Rufin Vogels

Practising orientation identification improves orientation coding in V1 neurons.

The adult brain shows remarkable plasticity, as demonstrated by the improvement in fine sensorial discriminations after intensive practice. The behavioural aspects of such perceptual learning are well documented, especially in the visual system. Specificity for stimulus attributes clearly implicates an early cortical site, where receptive fields retain fine selectivity for these attributes; however, the neuronal correlates of a simple visual discrimination task remained unidentified. Here we report electrophysiological correlates in the primary visual cortex (V1) of monkeys for learning orientation identification. We link the behavioural improvement in this type of learning to an improved neuronal performance of trained compared to naive neurons. Improved long-term neuronal performance resulted from changes in the characteristics of orientation tuning of individual neurons. More particularly, the slope of the orientation tuning curve that was measured at the trained orientation increased only for the subgroup of trained neurons most likely to code the orientation identified by the monkey. No modifications of the tuning curve were observed for orientations for which the monkey had not been trained. Thus training induces a specific and efficient increase in neuronal sensitivity in V1.

Human perceptual learning in identifying the oblique orientation: retinotopy, orientation specificity and monocularity.

1. Human perceptual learning in discrimination of the oblique orientation was studied using psychophysical methods. Subjects were trained daily to improve their ability to identify the orientation of a circular 2.5 deg diameter unidimensional noise field. Dramatic improvements in sensitivity to contour orientation occurred over a period of 15‐20 days. The improved performance persisted for several months. Improvement was more evident between daily sessions than within sessions. This was partly due to fatigue interfering with the learning effect. Moreover, a consolidation period seemed to be required. 2. Improvement was restricted to the position of the stimulus being trained. This position dependency of the learning effect proved very precise. After training at a specific stimulus position, merely displacing the stimulus to an adjacent position caused a marked increase in thresholds. 3. No transfer of the training effect was observed between orientations. Following a shift of 90 deg away from the trained orientation, performance fell, even below the initial level. 4. We observed complete to almost complete transfer between the two eyes. 5. Our results suggest plastic changes at a level of the visual processing stream where input from both eyes has come together, but where generalization for spatial localization and orientation has not yet occurred.

Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm

fMRI-based adaptation paradigms (fMR-A) have been used to infer neuronal stimulus selectivities in humans. Inferring neuronal selectivities from fMR-A, however, requires an understanding of the relationship between the stimulus selectivity of neuronal adaptation and responses. We studied this relationship by recording single cells in macaque inferior temporal (IT) cortex, an area that shows fMRI adaptation. Repetition of identical object images reduced the responsiveness of single IT neurons. Presentation of an image to which the neuron was unresponsive did not alter the response to a subsequent image that activated the neuron. Successive presentation of two different images to which the neuron responded similarly produced adaptation, but less so than the repeated presentation of an image. The neuronal adaptation at the single-cell level showed a greater degree of stimulus selectivity than the responses. This complicates the interpretation of fMR-A paradigms when inferring neuronal selectivity.

Spatial sensitivity of macaque inferior temporal neurons

Recent findings in dorsal visual stream areas and computational work raise the question whether neurons at the end station of the ventral visual stream can code for stimulus position. The authors provide the first detailed, quantitative data on the spatial sensitivity of neurons in the anterior part of the inferior temporal cortex (area TE) in awake, fixating monkeys. They observed a large variation in receptive field (RF) size (ranging from 2.8° to 26°). TE neurons differed in their optimal position, with a bias toward the foveal position. Moreover, the RF profiles of most TE neurons could be fitted well with a two‐dimensional Gaussian function. Most neurons had only one region of high sensitivity and showed a smooth decline in sensitivity toward more distal positions. In addition, the authors investigated some of the possible determinants of such spatial sensitivity. First, testing with low‐pass filtered versions of the stimuli revealed that the general preference for the foveal position and the size of the RFs was not due simply to TE neurons receiving input with a lower spatial resolution at more eccentric positions. The foveal position was still preferred after intense low‐pass filtering. Second, although an increase in stimulus size consistently broadened spatial sensitivity profiles, it did not change the qualitative features of these profiles. Moreover, size selectivity of TE neurons was generally position invariant. Overall, the results suggest that TE neurons can code for the position of stimuli in the central region of the visual field. J. Comp. Neurol. 426:505–518, 2000.

The response variability of striate cortical neurons in the behaving monkey

SummaryIn order to relate single cell performance to behavioral discrimination one needs measurements of the response variance of the units. We recorded from 183 single units of area V1 of monkeys performing an orientation discrimination task. The response variance was found to increase with increasing response strength. This relationship between response variance and response strength was well described by a power function with a power close to one. The response variance was on average 1.9 times the response strength. Despite important differences in preparation, the behaving monkey data are in good agreement with those previously obtained in paralysed and anesthetised animals.

Inferotemporal neurons represent low-dimensional configurations of parameterized shapes

Behavioral studies with parameterized shapes have shown that the similarities among these complex stimuli can be represented using a low number of dimensions. Using psychophysical measurements and single-cell recordings in macaque inferotemporal (IT) cortex, we found an agreement between low-dimensional parametric configurations of shapes and the representation of shape similarity at the behavioral and neuronal level. The shape configurations, computed from both the perceived and neuron-based similarities, revealed a low number of dimensions and contained the same stimulus order as the parametric configurations. However, at a metric level, the behavioral and neural representations deviated consistently from the parametric configurations. These findings suggest an ordinally faithful but metrically biased representation of shape similarity in IT.

Three-dimensional shape coding in inferior temporal cortex.

Neurons in the rostral lower bank of the superior temporal sulcus (TEs), part of the inferior temporal cortex, respond selectively to three-dimensional (3D) shapes. We have investigated how these neurons represent disparity-defined 3D structure. Most neurons were selective for either first-order (disparity gradients) or second-order (disparity curvature) disparities. The latter selectivity proved remarkably vulnerable to disparity discontinuities, such as sharp edges or steps in disparity. The majority of the neurons remained selective for small disparity variations within the stimulus. 3D shape selectivity was preserved when the frontoparallel position or the stimulus size was altered. Thus, in TEs, 3D shape is coded by first- and second-order disparity-selective neurons, which are highly sensitive to spatial variations of disparity.

The effect of practice on the oblique effect in line orientation judgments.

Line orientation discrimination improves with selective practice for oblique orientations and not for principal orientations. This training effect was observed with an identification task as well as with two alternative forced choice tasks. Despite the improvement for oblique orientations, just noticeable differences in orientation are still larger for the practised oblique orientation than for the principal orientations after 5000 practice trials. These findings suggest that the oblique effect in line orientation has at least two sensorial components, one of which is attributed to the meridional variations in the preferred orientation of area 17 S-cells.

Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study

In order to investigate the neural coding of ordinate‐level visual categories, single‐cell recordings were made in the anterior temporal cortex of two rhesus monkeys performing a categorization of colour images of trees versus images of other objects. Neurons showed a high average degree of selectivity for these complex colour images. Although most neurons responded to trees and non‐trees, about a quarter responded in a category‐specific manner, e.g. to trees but not non‐trees, and about one‐tenth responded almost exclusively to exemplars of the trained category. The responses of these neurons were largely invariant for stimulus transformations, e.g. changes in position or size, and decreased with the degree of image scrambling, mimicking the behavioural results. However, the responses of single neurons were insufficiently stimulus invariant to accommodate the entire range of variability present in the features of exemplars within the same category. This strong within‐category selectivity challenges the idea that a prototype is represented at the single neuron level, but suggests that ordinate‐level categorization is based on a population of neurons, each selective for a limited set of exemplars.

Learning to see the difference specifically alters the most informative V4 neurons

Perceptual learning is an instance of adult plasticity whereby training in a sensory (e.g., a visual task) results in neuronal changes leading to an improved ability to perform the task. Yet studies in primary visual cortex have found that changes in neuronal response properties were relatively modest. The present study examines the effects of training in an orientation discrimination task on the response properties of V4 neurons in awake rhesus monkeys. Results indicate that the changes induced in V4 are indeed larger than those in V1. Nonspecific effects of training included a decrease in response variance, and an increase in overall orientation selectivity in V4. The orientation-specific changes involved a local steepening in the orientation tuning curve around the trained orientation that selectively improved orientation discriminability at the trained orientation. Moreover, these changes were largely confined to the population of neurons whose orientation tuning was optimal for signaling small differences in orientation at the trained orientation. Finally, the modifications were restricted to the part of the tuning curve close to the trained orientation. Thus, we conclude that it is the most informative V4 neurons, those most directly involved in the discrimination, that are specifically modified by perceptual learning.