Inhibitory Contributions to Spatiotemporal Receptive-Field Structure and Direction Selectivity in Simple Cells of Cat Area 17

1999 ◽  
Vol 81 (3) ◽  
pp. 1212-1224 ◽  
Author(s):  
Aditya Murthy ◽  
Allen L. Humphrey
Keyword(s):  
Receptive Field ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Field Structure ◽  
Area 17 ◽  
Directional Tuning ◽  
Simple Cells ◽  
Layer 4 ◽  
Two Measures ◽  
Spatiotemporal Receptive Field

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.

scholarly journals Strobe Rearing Reduces Direction Selectivity in Area 17 by Altering Spatiotemporal Receptive-Field Structure

1998 ◽  
Vol 80 (6) ◽  
pp. 2991-3004 ◽  
Author(s):  
Allen L. Humphrey ◽  
Alan B. Saul
Keyword(s):  
Receptive Field ◽  
Frequency Tuning ◽  
Temporal Frequency ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Field Structure ◽  
Area 17 ◽  
Directional Tuning ◽  
Simple Cells ◽  
Spatiotemporal Receptive Field

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.

scholarly journals Receptive Fields and Response Properties of Neurons in Layer 4 of Ferret Visual Cortex

2003 ◽  
Vol 89 (2) ◽  
pp. 1003-1015 ◽  
Author(s):  
W. Martin Usrey ◽  
Michael P. Sceniak ◽  
Barbara Chapman
Keyword(s):  
Visual Cortex ◽  
Receptive Field ◽  
Receptive Fields ◽  
Field Structure ◽  
Orientation Selectivity ◽  
Stimulus Orientation ◽  
Orientation Tuning ◽  
Simple Cells ◽  
Response Properties ◽  
Layer 4

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated,on and off subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 ± 1.2° (mean ± SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.

Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity

1976 ◽  
Vol 39 (3) ◽  
pp. 512-533 ◽  
Author(s):  
J. R. Wilson ◽  
S. M. Sherman
Keyword(s):  
Visual Field ◽  
Receptive Field ◽  
Striate Cortex ◽  
Ocular Dominance ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Orientation Selectivity ◽  
Simple Cells ◽  
Complex Cells ◽  
Cat Striate Cortex

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.

Spatio-temporal receptive-field structure of phasic W cells in the cat retina

1995 ◽  
Vol 12 (1) ◽  
pp. 117-139 ◽  
Author(s):  
M.H. Rowe ◽  
L.A. Palmer
Keyword(s):  
Receptive Field ◽  
Input Signal ◽  
Receptive Fields ◽  
Correlation Method ◽  
Direction Selectivity ◽  
Field Structure ◽  
Local Motion ◽  
Accessory Optic System ◽  
Spatio Temporal ◽  
Local Receptive Fields

AbstractThe spatio-temporal receptive-field structure of 54 phasic W cells in cat retinas has been examined using the reverse-correlation method of Jones and Palmer (1987). Within this sample, 12 cells had on-center, 16 off-center, and 26 on-off receptive fields. Three of the on-center and seven of the on-off cells were directionally selective. Forty percent of the cells in this sample had local receptive fields consisting of two or more distinct subregions. However, no correlation was observed between the number of subregions in the local receptive field and other response properties such as center sign or direction selectivity. In all cases, individual subregions, including those in on-off cells, appear to be produced by a half-wave rectification of the input signal. For 76% of the cells, these local receptive fields were contained within large suppressive fields which could be seen to extend for at least 10 deg in all directions with no apparent spatial structure. The mechanism producing the suppressive field also appears to involve a rectification of the input signal, and has a relatively high spatial resolution. Furthermore, the suppressive field itself is only responsive to moving or flickering stimuli; large, stationary gratings have no effect on the output of the local receptive-field mechanism. Thus, the overall receptive-field organization of these cells is particularly well suited for detecting local motion. The remaining 24% of cells in the sample lacked suppressive fields, and consequently responded well to large moving stimuli, but these cells were otherwise similar in their receptive-field properties to cells with suppressive fields. The significance of these properties is discussed in the context of the projections of phasic W cells to the superior colliculus and accessory optic system.

Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. I. General characteristics and postnatal development

1993 ◽  
Vol 69 (4) ◽  
pp. 1091-1117 ◽  
Author(s):  
G. C. DeAngelis ◽  
I. Ohzawa ◽  
R. D. Freeman
Keyword(s):  
Receptive Field ◽  
Postnatal Development ◽  
Striate Cortex ◽  
Receptive Fields ◽  
Space Time ◽  
Field Structure ◽  
Temporal Response ◽  
Spatial Frequencies ◽  
Spatiotemporal Receptive Field ◽  
Time Courses

1. Most studies of cortical neurons have focused on the spatial structure of receptive fields. For a more complete functional description of these neurons, it is necessary to consider receptive-field structure in the joint domain of space and time. We have studied the spatiotemporal receptive-field structure of 233 simple cells recorded from the striate cortex of adult cats and kittens at 4 and 8 wk postnatal. The dual goal of this study is to provide a detailed quantitative description of spatiotemporal receptive-field structure and to compare the developmental time courses of spatial and temporal response properties. 2. Spatiotemporal receptive-field profiles have been measured with the use of a reverse correlation method, in which we compute the cross-correlation between a neuron's response and a random sequence of small, briefly presented bright and dark stimuli. The receptive-field profiles of some simple cells are space-time separable, meaning that spatial and temporal response characteristics can be dissociated. Other cells have receptive-field profiles that are space-time inseparable. In these cases, a particular spatial location cannot be designated, unambiguously, as belonging to either an on or off subregion. However, separate on and off subregions may be clearly distinguished in the joint space-time domain. These subregions are generally tilted along an oblique axis. 3. Our observations show that spatial and temporal aspects of receptive-field structure mature with clearly different time courses. By 4 wk postnatal, the spatial symmetry and periodicity of simple-cell receptive fields have reached maturity. The spatial extent (or size) of these receptive fields is adult-like by 8 wk postnatal. In contrast, the response latency and time duration of spatiotemporal receptive fields do not mature until well beyond 8 wk postnatal. 4. By applying Fourier analysis to spatiotemporal receptive-field profiles, we have examined the postnatal development of spatial and temporal selectivity in the frequency domain. By 8 wk postnatal, spatial frequency tuning has clearly reached maturity. On the contrary, temporal frequency selectivity remains markedly immature at 8 wk. We have also examined the joint distribution of optimal spatial and temporal frequencies. From 4 wk postnatal until 8 wk postnatal, the range of optimal spatial frequencies increases substantially, whereas the range of optimal temporal frequencies remains largely unchanged. From 8 wk postnatal until adulthood, there is a large increase in optimal temporal frequencies for cells tuned to low spatial frequencies. For cells tuned to high spatial frequencies, the distribution of optimal temporal frequencies does not change much beyond 8 wk postnatal.(ABSTRACT TRUNCATED AT 400 WORDS)

Laminar differences in the spatiotemporal structure of simple cell receptive fields in cat area 17

1998 ◽  
Vol 15 (2) ◽  
pp. 239-256 ◽  
Author(s):  
A. MURTHY ◽  
A.L. HUMPHREY ◽  
A.B. SAUL ◽  
J.C. FEIDLER
Keyword(s):  
Receptive Fields ◽  
Extracellular Recording ◽  
Direction Selectivity ◽  
Simple Cell ◽  
Directional Tuning ◽  
Temporal Phase ◽  
Great Heterogeneity ◽  
Layer 4 ◽  
Actual Amplitude ◽  
Second Procedure

Previous studies of cat visual cortex have shown that the spatiotemporal (S-T) structure of simple cell receptive fields correlates with direction selectivity. However, great heterogeneity exists in the relationship and this has implications for models. Here we report a laminar basis for some of the heterogeneity. S-T structure and direction selectivity were measured in 101 cells using stationary counterphasing and drifting gratings, respectively. Two procedures were used to assess S-T structure and its relation to direction selectivity. In the first, the S-T orientations of receptive fields were quantified by fitting response temporal phase versus stimulus spatial phase data. In the second procedure, conventional linear predictions of direction selectivity were computed from the amplitudes and phases of responses to stationary gratings. Extracellular recording locations were reconstructed histologically. Among direction-selective cells, S-T orientation was greatest in layer 4B and it correlated well (r = 0.76) with direction selectivity. In layer 6, S-T orientation was uniformly low, overlapping little with layer 4B, and it was not correlated with directional tuning. Layer 4A was intermediate in S-T orientation and its relation (r = 0.46) to direction selectivity. The same laminar patterns were observed using conventional linear predictions. The patterns do not reflect laminar differences in direction selectivity since the layers were equivalent in directional tuning. We also evaluated a model of linear spatiotemporal summation followed by a static nonlinear amplification (exponent model) to account for direction selectivity. The values of the exponents were estimated from differences between linearly predicted and actual amplitude modulations to counterphasing gratings. Comparing these exponents with another exponent—that required to obtain perfect matches between linearly predicted and measured directional tuning—indicates that an exponent model largely accounts for direction selectivity in most cells in layer 4, particularly layer 4B, but not in layer 6. Dynamic nonlinearities seem essential for cells in layer 6. We suggest that these laminar differences may partly reflect the differential involvement of geniculocortical and intracortical mechanisms.

Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat

1992 ◽  
Vol 68 (4) ◽  
pp. 1190-1208 ◽  
Author(s):  
A. B. Saul ◽  
A. L. Humphrey
Keyword(s):  
Receptive Field ◽  
Lateral Geniculate Nucleus ◽  
Temporal Frequency ◽  
Receptive Fields ◽  
Area 17 ◽  
Cortical Cells ◽  
Simple Cells ◽  
Absolute Phase ◽  
Phase Lags ◽  
Lagged Cells

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)

Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex

1990 ◽  
Vol 63 (6) ◽  
pp. 1529-1543 ◽  
Author(s):  
M. S. Gizzi ◽  
E. Katz ◽  
R. A. Schumer ◽  
J. A. Movshon
Keyword(s):  
Direction Selectivity ◽  
Directional Selectivity ◽  
Area 17 ◽  
Directional Tuning ◽  
Simple Cells ◽  
Tuning Curves ◽  
Complex Cells ◽  
Preferred Direction ◽  
Sinusoidal Gratings ◽  
Direction Of Movement

1. We consider the consequences of the orientation selectivity shown by most cortical neurons for the nature of the signals they can convey about the direction of stimulus movement. On theoretical grounds we distinguish component direction selectivity, in which cells are selective for the direction of movement of oriented components of a complex stimulus, from pattern direction selectivity, or selectivity for the overall direction of movement of a pattern irrespective of the directions of its components. We employed a novel test using grating and plaid targets to distinguish these forms of direction selectivity. 2. We studied the responses of 280 cells from the striate cortex and 107 cells from the lateral suprasylvian cortex (LS) to single sinusoidal gratings to determine their orientation preference and directional selectivity. We tested 73 of these with sinusoidal plaids, composed of two sinusoidal gratings at different orientations, to study the organization of the directional mechanisms within the receptive field. 3. When tested with single gratings, the directional tuning of 277 oriented cells in area 17 had a mean half width of 20.6 degrees, a mode near 13 degrees, and a range of 3.8-58 degrees. Simple cells were slightly more narrowly tuned than complex cells. The selectivity of LS neurons for the direction of moving gratings is not markedly different from that of neurons in area 17. The mean direction half width was 20.7 degrees. 4. We evaluated the directional selectivity of these neurons by comparing responses to stimuli moved in the optimal direction with those elicited by a stimulus moving in the opposite direction. In area 17 about two-thirds of the neurons responded less than half as well to the non-preferred direction as to the preferred direction; two-fifths of the units responded less than one-fifth as well. Complex cells showed a somewhat greater tendency to directional bias than simple cells. LS neurons tended to have stronger directional asymmetries in their response to moving gratings: 83% of LS neurons showed a significant directional asymmetry. 5. Neurons in both areas responded independently to each component of the plaid. Thus cells giving single-lobed directional-tuning curves to gratings showed bilobed plaid tuning curves, with each lobe corresponding to movement in an effective direction by one of the two component gratings within the plaid. The two best directions for the plaids were those at which one or other single grating would have produced an optimal response when presented alone.(ABSTRACT TRUNCATED AT 400 WORDS)

Motion selectivity and the contrast-response function of simple cells in the visual cortex

1991 ◽  
Vol 7 (6) ◽  
pp. 531-546 ◽  
Author(s):  
Duane G. Albrecht ◽  
Wilson S. Geisler
Keyword(s):  
Visual Cortex ◽  
Receptive Field ◽  
Response Function ◽  
Gain Control ◽  
Direction Selectivity ◽  
Metabolic Energy ◽  
Simple Cells ◽  
Contrast Response Function ◽  
Spatiotemporal Receptive Field ◽  
Contrast Response

AbstractThe responses of simple cells were recorded from the visual cortex of cats, as a function of the position and contrast of counterphase and drifting grating patterns, to assess whether direction selectivity can be accounted for on the basis of linear summation. The expected responses to a counterphase grating, given a strictly linear model, would be the sum of the responses to the two drifting components. The measured responses were not consistent with the linear prediction. For example, nearly all cells showed two positions where the responses approached zero (i.e. two “null phase positions”); this was true, even for the most direction selective cells. However, the measured responses were consistent with the hypothesis that direction selectivity is a consequence of the linear spatiotemporal receptive-field structure, coupled with the nonlinearities revealed by the contrast-response function: contrast gain control, halfwave rectification, and expansive exponent. When arranged in a particular sequence, each of these linear and nonlinear mechanisms performs a useful function in a general model of simple cells. The linear spatiotemporal receptive field initiates stimulus selectivity (for direction, orientation, spatial frequency, etc.). The expansive response exponent enhances selectivity. The contrast-set gain control maintains selectivity (over a wide range of contrasts, in spite of the limited dynamic response range and steep slope of the contrast-response function). Rectification conserves metabolic energy.

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