INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX REFERENCES

The improvement of sensory abilities with practice has been demonstrated for somatosensory, auditory, and visual stimuli in both animals and humans (Goldstone 1998). Studies of neurons in primary auditory and somatosensory cortex have revealed training-related changes in both the mapping of response properties across the cortical surface and the sensitivities of individual neurons. These changes suggest that adult cortex is remarkably plastic; training can increase the number of neurons whose selectivities correspond to the demands of the training task (Jenkins et al. 1990a; Recanzone et al. 1993) and can increase neuronal selectivity (Recanzone et al. 1992b).

In primary visual cortex (V1) plasticity of neuronal response properties has also been observed during the course of normal development (Chapman and Stryker 1993; Crair et al. 1998; DeAngelis et al. 1993; Fregnac and Imbert 1978; Ghose et al. 1994b; LeVay et al. 1980; Sclar et al. 1985), in response to environmental modifications including monocular deprivation (Blakemore et al. 1978, 1981; Cynader et al. 1980; Hubel and Wiesel 1965; Hubel et al. 1977; Olson and Freeman 1978, 1980; Shatz and Stryker 1978; Swindale et al. 1981; Wiesel and Hubel 1965a,b) and ocular misalignment during development (Chino et al. 1991, 1994; Kumagami et al. 2000; Sasaki et al. 1998). Plasticity in adult visual cortex has been shown in response to localized deafferentation by retinal lesioning (Chino et al. 1992, 1995; Gilbert and Wiesel 1992; Heinen and Skavenski 1991; Kaas et al. 1990). Yet few studies have addressed how neuronal properties in adult V1 change as a consequence of training. This is clearly important in order to understand whether the changes that have been reported in other modalities reflect a general property of sensory cortices. Moreover, visual cortex is an ideal arena for examining these changes for a number of reasons. First, our understanding of the synaptic (Adrien et al. 1985; Bear and Daniels 1983; Bear and Singer 1986; Bear et al. 1983; Carmignoto et al. 1993; Ghose et al. 1994a; Gu and Singer 1993; Hendry and Jones 1986; Kleinschmidt et al. 1987; Maffei et al. 1992; Ramoa et al. 1988; Speed et al. 1991) and anatomical (Antonini and Stryker 1993, 1996; Elliott et al. 1996; Kossel et al. 1995) aspects of such plasticity is more advanced for visual cortex than it is for any other sensory cortical area. Second, the anatomy, functional architecture, and receptive field selectivities of adult visual cortex are well characterized. Third, many studies have demonstrated improvements in visual discrimination with practice. The relatively sophisticated understanding of vision both physiologically and psychophysically enables a more detailed examination of correlations between behavior and physiology than is possible for other modalities. For example, the observed changes in other sensory cortices have been associated with parameters that are mapped among the inputs to the cortex: frequency in the case of auditory cortex and somatotopy in the case of somatosensory cortex. Neurons in visual cortex are robustly selective for many parameters that do not correspond with receptor surface (retinotopy), including orientation, spatial frequency, color, and disparity. Moreover, the early stages of visual cortex offer the opportunity to examine how training affects cortical processing specifically because several of these visual selectivities, including orientation and binocularity, first appear at the level of cortex.

To study the physiological correlates of perceptual learning in the early visual system, we trained two macaques to discriminate fine changes in orientation at a specific location in the visual field and around a fixed orientation. We then measured the response properties of cells in V1 and V2 that represented trained or untrained locations. Both animals showed considerable behavioral improvement with training. In contrast to studies in auditory and somatosensory cortex, we found only small location- and orientation-specific effects on neuronal responses. These results suggest that changes in early visual cortex may not underlie the behavioral improvements that arise from such training.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX REFERENCES

Behavioral training

Two adult monkeys (Macaca mulatta) were first trained to discriminate orthogonally oriented stimuli in a match to sample task. During this initial training the animals sat unrestrained in a primate chair for daily training sessions that lasted from 2 to 4 h. At other times the animals were unrestrained in primate cages and food was provided ad libidum, but liquid consumption was restricted to the training session in which juice or water rewards were given for correctly performed trials. Visual stimulation and behavior control were computer controlled. Stimuli were presented on a video display on a gray background (15.6 cd/m², CIE x = 0.33, y = 0.33). Each gun of the display was gamma-corrected for 256 (8 bit) levels. Stimuli were achromatic sinusoidally counter-phasing Gabors (temporal frequency = 3 or 4 Hz; spatial frequency = 2 cycles/deg,  = 0.5°) that were oriented either horizontally and vertically during this phase of the training. Trials consisted of a presentation of a sample stimulus followed by a 500-ms delay and then a test stimulus. Trials began when the monkey depressed a lever mounted in front of the chair in response to the appearance of a Gabor. The monkeys' task was to indicate whether the subsequently presented Gabor differed in orientation by releasing or not releasing the lever. Matching and nonmatching trials occurred equally often in a random sequence. One animal was required to release the lever for matches; the other animal had to release for nonmatches.

Once the monkeys learned to discriminate nonmatching stimuli that differed by 90°, the spatial frequencies of the stimuli were gradually changed over the course of several weeks such that the sample and test stimuli were of different spatial frequencies on each trial. This behaviorally irrelevant change in spatial frequency was introduced for several reasons. First, it made the task more demanding. Second, it reduced the chance that positional clues such as spatial phase could be used to solve the task. Third, because only two spatial frequencies were used, it provided a control for the effects of repeated exposure: any differences seen in response properties with respect to orientation that are not present with respect to spatial frequency cannot be explained simply by repeated exposure to the stimuli. Fourth, because most single neurons in the visual cortex are selective for both orientation and spatial frequency, it ensured that the task would either involve groups of neurons or would create neurons with fundamentally different response selectivities (i.e., bimodal or unusually broad spatial frequency tuning). In either case, the chances of detecting such a change would be larger than if the task could potentially be solved by the signals produced by a small number of normal neurons in visual cortex. Finally, it allowed us to examine potential correlates of attribute-selective training since the monkeys had to learn to ignore spatial frequency differences that were readily discriminable while attending to barely discernible changes in orientation.

After the monkeys performed this orientation task at a 90% correct for stimuli of 1 and 4 cycles/deg, a head post and scleral search coil were surgically implanted. After a 2-wk recovery period, the monkeys were trained to fixate. Once the animals could maintain fixation for 1.5 s within a square 1.2° across, location-specific training was begun using Gabors presented in the lower right quadrant at 3° eccentricity and 30° from the vertical meridian. These trials began when the monkey fixated on a small dot (0.1°) on the screen and depressed the lever. Sample stimuli were presented for 500 ms following an initial 500-ms prestimulus period. In monkey 2, 17 behaviorally irrelevant Gabors (distractors) were also presented in other locations during the sample and test periods. The distractor Gabors had random orientations, spatial frequencies, and temporal phases. The 18 Gabors (17 distractors + 1 training Gabor) were arranged in a regular grid at eccentricities 1.5, 3.0, and 6.0° with an angular interval of 60°. The Gabors were scaled for eccentricity:  was 0.25, 0.5, and 1.0° for the different eccentricities. For the monkey in which distractors were used, the gradual reduction of orientation difference at the training location was only begun after the monkey performance with full contrast distractors was around 95%. For the next 5-6 mo, orientation differences were gradually reduced so that the average correct performance in a daily session was no less than 75%.

Electrophysiological recording

When the training was complete, a second surgery was performed to implant a recording chamber over the portions of V1 and V2 representing the trained location. Maintenance of the trained threshold was verified by presenting 100-200 training trials to the monkeys at the beginning of each recording session before any electrophysiological recording. While neurophysiological data were being recorded, the monkey performed a different match-to-sample task using pairs of diagonally oriented fine lines (length 0.2°) surrounding the fixation point (eccentricity ~0.1°). Eye movements were minimal since the behavioral task was at the fixation point, and the peripherally presented stimuli were behaviorally irrelevant. In one of the animals, eye position data were acquired for both the fixation and the trained task. In this animal the average eye position difference between the two tasks was 0.14°.

The monkey's task was to use the lever to indicate whether the lines presented in the test period matched those of the sample period. Nonmatching lines differed by 90° in orientation. The timing of the sample and test stimulus presentations was the same as was used for the peripheral orientation discrimination training. Performance on this task was above 95%. Response properties of neurons were recorded using behaviorally irrelevant stimuli presented at the receptive field location during both the sample and test periods.

Single neurons in V1 were recorded extracellularly using transdural Pt-Ir electrodes (~1 M). To reduce selection bias while searching for cells, gratings of all orientations were presented in random interleaved sequences (Ringach et al. 1997). The timing of action potentials from isolated neurons and presentation of visual stimuli were recorded with 1-ms resolution. Eye position and lever movements were recorded with 5-ms resolution.

Once a single unit was isolated, its receptive field position, optimal orientation, and optimal spatial frequency were initially estimated by presenting Gabors with manually chosen parameters. After this initial estimate, Gabors were presented in computer-controlled randomly interleaved sequences to quantitatively measure response properties. Orientation selectivity was assessed using a fixed set of eight different orientations (22.5° increments). The optimal orientation was then used to measure selectivity for spatial frequency and size ( of the Gaussian envelope describing the Gabor). If any of these subsequent runs revealed an optimal parameter appreciably different from the initial estimate, orientation tuning was reexamined with the new optimal parameter (approximately 20% of neurons). Stimulus centering with respect to receptive field position was verified by ensuring that neurons responded to optimal stimuli whose  was 0.1°. To facilitate comparisons between different cells, all parameters were varied over consistent ranges: spatial frequency from 0.5 to 8 cycles/deg (octave increments); size from 0.1 to 0.5°. All tests included 12 repetitions of 500-ms presentations.

Identical methods were used for recording from the trained and untrained representations in V1 and V2. For studying the untrained representations in V1 and V2, a second recording chamber was mounted over the opposite hemisphere. For each recording region, approximately 100 cells from each animal were recorded with 23 to 45 electrode penetrations. About one-half of the V2 penetrations were done with transdural electrodes; in the remaining penetrations, guide tubes were used to penetrate the dura.

For monkey 2, after chronic and behavior testing was completed, multiunit activity in the trained hemisphere was recorded in an acute experiment in which recordings were made in an anesthetized (sufentanil) and paralyzed (vercuronium) preparation. No acute mapping was done in monkey 1 because the trained representation of V1 was unexpectedly damaged during V2 recording. Procedures for animal preparation and maintenance have been detailed elsewhere (Maunsell et al. 1999). Vertical penetrations were made at regular 1-mm intervals along a grid spanning the representation of the trained region in V1 and V2. Monocular multiunit receptive fields were plotted on a tangent screen using a hand-held projector. For each penetration, receptive field boundaries were confirmed by plotting receptive fields at two or more sites separated by at least 200 µm.

Behavioral testing

After neurophysiological data had been collected from trained and untrained regions in V1 and V2, extended psychophysical testing of orientation discrimination performance was done. Orientation discrimination thresholds were measured at an untrained location 3° from the vertical meridian in the lower left quadrant. For monkey 1, discrimination thresholds were determined by measuring performance to various orientation changes and taking the orientation difference associated with 79% performance on a fitted exponential sigmoid. For monkey 2, thresholds were measured by a staircase procedure that converged at a performance level of 79%. The staircase procedure was repeated to give an estimate of the variability of performance. Because of the aforementioned V1 damage in monkey 1, we were unable to obtain behavioral thresholds for nontrained stimuli at the trained location in that animal. However, for monkey 2, we evaluated the orientation specificity of the behavioral improvement. Probe trials were randomly inserted within a standard discrimination training run. For such trials, the monkey's task was the same peripheral orientation discrimination task that was trained, except that the base orientation around which stimuli were oriented and the orientation difference between nonmatching stimuli were varied.

Electrophysiological analysis

DESCRIPTIVE FUNCTIONS. Response functions for orientation, spatial frequency, and size (Table 2) were fit using a maximum likelihood method (Geisler and Albrecht 1997). Orientation responses were modeled by a wrapped Gaussian (Swindale 1998), and spatial frequency and size were modeled by symmetric Gaussians. Maximum-likelihood fits were obtained using measured spike count means and by assuming variance to be proportional to the mean (Geisler and Albrecht 1997).

DETECTION THEORY. To relate the physiological observations to performance in the task, we evaluated the performance of an ideal observer of the neuronal responses to the training stimuli. Because we typically did not record from neurons while the animal performed the discrimination task, we inferred the responses to our training stimuli using fitted descriptive functions of orientation and spatial frequency and assuming that the selectivities for these two parameters are separable. Specifically, we constructed two orientation tuning curves for 1 and 4 cycles/deg based on ratios derived from the spatial frequency tuning curve and the orientation tuning curve acquired at the preferred spatial frequency.

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION APPENDIX REFERENCES

Perceptual learning

Throughout training the orientation difference was reduced whenever the animals were performing at 80% correct for 200-400 trials. Within several days, the orientation difference was reduced from 90° to about 15-20° around an orientation of 45°, which is roughly the range in which naive humans perform this task (Fig. 1). Further reductions in the orientation discrimination threshold occurred more slowly, such that a threshold of 4-5° was reached only after about 6 mo of training (~100,000 correct trials). Behavioral improvements were well modeled by single exponentials. This pattern of slowing improvement is similar to that seen in monkeys during tactile discrimination training (Recanzone et al. 1992a).

View larger version (19K): [in this window] [in a new window]   Fig. 1. Orientation discrimination thresholds as a function of training in 2 macaques. The training of monkey 1 is shown in A, and the training of monkey 2 is shown in B. Each point indicates the average orientation difference of nonmatching trials in a daily recording session, which typically included 1,000-2,000 correct trials during the initial training. Thresholds were adjusted to maintain a performance of 75-80% correct trials. In both animals, initial training produced rapid changes in threshold. Reduction of threshold after 40,000 correct trials was considerably slower. The thresholds were fit by a single exponential, indicating asymptotic thresholds at 4.3 and 6.1° for the 2 monkeys.

Behavioral performance for untrained locations and orientations was measured after all recordings had been completed. For both animals, performance was measured for stimuli presented at an untrained location directly across the vertical meridian from the trained location. Orientation was varied around both the trained orientation (45°) and an untrained orientation (135°). For monkey 2 performance was also measured for an untrained orientation (135°) at the trained location. All performance was measured in the absence of any distractors.

In both animals learning was orientation specific (Table 1): orientation discrimination thresholds at both locations were poorer for stimuli varying around an untrained orientation and were similar to thresholds observed at the beginning of training (Fig. 1). In contrast, there was a much smaller effect of retinotopic position: orientation thresholds in the untrained location were similar to those seen in the trained location. The trained-orientation/untrained-location threshold was much lower than the trained-location/untrained-orientation threshold. The psychophysical data therefore indicate that despite orientation- and location-specific training, perceptual improvements were orientation specific but only marginally location specific. This is particularly notable for monkey 2, because the untrained location corresponded to the location of a distractor that had to be ignored during the course of training.

Single-cell receptive field properties

Orientation tuning curves were acquired from 867 cells in two animals. Spatial frequency and optimal size tuning was evaluated for 775 and 651 of these cells, respectively (Table 3). Only cells whose receptive fields overlapped the training stimuli (RF centers within 1.5 of the center of the training stimuli) were included in the trained population. Cells from the trained hemisphere outside of this border were excluded from analysis. Figure 2 shows cumulative distributions of cells in the trained hemisphere (dashed lines) and cells within the trained location (solid lines) for V1 and V2. Of the 169 V1 cells in the trained hemisphere, 139 were accepted for analysis; of the 153 V2 cells, 129 were accepted.

View larger version (15K): [in this window] [in a new window]   Fig. 2. The distribution of receptive field centers of cells in the trained hemisphere. Gray lines indicate the contrast function of the Gaussian envelope describing the Gabors used for training ( = 0.5°). Solid black lines indicate the cumulative distribution of receptive field locations after the application of a 0.75° criterion. The cells described by this distribution were considered to be within the training region for subsequent analyses. Dashed lines indicate the cumulative distribution of distances for all cells recorded from the trained hemisphere.

Figure 3 shows the responses and fitted descriptive functions for one cell from the trained V1 population and another cell from the untrained V1 population. Solid lines indicate the fitted functions for mean firing rates. Tuning curves were considered well fit when the correlation coefficient between the observations of response means and the fitted model was at least 0.80. For each neuronal population, approximately 75% of the functions met this criterion (Table 3). Among well-fit tuning curves, the average correlation coefficient for orientation was 0.93, and for spatial frequency and size was 0.96 in both V1 and V2 populations. The mean parameters in all neuronal populations were consistent with those reported by Geisler and Albrecht (1997) using similar methods.

View larger version (23K): [in this window] [in a new window]   Fig. 3. Two example cells from trained and untrained V1 and their descriptive function fits (solid lines). Circles indicate observed firing rates. Vertical lines indicate ±1 SE error bars, which are too small to be visible in most cases. A and B: orientation responses and their fitting by a wrapped Gaussian. C and D: mean firing rates as a function of spatial frequency and their fitting by a Gaussian. E and F: mean firing rates as a function of stimulus size ( is the space constant of the Gaussian envelope describing the Gabor patches used as stimuli). Bold values on the abscissas of A-F indicate parameter values used during training.

Receptive field properties were similar between trained and untrained populations and between trained and untrained orientations. Most receptive field properties did not depend on either receptive field location or preferred orientation. In the few cases in which significant differences were present, there were small and not obviously consistent with the pattern of improved performance (Table 1). The remainder of this section details the analyses used to examine the dependence of receptive field properties on location and orientation.

Preferred orientation distributions were compiled for each of the four neuronal populations (Fig. 4). In both animals there was a small but significant bias in the distribution of preferred orientations (Raleigh test, P < 0.005) in the V1 population representing the trained location (Fig. 4A). Unexpectedly, there were significantly fewer cells whose preferred orientations were near the trained orientation (45°) than would be expected with an unbiased distribution (V-test, P < 0.005). A similar trend was seen in the V2 trained population (B), but it was not statistically significant. No significant biases with respect to orientation were seen in the untrained populations (C and D).

View larger version (16K): [in this window] [in a new window]   Fig. 4. Preferred orientation distributions for the 4 studied neuronal populations: trained (black) and untrained (gray) representations in V1 (A and C) and V2 (B and D). For cells whose orientation responses were well-described by wrapped Gaussian descriptive functions, preferred orientation was defined by the center position of the Gaussian. Data from the 2 animals have been combined. Preferred orientations were then grouped into 8 nonoverlapping bins. The horizontal lines indicate an unbiased distribution in which each bin contains of the population. The V1-trained representation has significantly fewer cells at the trained orientation of 45° (filled) than would be expected from an unbiased distribution.

Preferred orientation distributions were also computed using all cells within the trained and untrained regions irrespective of the quality of their orientation fit (not shown). In one analysis, the preferred orientation of cells with well-fit orientation functions was taken from the function maximum, and the preferred orientation of the remaining cells was taken as the orientation that evoked the greatest response. In another analysis, the orientation that evoked largest response was used for all cells. For all the statistical analyses, these two methods yielded identical results as the distributions shown in Fig. 4.

Changes in preferred orientation is only one of the possible changes that might result from training. Orientation discrimination training might also affect the response rates of appropriately tuned cells or change the variability of the responses of such cells. Moreover, training effects might be location specific but not orientation specific, or vice versa. To examine these possibilities, all of the parameters of orientation tuning from the fitted cells of the animal-combined populations were examined as a function of preferred orientation and location. Orientation bandwidth, orientation tuning amplitude (peak response minus baseline response), peak response (Fig. 5), and the variance ratio were examined by two types of analyses. First, correlations between the response parameters and preferred orientation and distance from the center of the training stimuli were examined. For the distance correlations, no distance criterion was used to restrict the populations from either the trained or untrained hemispheres (dashed line, Fig. 2). None of these parameters was correlated with distance from the center of the training stimuli. With one exception, none of these parameters were significantly correlated with preferred orientation either (Hotelling, C-association tests). The exception was a significant correlation between tuning amplitude and preferred orientation in the untrained V1 population (C-association, P < 0.01) with cells near the trained orientation having lower tuning amplitudes.

View larger version (43K): [in this window] [in a new window]   Fig. 5. Receptive field parameters related to orientation tuning obtained by descriptive function fits as a function of preferred orientation for the 4 neuronal populations. Parameters from individual neurons are binned according to location and preferred orientation. Black indicates cells from untrained locations; gray indicates cells from trained locations. Filled bars represent cells whose preferred orientation was within 22.5° of the trained orientation; unfilled bars represent cells with other preferred orientations. For firing rates (C-F) means and variances were computed on log-transformed data. Vertical lines indicate +1 SE for 22.5° width bins. Neither orientation bandwidth (A and B), nor peak response (E and F), nor the variance ratio (G and H) showed any significant variations with either preferred orientation or location in either V1 or V2. However, there was a significant correlation between tuning amplitude and preferred orientation in the untrained V1 population (C-association, P < 0.01) with cells near the trained orientation having lower tuning amplitudes.

The aforementioned correlation and regression analyses test for relationships between a variety of response properties and the two specific response properties of the training stimuli: orientation and retinotopic location. However, even in the absence of a general relationship between response properties, it is possible that there are differences between neurons that had properties matched to the training stimuli (trained cells) and those that did not (untrained cells). To test for such differences, ANOVA was performed on cells grouped according to their preferred orientation and receptive field location (Fig. 6). Neurons whose preferred orientation was within 22.5° of 45° were classified as belonging to the trained orientation group; while neurons whose receptive field centers were within 0.75° of the training stimuli were classified as belonging to the trained location group. There were no significant effects of location or preferred orientation on orientation bandwidth or peak response in any neuronal population. Tuning amplitude and variance did depend on location, but not orientation, in V1. Tuning amplitude was slightly smaller in the trained population (14.6 spikes/s vs. 19.5 spikes/s), while the difference in variance was more substantial (1.85 vs. 2.36). By contrast, in V2, no orientation-related parameter showed significant dependence on either location or orientation.

View larger version (23K): [in this window] [in a new window]   Fig. 6. Receptive field parameters related to orientation tuning grouped according to location and preferred orientation. Color code is the same as Fig. 5. For V1, 139 cells were classified as belonging to the trained location and 180 to the untrained location; for V2, 129 were in the trained location and 170 in the untrained location. For V1, 36 cells had preferred orientations matching the trained orientation, and 283 had unmatched preferred orientations; for V2, 34 were matched, and 265 were unmatched. Consistent with the correlation analyses, most parameters did not depend on orientation or location.

Training might have also produced changes in response properties unrelated to orientation. For example, because our training stimuli were of two specific spatial frequencies, the distribution of preferred spatial frequency might be altered for those cells whose preferred orientation was near that of the training stimuli. To examine this possibility, preferred spatial frequency (Fig. 7, A and B) and spatial frequency bandwidth (Fig. 7, C and D), preferred size (Fig. 7, E and F), and distance from the training stimuli center (Fig. 7, G and H) were examined as a function of preferred orientation. For preferred size, analyses were done on optimal  (not shown), as well as optimal  normalized by eccentricity. No significant correlations between the spatial frequency and size parameters and either preferred orientation or distance from the training stimulus were seen. Furthermore, there were no correlations between preferred orientation and distance from the training stimuli (G and H).

View larger version (40K): [in this window] [in a new window]   Fig. 7. Receptive field parameters not related to orientation tuning as a function of preferred orientation for the 4 neuronal populations. Format is the same as Fig. 5. Neither spatial frequency bandwidth (C and D) nor preferred size (E and F) depend on preferred orientation or location. By definition, the distance from the training center was different between the trained and untrained representations irrespective of preferred orientation (G and H). However, preferred orientation and distance from the training center were independent for each population.

Few differences were found when cells were grouped according to location and orientation (Fig. 8). By definition, distance varied with location group (G and H). ANOVAs revealed that peak spatial frequency also varied with location. For preferred spatial frequency, there was an interaction between orientation and location: preferred spatial frequency was relatively low among trained orientation cells in the trained location group (mean = 2.0 cycles/deg), and relatively high among trained orientation cells in the untrained location group (mean = 3.6 cycles/deg).

View larger version (20K): [in this window] [in a new window]   Fig. 8. Receptive field parameters not related to orientation tuning grouped according to location and preferred orientation. Format is the same as Fig. 6. Only cells whose spatial frequency responses were well fit by descriptive functions are included in A-D. For these panels, 116 V1 and 111 V2 cells were in the trained location, and 163 V1 and 143 V2 cells were in the untrained location. With respect to the trained orientation, 29 V1 cells and 29 V2 cells had matched preferred orientation, and 250 V1 and 225 V2 cells had unmatched preferred orientations. There was a significant effect of location on peak spatial frequency, as well as an interaction between orientation and location in V1 (A). Only cells whose sigma responses were well fit were included in E and F. For these panels, 84 V1 and 95 V2 cells were in the trained location, and 131 V1 and 130 V2 cells were in the untrained location. With respect to the trained orientation, 26 V1 cells and 29 V2 cells had matched preferred orientation, and 189 V1 and 195 V2 cells had unmatched preferred orientations. In G and H, all cells recorded in the trained hemisphere were included irrespective of receptive field position relative to the training stimuli. For these panels, 169 V1 and 153 V2 cells were in the trained location, and 180 V1 and 170 V2 cells were in the untrained location. With respect to the trained orientation, 38 V1 cells and 38 V2 cells had matched preferred orientation, and 311 V1 and 285 V2 cells had unmatched preferred orientations. As dictated by the grouping, there is a significant effect of location. However, receptive field position does not depend on preferred orientation.

To summarize, there were few significant changes in receptive field properties associated with the training orientation or location in either V1 or V2. Correlation analysis was done on eight independent receptive field parameters in the four neuronal populations with respect to distance from the training stimuli and preferred orientation. Of these 64 correlation analyses, only 1 was significant: the correlation between tuning amplitude and preferred orientation in the untrained V1 population. ANOVA for the effects of orientation and location was also done on the eight parameters. In V1, there were location effects on preferred spatial frequency, tuning amplitude, and variance but no effects of orientation alone on any parameter.

The analyses of Figs. 5 and 7 ignore the nonuniform distribution of preferred orientation (Fig. 4) and therefore do not fully characterize the population response to different stimuli. To characterize the combined effects of potential changes in response rates (Fig. 5) and preferred orientation distributions (Fig. 4), we constructed a population response curve for each neuronal population in which the orientation tuning curves from each cell were averaged together (Fig. 9). Such an average takes into account orientation tuning parameters (bandwidth and peak firing rates) as well as the observed distribution of preferred orientation. The population metric therefore indicates the total amount of activity that would be produced by stimuli of different orientations. As expected, none of these population responses show dramatic orientation biases. However, at the trained orientation, the population response was lower in the trained V1 representation than in the untrained V1 representation (Fig. 9A). No significant orientation specific differences were seen in V2 (Fig. 9B) despite biases in the preferred orientation distribution that are similar to those seen in V1 (Fig. 4). Thus the difference in V1 arises from fewer cells with preferred orientations near that of the training stimuli as well the lower tuning response amplitudes of such cells (Fig. 5C).

View larger version (28K): [in this window] [in a new window]   Fig. 9. Average responses in the 4 neuronal populations as a function of orientation. Solid line indicate means; dashed lines, SEs. The combined effect of the paucity of cells whose preferred orientation was near the trained orientation (bold; Fig. 4), and the lower tuning amplitude of such cells (Fig. 5) creates a dip in the population response in the trained V1 representation at the trained location (A). No such dip is visible in V2 (B). A and B: orientation tuning averages based on the peak spatial frequency for each cell. C and D: the expected mean population response to stimuli at the 2 spatial frequencies used in training. The dip at the trained orientation in the V1 trained population is only visible for high spatial frequency stimuli (thick dashed line).

Because these population response curves are based on individual orientation tuning curves obtained at a variety of different spatial frequencies, significant orientation biases might exist among the subset of cells preferentially tuned to the spatial frequencies used in training (1 and 4 cycles/deg). To estimate the orientation population response at these spatial frequencies, we made use of the separability between orientation and spatial frequency (Webster and De Valois 1985), and for each cell constructed a orientation-spatial frequency response surface by multiplying the appropriately normalized tuning curves together for cells whose orientation and spatial frequency responses were well fit by descriptive functions (Fig. 9, C and D). Again, there are no large variances in population response as a function of orientation. Indeed, at a spatial frequency of 1 cycles/deg, there is no significant difference in orientation bias between the trained and untrained V1 populations. However, the orientation bias seen in the mixed spatial frequency average (A) is visible at a spatial frequency of 4 cycles/deg: responses at the trained orientation are lower in the trained population than in the untrained population (C). This indicates that the observed effects on the neuronal response properties would primarily effect the responses to the training stimuli with higher spatial frequencies.

Retinotopy

For both animals, visuotopic mapping was measured in the trained and untrained hemispheres by relating the position of each V1 penetration to the average of observed receptive field locations within that penetration. This method has limited accuracy because electrodes were secured several centimeters above the cortical surface, were not perfectly normal to the cortical surface, and were typically remounted and replaced on a daily basis. In monkey 2, visuotopy in and around the training region was also measured in an acute recording session for both V1 and V2.

Linear magnification factors were computed by dividing the penetration distance by the visuotopic distance for all possible pairs of penetrations. To evaluate the dependence of magnification on eccentricity, regression analysis was applied to the magnification factors as a function of the average eccentricity of the penetration pair (Fig. 10, A and B). For all cases except the V2 data from the second animal (Fig. 10B), there was a significant negative correlation between magnification and eccentricity. Each magnification factor was then normalized according to the magnification factor predicted by the regression equation (Fig. 10, C and D), and these normalized factors were plotted as a function of distance from the center of trained region. Correlation analysis revealed that in none of the acute or chronic recording (not shown) data sets was there a significant non-zero correlation between eccentricity corrected magnification and distance from the training region. Thus our training produced no measurable effect on the visuotopic mapping in either V1 or V2.

View larger version (23K): [in this window] [in a new window]   Fig. 10. Magnification factors in the trained and untrained V1 (A and C) and V2 (B and D) representations. A and B indicate magnification factors as a function of eccentricity; C and D indicate magnification factors normalized according to the regression prediction of the left panel. With the exception of the V2 population (B), all populations showed a significant negative correlation between magnification and eccentricity. However, when the eccentricity effects are compensated for by the normalization procedure, there is no correlation between magnification and distance from the center of the training region (C and D). Thus, other than the expected change in magnification with eccentricity, there were no significant changes in visuotopy as a function of position in visual space in either the trained or untrained representations.

Neurometric performance

Although the slight reduction in the trained V1 population response at the trained orientation appears inconsistent with orientation-specific improvement in performance, it might be the signature of response property changes that support improved performance. An orientation-selective cell is maximally sensitive to changes in orientation not at its preferred orientation (Fig. 11, A and B), but rather at orientations displaced from the peak of the curve (Fig. 11, C and D), where the slope of the orientation response function is the greatest. If a relative excess of neurons preferred orientations offset from the trained orientation, the population response to the trained orientation (Fig. 9) would be reduced. However, the population response shown in Fig. 9 is only a partial description of how neurons contribute to discrimination because it ignores the variance of neuronal responses and their spatial frequency tuning. For example, responses in the trained V1 population were less variable than those of the untrained V1 population (Fig. 5G). This should improve the discriminability of signals from the trained location. Additionally, because the average preferred spatial frequency was lower among V1 cells in the trained orientation and location groups (Fig. 8A), discriminability should be improved by the relatively large responses to the 1 cycle/deg stimuli.

View larger version (17K): [in this window] [in a new window]   Fig. 11. Discrimination and classification decision models applied to individual neuronal responses. In the discrimination model, orientations are evaluated by comparing an observed response (filled circle) to a template response (open circle) at the trained orientation (45°). In the classification model, orientations are evaluated by comparing the likelihood that the observed response is a response to an orientation less than 45° (gray region) to the likelihood that the response is a response to an orientation greater than 45° (black region). For both models, neurons whose peak orientation is at 45° provide poor signals for making an orientation decision. For the discrimination case (A) a small shift in orientation around the peak is associated with a small change in response. For the classification case (B), the observed response is equally likely to have originated from an orientation less than 45° as from an orientation greater than 45°. In both models neurons whose optimal orientation is not 45° can provide better performance. In the discrimination model (C), the small shift between observed and template responses is now associated with a larger change in response. In the classification model (D), the observed response will be associated with an orientation less than 45° (gray region) since no orientation in the black region produces such a response.

A behaviorally relevant description of the neuronal population must incorporate both the mean and variances of the responses of individual neurons to the stimuli used in the behavioral measurements (Table 1). Using such a description, we wish to ask three questions. First, how does behavioral performance compare with the performance of an ideal observer of individual neuronal responses? Second, how does behavioral performance compare with an observer of a population of neurons? Third, can patterns in the behavioral data be used to rule out or implicate specific decision and pooling models? All of these questions depend on invoking specific models of how physiological responses are used to make behavioral decisions. These models must specify the signals that are used for the decision (responses to particular orientations in our case), the method by which signals are compared (decision model), and how signals from multiple neurons are combined (pooling).

The decision model that has been traditionally applied to neuronal response data is a discrimination model. In this model an observed response is assigned to one of two response distributions. The reliability of such an assignment depends on the separation between the two response distributions: for largely overlapping distributions, there is little chance of a correct assignment (Fig. 11A); whereas for widely separated distributions, such assignments should be very accurate (Fig. 11C). In our case, the response distributions to orientations 3° away from 45° are compared to the response distribution of 45° stimuli (Fig. 11A). An alternative to the discrimination model is the classification model, in which an observed response is assigned to an orientation range (Fig. 11, B and D) on the basis of responses over the entire range. For both of these decision models, response means and variances were computed using the fitted descriptive functions for orientation and spatial frequency. To infer responses for arbitrary stimuli, we used the complete orientation-spatial frequency response surface for each cell obtained by multiplying appropriately normalized orientation and spatial frequency descriptive functions under the assumption of separability (Webster and De Valois 1985).

In any of these models, performance improves as the pool size is increased, and degrades with the introduction of noise or correlation between the neurons. To compare different decision and pooling models (see APPENDIX), we computed performance for a variety of pool sizes and estimated by linear interpolation the number of neurons necessary to achieve behavioral levels of performance at the trained orientation in the absence of noise or interneuronal correlations. We used this number as a summary statistic of the suitability of the four neuronal populations and five decision/pooling models to the discrimination task. A neuronal population that achieves a given behavioral performance with a smaller pool size than other populations is better suited to the behavior task. For every model and population, we computed performance on 6° orientation changes around 45°, and around 135°.

Figure 12 shows d' performance as a function of pool size in all four neuronal populations when discrimination-based response pooling is invoked. Solid horizontal lines indicate behavioral performance: 80% correct (d' = 1.2) at the trained orientation (A and C), and 50% correct (chance, d' = 0) at the untrained orientation (B and D). Individual cells (pool size = 1) of both trained (black) and untrained (gray) populations were much worse at discrimination at the trained orientation than the animal subjects. Thus, in contrast to most previous studies, even the best cells that we observed would be unable to provide a basis for the monkeys' behavior. Consistent with the behavioral observations, there is little difference between V1 and V2 at the two locations: signals from the individual neurons of both populations are similarly incapable of supporting discrimination decisions. However, the suitability of the neuronal populations is inconsistent with the behavior: in both V1 and V2 the untrained populations (gray) are capable of providing better performance than the trained populations (black). Finally, for both the trained and untrained populations, V2 surpasses V1 in performance. Thus, of the four neuronal populations, untrained V2 was the best suited for the trained task, while trained V1 was the most ill-suited. Thus the weaker population response of trained V1 is not consistent with an increased ability to discriminate changes in orientation.

View larger version (25K): [in this window] [in a new window]   Fig. 12. Ideal observer performance as a function of neuronal pool size for the 4 neuronal populations with discrimination-based decisions. Circles represent median performance for a pool size; error bars, the top and bottom quartiles of the performance distribution for a given pool size. Orientation differences of 6°, for which performance is around 79% at the trained orientation were used. Solid horizontal lines correspond with the d' associated with 79% (trained orientation, A, B, E, and F) and 50% (untrained orientation C, D, G, and H) performance in a 2-alternative forced choice. In all cases individual neurons are considerably worse than the animals' performance at the trained orientation. Consistent with psychophysical observations, performances are approximately consistent between trained (black) and untrained (gray) representations for both V1 (A) and V2 (B). However, inconsistent with behavioral observations, performance is not orientation dependent: it is similar at an untrained orientation orthogonal to the trained orientation (C vs. A, D vs. B). Thus the predicted performance at the untrained orientation using the pool sizes necessary for performance at the trained orientation far exceeds behavioral observations. Orientation dependency can be introduced by assuming a biased sampling so that decision pools only include the most capable neurons (E-H). With such biased pooling, the performance curves for the trained orientation shift leftward (E vs. A, F vs. B), and performance curves for the untrained orientation shift rightward (G vs. C, H vs. D). A smaller number of neurons is required to explain the behavior at the trained orientation (E vs. A, F vs. B), and predicted performance at the untrained orientation is much closer to the chance levels seen in behavior (G and H).

To test this specific pooling and decision model, we also computed performance as a function of pool size for 6° discriminations around an untrained orientation (Fig. 12B). The pool sizes obtained from Fig. 12A were used to predict performance on this task. Since the animals could not perform such a task, the behavioral d' is zero. The predicted d' is computed by using the pool size necessary to explain performance at the trained orientation. These predicted d's are all much larger than the behaviorally observed value of zero. Despite the behavioral difference between trained and untrained orientations, the performance of these models for all neuronal populations and pool sizes is similar to that seen with the trained orientation. Indeed, in some cases, the pooled ideal observer performances are actually better in the untrained orientation (B) than in the trained orientation (A).

The physiological properties of the observed populations therefore do not reflect the orientation selectivity of the psychophysical observations. However, most cells are ill-suited for discrimination around the trained orientation: the majority of neurons have a d' near zero. Consistent with previous neuronal pooling models (Britten et al. 1992; Prince et al. 2000; Shadlen et al. 1996), we have included both neurons that are well suited for the discrimination by virtue of their tuning properties as well as those that are not. Ideal detector performance can be significantly improved at a particular orientation by introducing a pooling bias, so that only those cells that are most capable are considered. This is equivalent to stating that, although our sampling was unbiased with respect to all cells, the sampling the animal used to arrive at decisions was biased. Such a bias will also have the effect of worsening performance at other orientations. In our case, an "optimized" pool will be one in which only cells whose peak orientation is near the trained orientation are considered: this will increase performance at the trained orientation and decrease performance at the untrained orientation.

We implemented this optimized pool for each neuronal population by shifting each neuron's orientation tuning function while keeping all other parameters (response rate, spatial frequency tuning, and variance) fixed. For each neuron, the peak orientation was displaced from the trained orientation such that the maximum slope of the orientati