucleus and within area 17, are sufficient to create some S-T orientation and that inhibition accentuates it. Finally, BMI also reduced direction selectivity in 8 of 10 simple cells tested in layer 6, but the reductions were not accompanied by systematic changes in S-T structure. This reflects the fact that S-T orientation, as revealed by our first-order measures of the receptive field, is weak there normally. Inhibition likely affects layer 6 cells via more complex, nonlinear interactions.


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.


1991 ◽  
Vol 66 (2) ◽  
pp. 505-529 ◽  
Author(s):  
R. C. Reid ◽  
R. E. Soodak ◽  
R. M. Shapley

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (3) ◽  
pp. 512-533 ◽  
Author(s):  
J. R. Wilson ◽  
S. M. Sherman

1. Receptive-field properties of 214 neurons from cat striate cortex were studied with particular emphasis on: a) classification, b) field size, c) orientation selectivity, d) direction selectivity, e) speed selectivity, and f) ocular dominance. We studied receptive fields located throughtout the visual field, including the monocular segment, to determine how receptivefield properties changed with eccentricity in the visual field.2. We classified 98 cells as "simple," 80 as "complex," 21 as "hypercomplex," and 15 in other categories. The proportion of complex cells relative to simple cells increased monotonically with receptive-field eccenticity.3. Direction selectivity and preferred orientation did not measurably change with eccentricity. Through most of the binocular segment, this was also true for ocular dominance; however, at the edge of the binocular segment, there were more fields dominated by the contralateral eye.4. Cells had larger receptive fields, less orientation selectivity, and higher preferred speeds with increasing eccentricity. However, these changes were considerably more pronounced for complex than for simple cells.5. These data suggest that simple and complex cells analyze different aspects of a visual stimulus, and we provide a hypothesis which suggests that simple cells analyze input typically from one (or a few) geniculate neurons, while complex cells receive input from a larger region of geniculate neurons. On average, this region is invariant with eccentricity and, due to a changing magnification factor, complex fields increase in size with eccentricity much more than do simple cells. For complex cells, computations of this geniculate region transformed to cortical space provide a cortical extent equal to the spread of pyramidal cell basal dendrites.


1999 ◽  
Vol 16 (3) ◽  
pp. 513-525 ◽  
Author(s):  
ALLEN L. HUMPHREY ◽  
ADITYA MURTHY

Previous evidence concerning the physiological cell classes in the medial interlaminar nucleus (MIN) has been conflicting. We reexamined the MIN using standard functional tests to distinguish X-, Y- and W-cells. Discharge patterns to flashing spots also were used to identify some cells as lagged or nonlagged, as previously done for the geniculate A-layers. Also, each cell's response timing (latency and absolute phase) was measured from discharges to a spot undergoing sinusoidal luminance modulation. Of 71 MIN cells, 48% were Y, 27% were W, 8% were X, and 17% were unclassifiable. Lagged and nonlagged discharge profiles were observed in each cell group, with 28% of all cells being lagged. Lagged cells displayed a response suppression and long latency to discharge following spot onset, and a slow decay in firing at spot offset that was often preceded by a transient discharge. These profiles were indistinguishable from those of lagged cells in the A-layers. MIN cells also were heterogeneous in response timing, displaying a range of latency and absolute phase values similar to that in the A-layers. We extended these analyses to 27 cells in the geniculate C-layers. In layer C, 35% of cells were Y, 10% were X, 25% were W, and 30% were unclassifiable. About 11% had lagged profiles, and were X-cells or unclassifiable cells. Layers C1 and C2 contained only W-cells and no lagged profiles. The range of timings in the C-layers was somewhat narrower than in the MIN. Overall, these results show that the MIN contains a greater variety of functional cell classes than heretofore appreciated. Further, it appears that mechanisms which create different timing delays in the A-layers also exist in the MIN and layer C. These timings may contribute to direction selectivity in extrastriate cortex.


Perception ◽  
1996 ◽  
Vol 25 (1_suppl) ◽  
pp. 157-157 ◽  
Author(s):  
A Thiele ◽  
K-P Hoffmann

Direction-selective neurons from the middle temporal area (MT) and the middle superior temporal area (MST) were recorded while a monkey performed a direction discrimination task. Stimuli consisted of evenly spaced bars moving in one of the four cardinal directions. Monkey's reaction time, single-cell latency, and direction selectivity were calculated when stimuli of 53%, 24%, and 4% contrast were presented, and the monkey indicated a correct decision. Mean reaction time was 359±77 ms at 53% contrast, 391±107 ms at 24% contrast, and 582±374 ms at 4% contrast. Most neurons exhibiting direction selective responses at 53% contrast was also active at 24% contrast (MT, 99%; MST, 88%). The number of neurons still exhibiting stimulus-related activity at 4% contrast dramatically decreased (MT to 28%; MST to 41%). Shortest latencies were found at high contrast level (53% contrast; MT, 29 ms; population mean, 76±40 ms; MST, 35 ms; population mean, 77±27 ms). Single cell and population latency increased at lower contrast (4% contrast: MT minimum, 86 ms; population mean, 180±76 ms; MST minimum, 97 ms; population mean, 205±56 ms). This indicates that the mean increase in latency at the single-cell level only partially reflects the increase in reaction time (mean reaction time increased by 223 ms, while mean single-cell latency increased by ∼100 ms in MT and MST). We therefore calculated the normalised population response at different contrast levels. The maximal population activity was always found at the highest contrast level and this was set to 1. In MT it took 75 – 80 ms from stimulus onset until half maximal activity (0.5) was reached at 53% contrast. To reach 0.5 took 85 – 90 ms at 24% contrast and 205 – 210 ms at 4% contrast. For MST the respective values were 85 ms (53% contrast), 90 ms (24% contrast) and 255 ms (4%) contrast. Thus the time to reach half the maximal population activity much better reflects the reaction time than the mean of the latencies calculated from single cells.


2010 ◽  
Vol 103 (2) ◽  
pp. 677-697 ◽  
Author(s):  
Lionel G. Nowak ◽  
Maria V. Sanchez-Vives ◽  
David A. McCormick

The aim of the present study was to characterize the spatial and temporal features of synaptic and discharge receptive fields (RFs), and to quantify their relationships, in cat area 17. For this purpose, neurons were recorded intracellularly while high-frequency flashing bars were used to generate RFs maps for synaptic and spiking responses. Comparison of the maps shows that some features of the discharge RFs depended strongly on those of the synaptic RFs, whereas others were less dependent. Spiking RF duration depended poorly and spiking RF amplitude depended moderately on those of the underlying synaptic RFs. At the other extreme, the optimal spatial frequency and phase of the discharge RFs in simple cells were almost entirely inherited from those of the synaptic RFs. Subfield width, in both simple and complex cells, was less for spiking responses compared with synaptic responses, but synaptic to discharge width ratio was relatively variable from cell to cell. When considering the whole RF of simple cells, additional variability in width ratio resulted from the presence of additional synaptic subfields that remained subthreshold. Due to these additional, subthreshold subfields, spatial frequency tuning predicted from synaptic RFs appears sharper than that predicted from spiking RFs. Excitatory subfield overlap in spiking RFs was well predicted by subfield overlap at the synaptic level. When examined in different regions of the RF, latencies appeared to be quite variable, but this variability showed negligible dependence on distance from the RF center. Nevertheless, spiking response latency faithfully reflected synaptic response latency.


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