Department of Neurobiology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261
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ABSTRACT |
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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.
Direction selectivity is an important property of neurons in primary visual cortex. In area 17 of cats, ~80% of cells in all layers are direction selective, responding strongly to a stimulus moving in one direction across their receptive field and weakly or not at all to movement in the opposite direction (Hubel and Wiesel 1962 Strobe and normal rearing
Fourteen kittens were reared from birth to 8-9 mo of age in a normal colony room illuminated only by a strobe lamp (PS-31, Grass Instruments) operating at 8 Hz (10 µs/flash) for 12 h/day, interleaved with 12 h of darkness. Recording sessions commenced from 4 h to 21 mo after their removal from the strobe room. Two additional kittens were reared under virtually identical conditions by Dr. Tatiana Pasternak at the University of Rochester, and we recorded from them at 12 yr of age. No differences were observed among animals in directional tuning or receptive-field structure, so data from all ages are combined. For comparison, data from five normally reared cats were collected under conditions identical to those used for testing the strobe animals.
General procedures
Methods were similar to those previously described (Saul and Humphrey 1990 Stimulus protocols
Visual stimuli were presented on a Tektronix 608 monitor driven by a Picasso image synthesizer (Innisfree) with a 200-Hz refresh rate, controlled by an LSI 11/73 computer. For all stimuli, mean luminance was 15 cd/m2, and Rayleigh-Michelson contrast was ~0.5. Standard stimuli were used to assess the visual response properties of cortical cells (Saul and Humphrey 1992a ORIENTATION SELECTIVITY AND SPATIAL- AND TEMPORAL-FREQUENCY TUNING.
Each cell's optimal orientation and tuning range were determined using drifting sinewave gratings of near-optimal spatial and temporal frequency. The cell's spatial response properties were characterized next using sinewave gratings drifting in each direction at near-optimal temporal frequency and at spatial frequencies ranging over 3 octaves. Temporal response tuning and direction selectivity were examined using gratings of optimal spatial frequency drifting in opposite directions over a range of temporal frequencies from 0.25 to 16 Hz. Each stimulus was randomly presented 5-10 times, at 4 s per trial, to generate a peristimulus time histogram (PSTH).
S-T RECEPTIVE-FIELD STRUCTURE.
Two methods were used to evaluate receptive-field structure in most cells. In the first an optimally oriented, stationary, elongated (5-8°) bar undergoing sinusoidal luminance modulation was used to generate a form of line-weighting function (LWF). The bar was placed in 8 or 16 positions spanning the receptive field and adjacent regions, and luminance was modulated at five to seven temporal frequencies, usually 0.5-6 Hz. Bar width was typically 0.2-0.3°. Each unique temporal frequency/bar position pair was presented randomly for 4 s, with 5-10 iterations of each pair, to generate a PSTH.
Data analysis
Action potentials were collected at 1-ms resolution and histograms constructed using ~5- to 8-ms binwidths. Responses to sinusoidally varying stimuli were analyzed by converting spike counts to firing frequency at each point in the stimulus cycle and Fourier analyzing each resulting PSTH; means ± SE of the fundamental response amplitude and phase were calculated (Saul and Humphrey 1992a AMPLITUDE TUNING.
For measuring spatial- and temporal-frequency tuning, curves of response amplitude versus frequency were fit by a difference of Gaussians function (Saul and Humphrey 1990 DIRECTION SELECTIVITY.
At each temporal frequency, direction selectivity was computed as the Rayleigh-Michelson (R-M) ratio, R-M = (PD
S-T RECEPTIVE-FIELD STRUCTURE.
The line-weighting functions derived from counterphasing bars were used to quantify the S-T inseparability of each receptive field. In principle, the procedure was equivalent to comparing the fits of a line and a step function to the response phase versus bar position data for each tested temporal frequency. In practice, we compared the residuals (R0, R1) of the fits for lines of zero slope (L0) and nonzero slope (L1). A separable receptive field has constant phase across space, except for half-cycle jumps between ON and OFF zones. We therefore used phase values modulo a half cycle for fitting the constant phase line, L0, to normalize ON and OFF responses. We compared a separable hypothesis where L0 gives a good fit, and an inseparable hypothesis were L1 fits better. The index of inseparability was R0/(R0 + R1). A perfect fit with L0 would give R0 = 0 and R1 > 0, and thus an inseparability value of 0 (i.e., complete separability). A perfect fit with L1 would give R0 > 0 and R1 = 0, and a value of 1 (i.e., complete inseparability). For population comparisons, an Inseparability Index (II) was computed for each cell that reflected the average of its inseparability values at 1 and 2 Hz (or higher frequencies for some cells).
LINEAR PREDICTIONS OF DIRECTION SELECTIVITY.
Our primary measure of S-T structure (the II) is based on the distribution of response phase across the receptive field. We recently showed (Murthy et al. 1998 Cell identification
Simple and complex cells were distinguished based on the segregation of ON and OFF zones in hand plots (Hubel and Wiesel 1962 Histology
Electrode tracks were reconstructed in Nissl-stained sections with the aid of HRP deposits applied extracellularly at the end of each penetration (Saul and Humphrey 1992a Statistics
All statistical comparisons of means were done using the t-test.
Directional selectivity was examined quantitatively in 128 and 81 simple cells, respectively, in strobe-reared and normal cats. S-T receptive-field structure was analyzed in about half of these cells. We first summarize the strobe-induced loss of direction selectivity and then document its impact on the receptive fields of typical cells. We then present population analyses that reveal that the directional loss reflects a virtual elimination of S-T inseparability. Finally, we show that strobe rearing only impacts directional tuning, leaving other response properties normal.
Direction selectivity
Figure 1, A and B, illustrates directional tuning as a function of temporal frequency for two simple cells in normal cats. The cell in A was highly selective at most frequencies, giving virtually no response in the nonpreferred direction. Its DI was 0.92. The cell in B responded over a roughly similar range of temporal frequencies but was direction selective only below 4 Hz (DI = 0.78). Although simple cells differ in the details of their directional and temporal frequency tuning (Saul and Humphrey 1992b
S-T receptive-field structure and direction selectivity: individual cells
Spatiotemporal structure was measured primarily from line-weighting functions obtained with counterphasing bars. For about one-half of the cells, S-T maps also were generated using sparse-noise stimulation. The latter maps were used to confirm qualitatively the S-T structure revealed in the LWFs and to make linear predictions of directional tuning. We first provide examples of S-T structures in normal cats and then show typical examples from strobe-reared animals.
NORMAL CATS.
S-T maps for a direction-selective cell recorded in layer 4B are shown in Fig. 3A. Each map plots the average response to a bar presented at six positions in the receptive field. Stimulus luminance was modulated at the indicated temporal frequencies, and a vigorous response was obtained at most positions. Hand plotting of the receptive field revealed an ON zone flanked by two OFF zones (see inset). The LWFs confirmed this spatial organization. For example, the map obtained at 1 Hz shows the ON zone at positions
STROBE-REARED CATS.
Strobe rearing had a striking effect on simple-cell receptive fields: virtually all were S-T separable. Results from a typical cell, recorded in layer 4B, are illustrated in Fig. 5. The cell responded well at all tested temporal frequencies but was not direction selective (Fig. 5C). Counterphasing bars revealed robustly responding ON and OFF zones; response timing was constant within each zone and differed by a half-cycle between them (Fig. 5, A and B). Consequently, all Inseparability values were uniformly low (
Relation between S-T inseparability and direction selectivity: population data
INSEPARABILITY INDEX.
Figure 7A summarizes the frequency distribution of II for simple cells in normal cats. A full range of values was seen; the mean index was 0.39 and >70% of the cells had indexes >0.2. In comparison, indexes for strobe-reared cats were uniformly low (Fig. 7B); the mean index was 0.09, and only 6% of cells had values >0.2. Qualitatively, indexes <0.2 reflected receptive fields that, under visual inspection, had little or no space-time orientation (e.g., Figs. 4 and 5). Thus nearly all receptive fields in strobe-reared cats were S-T nonoriented, whereas the majority in our normal sample were moderately to highly oriented.
INSEPARABILITY VERSUS DIRECTIONAL INDEXES.
In a recent study using counterphasing gratings to assess receptive-field structure, we reported that direction-selective cells in layer 4 generally had S-T well-oriented receptive fields (Murthy et al. 1998
LINEAR PREDICTIONS.
Fourier analyses of S-T maps were also employed to make linear predictions of directional tuning based on the distribution of response phase and amplitude in the receptive field (e.g., Albrecht and Geisler 1991
Strobe rearing does not affect other visual response properties
In agreement with previous reports (Cynader and Chernenko 1976 These experiments produced five major findings. 1) Strobe rearing reduced the proportions of direction-selective simple cells in area 17 from ~80% to ~10%. 2) The loss of direction selectivity reflected the elimination of S-T inseparable receptive-field structure; all of the nondirectional cells had separable receptive fields. 3) The few directional cells that existed after strobe rearing were selective over a narrower range of temporal frequencies, and exhibited weaker directional tuning, than normal. 4) Strobe rearing was highly selective; no changes in other measured receptive-field properties were seen. 5) The effects were permanent; the deficits were observed up to 12 yr postdeprivation.
Relation to previous studies
Cynader and Chernenko (1976) S-T receptive-field structure as a mechanism for direction selectivity
In this section we briefly review evidence linking receptive-field structure to directional tuning in normal cats, summarize two classes of models for direction selectivity that are founded on this link, and consider our data in light of the models.
Permanence of the changes in direction selectivity and S-T structure
These results add a new perspective to how altered visual experience early in life can modify neural networks. Previous studies have shown that spatial aspects of neural organization such as those for processing ocular inputs and contour orientation are modifiable during the critical period of development (for reviews, see Daw 1995
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). A variety of mechanisms has been proposed to account for this tuning (Douglas and Martin 1991
; Eysel 1992
; Hubel and Wiesel 1962
; Sillito 1977
), but the precise substrates remain a matter of debate. An important insight, initially made by Movshon et al. (1978)
and extended by others (Albrecht and Geisler 1991
; McLean and Palmer 1989
; Reid et al. 1987
), is that direction selectivity in simple cells is linked to the spatiotemporal (S-T) structure of the receptive field. When tested with stationary stimuli, many direction-selective cells display S-T inseparable structure, in which response timing changes progressively from one position to the next across the receptive field. This organization produces a space-time orientation to the receptive field that confers a preferred direction of motion by virtue of greater response summation to one direction than to the other (Jagadeesh et al. 1997
; McLean et al. 1994
; Reid et al. 1991
). In contrast, simple cells that lack directional tuning are all S-T separable. Their receptive fields are not oriented in space-time (McLean et al. 1994
), hence motion in either direction evokes similar responses.
) and to behavioral deficits in directional discrimination (Pasternak et al. 1985
; Pasternak and Leinen 1986
). The mechanisms underlying the directional loss have never been explored. Given the normal involvement of S-T structure in direction selectivity, we wondered whether strobe rearing might produce its effect by altering that structure, perhaps by eliminating S-T inseparability. Finding such a change would not only reveal how strobe rearing acts on cortex, but it would provide further support for the spatiotemporal model of directional tuning. Alternatively, S-T structure might be normal after strobe rearing, which would indicate that the directional loss depends on other mechanisms. Inhibition evoked by motion in the nonpreferred direction has been reported to be essential for direction selectivity (Eysel 1992
; Maex and Orban 1996
; Sillito 1984
; Suarez et al. 1995
). One type of inhibition proposed (Sato et al. 1995
) is that in which response thresholds are tonically raised so as to suppress weak activity. Such inhibition, however, would not be expected to impact response timing. Thus a strobe-induced loss of tonic inhibition would not affect S-T structure.
). In layer 4, most direction-selective cells have inseparable receptive fields, and the degree of inseparability correlates well with their directional tuning. In layer 6, inseparability is much weaker and poorly related to tuning. In the present study we were careful to distinguish these two layers.
) we explore the specific changes in response timings associated with the temporal reorganization of the receptive field and suggest a mechanism for how strobe rearing produces its effects. Portions of these results have been reported in abstract form (Humphrey and Saul 1995
; Saul and Humphrey 1994
).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
, 1992a
). Animals were anesthetized using halothane in 70% nitrous oxide-30% oxygen; halothane levels were 4%, 1.0-1.5%, and 0.2-1.0%, respectively, during induction, surgery, and recording. Heart rate, expired CO2, mean arterial blood pressure, and the raw and Fourier analyzed cortical electroencephalogram (EEG) were monitored throughout the experiment. Anesthetic was adjusted to maintain the dominant frequencies of the EEG below 4 Hz. Paralysis was maintained by continuous infusion of gallamine triethiodide (Flaxedil; 5 mg·kg
1·h
1) and d-tubocurarine chloride (0.35 mg·kg
1·h
1), in 6 ml/h of 5% lactated Ringer solution. Additional Ringer solution was administered at ~6 ml/h to maintain normal hydration and blood pressure. Wound margins and pressure points were infused with 2% lidocaine, and the head was supported by a skull attachment that allowed removal of the ear and eye bars.
) electrodes assured adequate sampling of small as well as large neurons (Humphrey and Weller 1988a
,b
). Each experiment was terminated by intravenously infusing a bolus of pentobarbital sodium (Nembutal), and the brain was perfused with aldehydes.
,b
).
). An elongated, narrow bar was randomly placed sequentially in 32 positions spanning the receptive field and adjacent regions. Bright and dark bars were used, at contrasts of 0.8 relative to background. Stimulus duration was 40 ms. Stimulus order was rerandomized for each trial. Ten to 35 independent trials, 32 s each, generated separate maps of responses to the bright and dark bars.
). Standard errors of phase were computed in the complex plane, with deviations weighted by the amplitudes (Saul and Humphrey 1992a
). Response phase was expressed in cycles (cyc). At low temporal frequencies 0.0 cyc corresponds to a response whose phase coincides with the maximal luminance, and 0.5 cyc reflects a response in register with the minimum luminance.
). Resolution frequency was taken as the frequency above optimum that elicited 10% of maximal response. Curves of response versus stimulus orientation were fit by a Gaussian function, with half-width at 1/e of the curve being the measure of orientation tuning.
NPD)/(PD + NPD), where PD and NPD are response amplitudes to the preferred and nonpreferred directions of motion, respectively. For each temporal frequency the two directions were compared using the t-statistic (Saul and Humphrey 1992b
). Our criterion for direction selectivity was an R-M ratio
0.33 and a t-score >2, reflecting a response at least twice as great in the preferred than nonpreferred direction, that differed at or below the 0.05 level of significance.
); and 3) strobe rearing did not affect temporal frequency tuning (Table 1). For a few (<5%) cells in each group whose directional tuning and/or optimal temporal frequency was shifted to much higher frequencies (e.g., >4 Hz), DIs were compiled at those higher frequencies that best reflected the directional tuning.
View this table:
TABLE 1.
Response properties of simple cells
,b
; Jones and Palmer 1987
). Spike trains were correlated with the position and contrast of the bars preceding each spike. Temporal resolution of the maps was generally 10 ms, with durations from 320 to 2,560 ms, depending on the type of analysis desired. Responses to bright and dark bars were compiled into separate maps, which were subtracted to yield a difference map of the net excitatory response to the two contrasts. ON and OFF excitatory regions are indicated, respectively, by continuous and dashed contours, with 10-16 levels between the maximum positive and negative responses.
) that a phase-based measure predicts directional tuning better than conventional linear predictions. The latter use response phase and amplitude, but amplitude nonlinearities produce underestimates of the linear component of direction selectivity. Nevertheless, to allow comparison of our data with those of other studies, we also used conventional linear predictions as follows. Response versus position data from the line-weighting functions were Fourier transformed to estimate the response amplitude to opposite directions of motion as a function of spatial frequency for each temporal frequency. The sparse-noise maps were similarly analyzed by 2-D transformation to the frequency domain. Predicted direction selectivity was then computed for each cell at its optimal spatial frequency and at a range of temporal frequencies (DeAngelis et al. 1993a
). To compare these predictions to actual DIs, the mean predicted direction selectivity at 1 and 2 Hz (or higher for some cells) was computed for each cell.
), line-weighting functions (Movshon et al. 1978
; Saul and Humphrey 1992a
), and/or sparse-noise tests (Jones and Palmer 1987
), and on the degree of response modulation to drifting gratings (Skottun et al. 1991
). Cells with only one zone were considered to be simple if they produced well-modulated responses to drifting gratings of high spatial frequency. Cells were deemed unclassified if their receptive-field structure was unclear.
). Laminar borders were identified using standard criteria (Humphrey et al. 1985
; O'Leary 1941
), and cell recording locations were assigned accordingly.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
), these profiles are representative of most neurons in area 17 of normal cats.
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FIG. 1.
Typical examples of temporal frequency tuning curves for cells in normal (A and B) and strobe-reared (C and D) cats. Open and filled circles represent average fundamental response amplitudes (±SE) to sinewave gratings moving in opposite directions. Each set of responses is fit by a difference-of-Gaussians function. The directional index (DI), reflecting the average tuning at 1 and 2 Hz, is indicated for each cell.
0.12). These tuning curves are representative of nearly all cells in strobe-reared cats.
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FIG. 2.
Frequency distributions of DIs for simple cells in normal (A) and strobe-reared (B) cats. The mean DI in A and B is 0.65 and 0.15, respectively; the difference is significant (P < 0.001). Strobe rearing reduced the frequency of direction-selective cells to ~10% from a norm of 80%. Arrows indicate a DI of 0.33, reflecting a response twice as great in the preferred than nonpreferred direction.
0.4° and
0.1° discharging to increasing stimulus luminance, and the OFF flanks at positions
1.0°, and +0.1° to +0.4° firing with deceasing luminance.
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FIG. 3.
Spatiotemporal (S-T) structure and directional tuning of a direction-selective simple cell in layer 4B of a normal cat. A: peristimulus time histograms (PSTHs) of responses to a stationary bar undergoing sinusoidal luminance modulation at 6 positions in the receptive field and 3 temporal frequencies. Two cycles of stimulation are shown for clarity, with the 2nd response in each PSTH being a duplicate of the 1st. Each set of PSTHs provides an S-T map of the receptive field at 1 temporal frequency; all maps reveal a highly S-T oriented field. The handplotted receptive-field and bar stimulus are shown to the right; bar width and field dimensions are scaled to the S-T map. The vertical scale bar and response scaling value (in impulses/s) are shown in the top right of each map. Values for receptive-field position reflect rounding. B: mean ± SE 1st harmonic response phase is plotted as a function of bar position for each temporal frequency tested. Note that the standard errors for many points are smaller than the symbols used to indicate phase. Phase values were adjusted by addition of integers to minimize the difference between adjacent positions and maintain increasing phase with temporal frequency. Each set of phase vs. position values was fit by lines (not illustrated; see METHODS) to derive an Inseparability value, which is indicated in parentheses. C: mean ± SE fundamental response amplitude is plotted as a function of the temporal frequency of a grating drifting in opposite directions. The cell was highly direction selective up to ~4 Hz (DI = 0.98). D: space-time response profile obtained by the use of the sparse-noise method. Contours represent net excitatory responses to the bright (continuous lines) and dark (dashed lines) bars. The receptive field is highly oriented in space-time. For illustration, the contours in this and following figures were smoothed slightly using a narrow Gaussian filter.
).
1.5° also was revealed. All regions were highly oriented in space-time, as expected for an inseparable receptive field (DeAngelis et al. 1993a
,b
; McLean et al. 1994
). Transformation of these data to the frequency domain yielded a predicted DI of 0.56, about one-half that actually observed (0.98).
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FIG. 4.
S-T structure of a nondirectional cell in layer 6 of a normal cat. A: receptive-field maps obtained using 3 temporal frequencies of luminance modulation. The receptive field was S-T separable. B: phase vs. bar position plots for 6 temporal frequencies. Response phase was constant within each zone and differed by a half cycle between zones. C: response amplitude vs. temporal frequency for a drifting grating reveals that the cell was insensitive to direction at all drift rates. D: response profile obtained using sparse-noise stimulation revealed a nonoriented space-time map; predicted DI = 0.08. All conventions are as in Fig. 3.
0.16). This basic spatiotemporal organization was confirmed by sparse-noise stimulation (Fig. 5D), which predicted no directional tuning.
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FIG. 5.
S-T structure of a cell lacking direction selectivity in layer 4B of a strobe-reared cat. A: S-T maps show an inseparable receptive field. B: phase vs. bar position plots for different temporal frequencies confirm the constancy of timing within the receptive field except for the half-cycle difference between ON and OFF zones. C: amplitude vs. temporal frequency plots show that the cell was not direction selective (R-M ratio 0.22 at all frequencies). D: response profile obtained using sparse-noise stimulation confirmed the absence of space-time orientation. Predicted DI = 0.06. Conventions are as in Fig. 3.
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FIG. 6.
S-T structure of a nondirectional receptive field in layer 4 of a strobe-reared cat. A: S-T maps reveal 2 ON and 3 OFF zones. B: phase vs. bar position plots reveal half-cycle differences in response timing between each zone, yielding uniformly low inseparability values at all temporal frequencies. Grid lines are added to the ordinate to help visualize the half-cycle jumps. C: response profile obtained with sparse noise. Except for a slightly oriented "bridge" at position 0.8°, the receptive field was nonoriented in space-time. Predicted DI = 0.18. Conventions as in Fig. 3.
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FIG. 7.
Frequency distributions of Inseparability Indexes among simple cells in normal (A) and strobe-reared (B) cats. Strobe rearing eliminated virtually all inseparable receptive-field structure. The mean Index in A and B is 0.39 and 0.09, respectively; the difference is significant (P < 0.001).
). Cells in layer 6, in contrast, displayed uniformly low S-T orientation despite being direction selective. Here we reexamine these two laminar regions with regard to inseparability measured with the use of counterphasing bars.
).
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FIG. 8.
Inseparability vs. direction selectivity among simple cells as a function of cortical layer. A and B: cells recorded in layer 4 and along its border zone with layers 3 and 5. C and D: cells localized to layer 6 and the 5/6 border; D includes 6 cells recorded in layer 5B. A: in layer 4 of normal cats, there was a wide range of inseparability and directional values, and the 2 indexes were well correlated (r = 0.77; slope = 0.78). B: strobe rearing eliminated direction selectivity and inseparability in nearly all layer 4 cells; among cells that were not direction selective, the 2 measures were uncorrelated. C: in layer 6 of normal cats, there was a wide range of direction selectivities, but cells displayed low inseparability values (r = 0.79, slope = 0.30). D: strobe rearing not only eliminated direction selectivity in the infragranular layers, it further reduced inseparability values there (r = 0). The sign of inseparability value indicates whether the S-T maps predicted the preferred direction of motion correctly (positive values) or incorrectly (negative values). Arrows indicate criterion breakpoint for direction selectivity.
). The mean of the absolute values of IIs for the cells was 0.17.
; DeAngelis et al. 1993a
,b
). Evaluating first the maps obtained with counterphasing bars, Fig. 9A plots DI versus predicted DI for simple cells in all layers of normal cats. Despite the full range of DIs, predicted selectivity was generally low (mean absolute value = 0.23). The correlation between the two measures was 0.5, a value similar to that reported for simple cells in all layers by Reid et al. (1991)
and Murthy et al. (1998)
based on responses to gratings. Among strobe-reared cats (Fig. 9B) predicted direction selectivity was significantly lower than normal (mean absolute value = 0.07, P < 0.001), matching at least qualitatively the loss of directional tuning.
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FIG. 9.
Linearly predicted vs. actual directional tuning. Predictions were made at the same temporal frequencies as those used for calculating DI. A and B: predictions based on line-weighting functions. Strobe rearing reduced mean predicted selectivity from a norm of 0.23 to 0.07 (absolute values used). C and D: predictions based on maps obtained using sparse-noise stimulation. Absolute value of predicted direction selectivity was 0.29 and 0.09, respectively, for normal and strobe-reared cats. The sign of the prediction value indicates whether the S-T maps predicted the preferred direction of motion correctly (positive values) or incorrectly (negative values). Arrows indicate criterion breakpoint for direction selectivity.
and McLean et al. (1994)
, although the slope (0.30) is lower. Again in strobe-reared animals, however, the S-T maps predicted the loss of direction selectivity (Fig. 9D). The absolute value of the mean predicted selectivity was 0.09, significantly lower than normal (P < 0.05).
) reviewed evidence (e.g., Albrecht and Geisler 1991
; Movshon et al. 1978
; Reid et al. 1991
) that conventional "linear" predictions are confounded by static nonlinearities that result in underestimates of the linear component of direction selectivity. Response phase is not affected by such nonlinearities. Thus the II, which reflects only response phase, should better predict directional tuning.
; Pasternak et al. 1985
), we found that strobe rearing had a remarkably specific effect on simple cells, impacting only direction selectivity. Qualitatively, there were no deviations from normal in the sampling of simple, complex, and unclassifiable cells or in their optimal orientations and ocular dominance values. The numbers and widths of ON and OFF zones in simple-cell receptive fields were normal, and cells were quite visually responsive to stationary and moving stimuli. In fact, if one were not aware that most area 17 cells are normally direction selective, no deficits would have been noticed.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
discovered that rearing cats in 8-Hz stroboscopic illumination reduced the number of direction-selective cells in area 17 from ~80% to ~10%. Their stimuli were hand-held bars of light, and the deficit was associated with all cell classes. Pasternak et al. (1985)
confirmed this and suggested that the directional loss might be greater among complex than simple cells. Our results from qualitative testing confirm the paucity of directional tuning in both cell classes following strobe rearing. Because our quantitative tests were restricted to simple cells, we cannot address the relative impact of the rearing on different classes. However, it is clear that simple cells were profoundly affected.
; Cynader et al. 1973
; Kennedy and Orban 1983
; Olson and Pettigrew 1974
) have examined how lower rates of strobe stimulation, generally 0.5-2 Hz, affect cortical organization. Such rates not only tend to reduce directional tuning but affect other response properties. On the whole, the changes include a reduction in the number of orientation-selective cells and/or a widening of orientation tuning (Cremieux et al. 1987
; Cynader et al. 1973
); abnormal spatial receptive-field structures (Cynader et al. 1973
; Kennedy and Orban 1983
); alterations in velocity tuning and its dependence on retinal eccentricity (Kennedy and Orban 1983
); and reduction in the frequency of binocular receptive fields (Cremieux et al. 1987
; Kennedy and Orban 1983
; Olson and Pettigrew 1974
). This broader range of deficits probably reflects illumination conditions that approach dark rearing. Rearing kittens in the dark results in widespread and profound degradative changes in cortical receptive-field structures and response selectivities (Sherman and Spear 1982
). At low strobe rates the stimulation may be insufficient to sustain normal maturation of circuits underlying spatial and temporal structures. An 8-Hz rate does suffice.
). We note in the companion paper (Humphrey et al. 1998
) that cells in the lateral geniculate nucleus (LGN) of strobe-reared cats also are normal in their frequency tuning. In normal cats, cells in area 17 tend to have lower temporal resolution than their geniculate inputs (Orban et al. 1985
). This difference is thought to reflect integrative mechanisms in cortex that effect low-pass filtering (Orban et al. 1985
), although inputs from lagged-type LGN cells, which have low temporal resolution (Saul and Humphrey 1990
), may account for some of the difference. Whatever the mechanisms for the cortical tuning, they appear either to be resistant to alteration by strobe stimulation or to readjust quickly (within hours?) when cats are moved into natural illumination. We cannot directly address the issue of readjustment, but we note that temporal frequency tuning was not obviously different when cats were tested immediately or many months after removal from the strobe room. Regarding LGN inputs, we show in the following paper (Humphrey et al. 1998
) that strobe rearing did not affect the development of lagged cells.
), the superior colliculus (Flandrin et al. 1976
), and the lateral syprasylvian area (Spear et al. 1985
). We did not examine area 18, but it is likely that the directional loss there also reflects changes in S-T receptive-field structure. This follows simply because S-T structure and direction selectivity are correlated in area 18 (McLean et al. 1994
). The loss of directional tuning in the superior colliculus and lateral suprasylvian cortex is probably secondary to changes in areas 17 and 18 because, in normal cats, direction selectivity in these territories is dependent on inputs from primary visual cortex (Rosenquist and Palmer 1971
; Spear and Bauman 1979; Wickelgren and Sterling 1969
; but cf. Guedes et al. 1983
; Mendola and Payne 1993
). Thus the strobe-induced changes in S-T structure in primary visual cortex probably have widespread consequences for processing directional information elsewhere in the brain.
showed that the cats display normal, low-contrast thresholds for detecting whether a grating is moving, but they require contrasts at least 10 times higher than normal to discriminate the direction of motion. Further, at moderate spatial frequencies (
0.77 cycle/deg) they cannot discriminate direction despite being able to spatially resolve stimuli and detect that they are moving. In addition, cats' ability to determine the direction of stimulus motion in the presence of visual noise is greatly reduced by strobe rearing (Pasternak et al. 1990
). Together, these studies clearly demonstrate the importance of direction-selective neurons for detecting and discriminating the trajectories of moving objects.
; Reid et al. 1991
; Tolhurst and Dean 1991
). This heterogeneity partly reflects cells' laminar locations (Murthy et al. 1998
). Cells in and adjacent to layer 4 display the most prominent S-T orientation, and a moderate to strong relationship exists between S-T structure and direction selectivity. On average, S-T orientation predicts over one-half the observed directional tuning in layer 4 cells. Layer 6 cells, in contrast, uniformly display weak or no first-order S-T orientation despite being as directionally tuned as layer 4 cells.
) that directional tuning in most layer 4 cells can be accounted for by a linear-nonlinear model (i.e., "exponent model," Albrecht and Geisler 1991
; Heeger 1993
; Jagadeesh et al. 1997
). Here linear S-T summation across an S-T oriented receptive field confers a preferred direction of motion. This preference is then accentuated via a static, power-law amplification of suprathreshold responses, and suppression of subthreshold responses, to produce stronger directional tuning. This exponent model fails to account for strong direction selectivity in layer 6 because cells there lack even moderate first-order S-T orientation. Dynamic nonlinear processes likely predominate in layer 6.
). These maps reveal motion kernels (Emerson and Citron 1992
), or interaction functions (Baker and Boulton 1994), that are S-T inseparable. They show that nonlinear facilitatory and/or suppressive interactions are dependent on temporal offsets of responses evoked at different spatial positions. Importantly, the interaction functions accurately predict direction selectivity among cells that are first-order separable (Emerson and Citron 1989
). It is likely that these types of interactions account for directional tuning in layer 6. Overall, this brief review suggests that S-T inseparability, whether revealed in first- or second-order maps, is a critical determinant of direction selectivity.
; Heeger 1993
), would be incapable of producing direction selectivity.
). Although we have not measured second-order structure, a clear prediction from this work is that the directional deficit in layer 6 reflects a loss of second-order inseparability.
) as a nonspecific inhibition that simply raises a cell's threshold to excitatory inputs. It would affect response amplitude but not phase. The fact that the temporal receptive-field structure was markedly altered by strobe rearing indicates that mechanisms other than nonspecific suppression are critical. We will address the issue of mechanisms in the following paper (Humphrey et al. 1998
).
; Sherman and Spear 1982
). Ocular dominance changes such as those induced by monocular lid suture primarily reflect alterations in connectivity that are permanent and that produce enduring amblyopia. Our study reveals that the temporal organization of cells' receptive fields is also developmentally modifiable, and once changes are made they are permanent. Indeed, we were struck by the S-T separability of all simple-cell receptive fields in the two Rochester cats strobe reared 12 yr before our recordings. These animals, labeled 810 and 811 in Pasternak and Leinen (1986)
, had undergone years of extensive psychophysical testing that required them to make fine directional discriminations. Despite the training, there was no improvement in their visual behavior nor any significant reorganization of their S-T receptive-field structure. This implies that strobe rearing caused permanent changes in the inputs to, and connections among, cortical cells. In the following paper (Humphrey et al. 1998
) we describe the changes in specific response timings within receptive fields of strobe-reared cats and suggest how alterations in convergence patterns of afferents to cortical cells could give rise to these changes.
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ACKNOWLEDGEMENTS |
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We thank P. Baker for computer programming, M. Kieler for electronics support, and J. Feidler for helpful discussions and comments on the manuscript. We are particularly grateful to Dr. Tania Pasternak for kindly providing the first strobe-reared cats used in this study.
This research was supported by National Eye Institute Grants EY-06459 to A. L. Humphrey, EY-10826 to A. B. Saul, and a Core Grant for Vision Research (EY-08098) to the Eye and Ear Institute of Pittsburgh.
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FOOTNOTES |
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1 The nonzero and sometimes negative Inseparability values for nondirectional cells reflect noise in the inseparability measure, which can be slightly affected by excessive variations in response timings in some receptive fields.
2 By first-order we mean maps, such as those here, derived from responses to stationary stimuli presented singly.
Address for reprint requests: A. L. Humphrey, Dept. of Neurobiology, BST E1440, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261.
Received 30 March 1998; accepted in final form 17 August 1998.
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REFERENCES |
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