Foundations of visual form selectivity for neurons in macaque V1 and V2.

We have measured the visually evoked activity of single neurons recorded in areas V1 and V2 of awake, fixating macaque monkeys, and captured their responses with a common computational model. We used a stimulus set composed of "droplets" of localized contrast, band-limited in orientation and spatial frequency; each brief stimulus contained a random superposition of droplets presented in and near the mapped receptive field. We accounted for neuronal responses with a 2-layer linear-nonlinear model, representing each receptive field by a combination of orientation- and scale-selective filters. We fit the data by jointly optimizing the model parameters to enforce sparsity and to prevent overfitting. We visualized and interpreted the fits in terms of an "afferent field" of nonlinearly combined inputs, dispersed in the 4 dimensions of space and spatial frequency. The resulting fits generally give a good account of the responses of neurons in both V1 and V2, capturing an average of 40% of the explainable variance in neuronal firing. Moreover, the resulting models predict neuronal responses to image families outside the test set, such as gratings of different orientations and spatial frequencies. Our results offer a common framework for understanding processing in the early visual cortex, and also demonstrate the ways in which the distributions of neuronal responses in V1 and V2 are similar but not identical.

Sensitivity to naturalistic texture relies primarily on high spatial frequencies.

Natural images contain information at multiple spatial scales. Though we understand how early visual mechanisms split multiscale images into distinct spatial frequency channels, we do not know how the outputs of these channels are processed further by mid-level visual mechanisms. We have recently developed a texture discrimination task that uses synthetic, multi-scale, "naturalistic" textures to isolate these mid-level mechanisms. Here, we use three experimental manipulations (image blur, image rescaling, and eccentric viewing) to show that perceptual sensitivity to naturalistic structure is strongly dependent on features at high object spatial frequencies (measured in cycles/image). As a result, sensitivity depends on a texture acuity limit, a property of the visual system that sets the highest retinal spatial frequency (measured in cycles/degree) at which observers can detect naturalistic features. Analysis of the texture images using a model observer analysis shows that naturalistic image features at high object spatial frequencies carry more task-relevant information than those at low object spatial frequencies. That is, the dependence of sensitivity on high object spatial frequencies is a property of the texture images, rather than a property of the visual system. Accordingly, we find human observers' ability to extract naturalistic information (their efficiency) is similar for all object spatial frequencies. We conclude that the mid-level mechanisms that underlie perceptual sensitivity effectively extract information from all image features below the texture acuity limit, regardless of their retinal and object spatial frequency.

The neural basis of tactile texture perception.

Running our fingers across a textured surface gives rise to two types of skin deformations, each transduced by different tactile nerve fibers. Coarse features produce large-scale skin deformations whose spatial configuration is reflected in the spatial pattern of activation of some tactile fibers. Scanning a finely textured surface elicits vibrations in the skin, which in turn evoked temporally patterned responses in other fibers. These two neural codes-spatial and temporal-drive a spectrum of neural response properties in somatosensory cortex: At one extreme, neurons are sensitive to spatial patterns and encode coarse features; at the other extreme, neurons are sensitive to vibrations and encode fine features. While the texture responses of nerve fibers are dependent on scanning speed, those of cortical neurons are less so, giving rise to a speed invariant texture percept. Neurons in high-level somatosensory cortices combine information about texture with information about task variables.

Texture is encoded in precise temporal spiking patterns in primate somatosensory cortex.

Humans are exquisitely sensitive to the microstructure and material properties of surfaces. In the peripheral nerves, texture information is conveyed via two mechanisms: coarse textural features are encoded in spatial patterns of activation that reflect their spatial layout, and fine features are encoded in highly repeatable, texture-specific temporal spiking patterns evoked as the skin moves across the surface. Here, we examined whether this temporal code is preserved in the responses of neurons in somatosensory cortex. We scanned a diverse set of everyday textures across the fingertip of awake macaques while recording the responses evoked in individual cortical neurons. We found that temporal spiking patterns are highly repeatable across multiple presentations of the same texture, with millisecond precision. As a result, texture identity can be reliably decoded from the temporal patterns themselves, even after information carried in the spike rates is eliminated. However, the combination of rate and timing is more informative than either code in isolation. The temporal precision of the texture response is heterogenous across cortical neurons and depends on the submodality composition of their input and on their location along the somatosensory neuraxis. Furthermore, temporal spiking patterns in cortex dilate and contract with decreases and increases in scanning speed, respectively, and this systematic relationship between speed and patterning may contribute to the observed perceptual invariance to speed. Finally, we find that the quality of a texture percept can be better predicted when these temporal patterns are taken into consideration. We conclude that high-precision spike timing complements rate-based signals to encode texture in somatosensory cortex.

Effect of scanning speed on texture-elicited vibrations.

To sense the texture of a surface, we run our fingers across it, which leads to the elicitation of skin vibrations that depend both on the surface and on exploratory parameters, particularly scanning speed. The transduction and processing of these vibrations mediate the ability to discern fine surface features. The objective of the present study is to characterize the effect of changes in scanning speed on texture-elicited vibrations to better understand how the exploratory movements shape the neuronal representation of texture. To this end, we scanned a variety of textures across the fingertip of human participants at a variety of speeds (10-160 mm s-1) while measuring the resulting vibrations using a laser Doppler vibrometer. First, we found that the intensity of the vibrations-as indexed by root-mean-square velocity-increases with speed but that the skin displacement remains constant. Second, we found that the frequency composition of the vibrations shifts systematically to higher frequencies with increases in scanning speed. Finally, we show that the speed-dependent shift in frequency composition accounts for the speed-dependent change in intensity.

Emergence of an Invariant Representation of Texture in Primate Somatosensory Cortex.

A major function of sensory processing is to achieve neural representations of objects that are stable across changes in context and perspective. Small changes in exploratory behavior can lead to large changes in signals at the sensory periphery, thus resulting in ambiguous neural representations of objects. Overcoming this ambiguity is a hallmark of human object recognition across sensory modalities. Here, we investigate how the perception of tactile texture remains stable across exploratory movements of the hand, including changes in scanning speed, despite the concomitant changes in afferent responses. To this end, we scanned a wide range of everyday textures across the fingertips of rhesus macaques at multiple speeds and recorded the responses evoked in tactile nerve fibers and somatosensory cortical neurons (from Brodmann areas 3b, 1, and 2). We found that individual cortical neurons exhibit a wider range of speed-sensitivities than do nerve fibers. The resulting representations of speed and texture in cortex are more independent than are their counterparts in the nerve and account for speed-invariant perception of texture. We demonstrate that this separation of speed and texture information is a natural consequence of previously described cortical computations.

Feeling fooled: Texture contaminates the neural code for tactile speed.

Motion is an essential component of everyday tactile experience: most manual interactions involve relative movement between the skin and objects. Much of the research on the neural basis of tactile motion perception has focused on how direction is encoded, but less is known about how speed is. Perceived speed has been shown to be dependent on surface texture, but previous studies used only coarse textures, which span a restricted range of tangible spatial scales and provide a limited window into tactile coding. To fill this gap, we measured the ability of human observers to report the speed of natural textures-which span the range of tactile experience and engage all the known mechanisms of texture coding-scanned across the skin. In parallel experiments, we recorded the responses of single units in the nerve and in the somatosensory cortex of primates to the same textures scanned at different speeds. We found that the perception of speed is heavily influenced by texture: some textures are systematically perceived as moving faster than are others, and some textures provide a more informative signal about speed than do others. Similarly, the responses of neurons in the nerve and in cortex are strongly dependent on texture. In the nerve, although all fibers exhibit speed-dependent responses, the responses of Pacinian corpuscle-associated (PC) fibers are most strongly modulated by speed and can best account for human judgments. In cortex, approximately half of the neurons exhibit speed-dependent responses, and this subpopulation receives strong input from PC fibers. However, speed judgments seem to reflect an integration of speed-dependent and speed-independent responses such that the latter help to partially compensate for the strong texture dependence of the former.

High-dimensional representation of texture in somatosensory cortex of primates.

In the somatosensory nerves, the tactile perception of texture is driven by spatial and temporal patterns of activation distributed across three populations of afferents. These disparate streams of information must then be integrated centrally to achieve a unified percept of texture. To investigate the representation of texture in somatosensory cortex, we scanned a wide range of natural textures across the fingertips of rhesus macaques and recorded the responses evoked in Brodmann's areas 3b, 1, and 2. We found that texture identity is reliably encoded in the idiosyncratic responses of populations of cortical neurons, giving rise to a high-dimensional representation of texture. Cortical neurons fall along a continuum in their sensitivity to fine vs. coarse texture, and neurons at the extrema of this continuum seem to receive their major input from different afferent populations. Finally, we show that cortical responses can account for several aspects of texture perception in humans.

The neural code for tactile roughness in the somatosensory nerves.

Roughness is the most salient perceptual dimension of surface texture but has no well-defined physical basis. We seek to determine the neural determinants of tactile roughness in the somatosensory nerves. Specifically, we record the patterns of activation evoked in tactile nerve fibers of anesthetized Rhesus macaques to a large and diverse set of natural textures and assess what aspect of these patterns of activation can account for psychophysical judgments of roughness, obtained from human observers. We show that perceived roughness is determined by the variation in the population response, weighted by fiber type. That is, a surface will feel rough to the extent that the activity varies across nerve fibers and varies across time within nerve fibers. We show that this variation-based neural code can account not only for magnitude estimates of roughness but also for roughness discrimination performance.NEW & NOTEWORTHY Our sense of touch endows us with an exquisite sensitivity to the microstructure of surfaces, the most salient aspect of which is roughness. We analyze the responses evoked in tactile fibers of monkeys by natural textures and compare them to judgments of roughness obtained for the same textures from human observers. We then describe how texture signals from three populations of nerve fibers are integrated to culminate in a percept of roughness.

Spatial and temporal codes mediate the tactile perception of natural textures.

When we run our fingers over the surface of an object, we acquire information about its microgeometry and material properties. Texture information is widely believed to be conveyed in spatial patterns of activation evoked across one of three populations of cutaneous mechanoreceptive afferents that innervate the fingertips. Here, we record the responses evoked in individual cutaneous afferents in Rhesus macaques as we scan a diverse set of natural textures across their fingertips using a custom-made rotating drum stimulator. We show that a spatial mechanism can only account for the processing of coarse textures. Information about most natural textures, however, is conveyed through precise temporal spiking patterns in afferent responses, driven by high-frequency skin vibrations elicited during scanning. Furthermore, these texture-specific spiking patterns predictably dilate or contract in time with changes in scanning speed; the systematic effect of speed on neuronal activity suggests that it can be reversed to achieve perceptual constancy across speeds. The proposed temporal coding mechanism involves converting the fine spatial structure of the surface into a temporal spiking pattern, shaped in part by the mechanical properties of the skin, and ascribes an additional function to vibration-sensitive mechanoreceptive afferents. This temporal mechanism complements the spatial one and greatly extends the range of tangible textures. We show that a combination of spatial and temporal mechanisms, mediated by all three populations of afferents, accounts for perceptual judgments of texture.