Multi-finger receptive field properties in primary somatosensory cortex: A revised account of the spatiotemporal integration functions of area 3b.

The leading view in the somatosensory system indicates that area 3b serves as a cortical relay site that primarily encodes (cutaneous) tactile features limited to individual digits. Our recent work argues against this model by showing that area 3b cells can integrate both cutaneous and proprioceptive information from the hand. Here, we further test the validity of this model by studying multi-digit (MD) integration properties in area 3b. In contrast to the prevailing view, we show that most cells in area 3b have a receptive field (RF) that extends to multiple digits, with the size of the RF (i.e., the number of responsive digits) increasing across time. Further, we show that MD cells' orientation angle preference is highly correlated across digits. Taken together, these data show that area 3b plays a larger role in generating neural representations of tactile objects, as opposed to just being a "feature detector" relay site.

Functional consequences of experience-dependent plasticity on tactile perception following perceptual learning.

Continuous training enhances perceptual discrimination and promotes neural changes in areas encoding the experienced stimuli. This type of experience-dependent plasticity has been demonstrated in several sensory and motor systems. Particularly, non-human primates trained to detect consecutive tactile bar indentations across multiple digits showed expanded excitatory receptive fields (RFs) in somatosensory cortex. However, the perceptual implications of these anatomical changes remain undetermined. Here, we trained human participants for 9 days on a tactile task that promoted expansion of multi-digit RFs. Participants were required to detect consecutive indentations of bar stimuli spanning multiple digits. Throughout the training regime we tracked participants' discrimination thresholds on spatial (grating orientation) and temporal tasks on the trained and untrained hands in separate sessions. We hypothesized that training on the multi-digit task would decrease perceptual thresholds on tasks that require stimulus processing across multiple digits, while also increasing thresholds on tasks requiring discrimination on single digits. We observed an increase in orientation thresholds on a single digit. Importantly, this effect was selective for the stimulus orientation and hand used during multi-digit training. We also found that temporal acuity between digits improved across trained digits, suggesting that discriminating the temporal order of multi-digit stimuli can transfer to temporal discrimination of other tactile stimuli. These results suggest that experience-dependent plasticity following perceptual learning improves and interferes with tactile abilities in manners predictive of the task and stimulus features used during training.

Multimodal Interactions between Proprioceptive and Cutaneous Signals in Primary Somatosensory Cortex.

The classical view of somatosensory processing holds that proprioceptive and cutaneous inputs are conveyed to cortex through segregated channels, initially synapsing in modality-specific areas 3a (proprioception) and 3b (cutaneous) of primary somatosensory cortex (SI). These areas relay their signals to areas 1 and 2 where multimodal convergence first emerges. However, proprioceptive and cutaneous maps have traditionally been characterized using unreliable stimulation tools. Here, we employed a mechanical stimulator that reliably positioned animals' hands in different postures and presented tactile stimuli with superb precision. Single-unit recordings in SI revealed that most neurons responded to cutaneous and proprioceptive stimuli, including cells in areas 3a and 3b. Multimodal responses were characterized by linear and nonlinear effects that emerged during early (∼20 ms) and latter (> 100 ms) stages of stimulus processing, respectively. These data are incompatible with the modality specificity model in SI, and provide evidence for distinct mechanisms of multimodal processing in the somatosensory system.

Differential roles of delay-period neural activity in the monkey dorsolateral prefrontal cortex in visual-haptic crossmodal working memory.

Previous studies have shown that neurons of monkey dorsolateral prefrontal cortex (DLPFC) integrate information across modalities and maintain it throughout the delay period of working-memory (WM) tasks. However, the mechanisms of this temporal integration in the DLPFC are still poorly understood. In the present study, to further elucidate the role of the DLPFC in crossmodal WM, we trained monkeys to perform visuo-haptic (VH) crossmodal and haptic-haptic (HH) unimodal WM tasks. The neuronal activity recorded in the DLPFC in the delay period of both tasks indicates that the early-delay differential activity probably is related to the encoding of sample information with different strengths depending on task modality, that the late-delay differential activity reflects the associated (modality-independent) action component of haptic choice in both tasks (that is, the anticipation of the behavioral choice and/or active recall and maintenance of sample information for subsequent action), and that the sustained whole-delay differential activity likely bridges and integrates the sensory and action components. In addition, the VH late-delay differential activity was significantly diminished when the haptic choice was not required. Taken together, the results show that, in addition to the whole-delay differential activity, DLPFC neurons also show early- and late-delay differential activities. These previously unidentified findings indicate that DLPFC is capable of (i) holding the coded sample information (e.g., visual or tactile information) in the early-delay activity, (ii) retrieving the abstract information (orientations) of the sample (whether the sample has been haptic or visual) and holding it in the late-delay activity, and (iii) preparing for behavioral choice acting on that abstract information.

Temporal correlation mechanisms and their role in feature selection: a single-unit study in primate somatosensory cortex.

Studies in vision show that attention enhances the firing rates of cells when it is directed towards their preferred stimulus feature. However, it is unknown whether other sensory systems employ this mechanism to mediate feature selection within their modalities. Moreover, whether feature-based attention modulates the correlated activity of a population is unclear. Indeed, temporal correlation codes such as spike-synchrony and spike-count correlations (r(sc)) are believed to play a role in stimulus selection by increasing the signal and reducing the noise in a population, respectively. Here, we investigate (1) whether feature-based attention biases the correlated activity between neurons when attention is directed towards their common preferred feature, (2) the interplay between spike-synchrony and rsc during feature selection, and (3) whether feature attention effects are common across the visual and tactile systems. Single-unit recordings were made in secondary somatosensory cortex of three non-human primates while animals engaged in tactile feature (orientation and frequency) and visual discrimination tasks. We found that both firing rate and spike-synchrony between neurons with similar feature selectivity were enhanced when attention was directed towards their preferred feature. However, attention effects on spike-synchrony were twice as large as those on firing rate, and had a tighter relationship with behavioral performance. Further, we observed increased r(sc) when attention was directed towards the visual modality (i.e., away from touch). These data suggest that similar feature selection mechanisms are employed in vision and touch, and that temporal correlation codes such as spike-synchrony play a role in mediating feature selection. We posit that feature-based selection operates by implementing multiple mechanisms that reduce the overall noise levels in the neural population and synchronize activity across subpopulations that encode the relevant features of sensory stimuli.

Neural coding of passive lump detection in compliant artificial tissue.

Here, we investigate the neural mechanisms of detecting lumps embedded in artificial compliant tissues. We performed a combined psychophysical study of humans performing a passive lump detection task with a neurophysiological study in nonhuman primates (Macaca mulatta) where we recorded the responses of peripheral mechanoreceptive afferents to lumps embedded at various depths in intermediates (rubbers) of varying compliance. The psychophysical results reveal that human lump detection is greatly degraded by both lump depth and decreased compliance of the intermediate. The neurophysiology results reveal that only the slowly adapting type 1 (SA1) afferents provide a clear spatial representation of lumps at all depths and that the representation is affected by lump size, depth, and compliance of the intermediate. The rapidly adapting afferents are considerably less sensitive to the lump. We defined eight neural response measures that we hypothesized could explain the psychophysical behavior, including peak firing rate, spatial spread of neural activity, and additional parameters derived from these measures. We find that peak firing rate encodes the depth of the lump, and the neural spatial spread of the SA1 response encodes for lump size but not lump shape. We also find that the perception of lump size may be affected by the compliance of the intermediate. The results show that lump detection is based on a spatial population code of the SA1 afferents, which is distorted by the depth of the lump and compliance of the tissue.

Feeling better: separate pathways for targeted enhancement of spatial and temporal touch.

People perceive spatial form and temporal frequency through touch. Although distinct somatosensory neurons represent spatial and temporal information, these neural populations are intermixed throughout the somatosensory system. Here, we show that spatial and temporal touch can be dissociated and separately enhanced via cortical pathways that are normally associated with vision and audition. In Experiments 1 and 2, we found that anodal transcranial direct current stimulation (tDCS) applied over visual cortex, but not auditory cortex, enhances tactile perception of spatial orientation. In Experiments 3 and 4, we found that anodal tDCS over auditory cortex, but not visual cortex, enhances tactile perception of temporal frequency. This double dissociation reveals separate cortical pathways that selectively support spatial and temporal channels. These results bolster the emerging view that sensory areas process multiple modalities and suggest that supramodal domains may be more fundamental to cortical organization.

Representation of tactile curvature in macaque somatosensory area 2.

Tactile shape information is elaborated in a cortical hierarchy spanning primary (SI) and secondary somatosensory cortex (SII). Indeed, SI neurons in areas 3b and 1 encode simple contour features such as small oriented bars and edges, whereas higher order SII neurons represent large curved contour features such as angles and arcs. However, neural coding of these contour features has not been systematically characterized in area 2, the most caudal SI subdivision in the postcentral gyrus. In the present study, we analyzed area 2 neural responses to embossed oriented bars and curved contour fragments to establish whether curvature representations are generated in the postcentral gyrus. We found that many area 2 neurons (26 of 112) exhibit clear curvature tuning, preferring contours pointing in a particular direction. Fewer area 2 neurons (15 of 112) show preferences for oriented bars. Because area 2 response patterns closely resembled SII patterns, we also compared area 2 and SII response time courses to characterize the temporal dynamics of curvature synthesis in the somatosensory system. We found that curvature representations develop and peak concurrently in area 2 and SII. These results reveal that transitions from orientation tuning to curvature selectivity in the somatosensory cortical hierarchy occur within SI rather than between SI and SII.

Second-order receptive fields reveal multidigit interactions in area 3b of the macaque monkey.

Linear receptive field (RF) models of area 3b neurons reveal a three-component structure: a central excitatory region flanked by two inhibitory regions that are spatially and temporally nonoverlapping with the excitation. Previous studies also report that there is an "infield" inhibitory region throughout the neuronal RF, which is a nonlinear interactive (second order) effect whereby stimuli lagging an input to the excitatory region are suppressed. Thus linear models may be inaccurate approximations of the neurons' true RFs. In this study, we characterize the RFs of area 3b neurons, using a second-order quadratic model. Data were collected from 80 neurons of two awake, behaving macaque monkeys while a random dot pattern was scanned simultaneously across the distal pads of digits D2, 3, and 4. We used an iterative method derived from matching pursuit to identify a set of linear and nonlinear terms with significant effects on the neuronal response. For most neurons (65/80), the linear component of the quadratic RF was characterized by a single excitatory region on the dominant digit. Interactions within the dominant digit were characterized by two quadratic filters that capture the spatial aspects of the interactive infield inhibition. Interactions between the dominant (most responsive) digit and its adjacent digit(s) formed the largest class of cross-digit interactions. The results demonstrate that a significant part of area 3b responses is due to nonlinear mechanisms, and furthermore, the data support the notion that area 3b neurons have "nonclassical RF"-like input from adjacent fingers, indicating that area 3b plays a role in integrating shape inputs across digits.

Behavioral choice-related neuronal activity in monkey primary somatosensory cortex in a haptic delay task.

The neuronal activity in the primary somatosensory cortex was collected when monkeys performed a haptic-haptic DMS task. We found that, in trials with correct task performance, a substantial number of cells showed significant differential neural activity only when the monkeys had to make a choice between two different haptic objects. Such a difference in neural activity was significantly reduced in incorrect response trials. However, very few cells showed the choice-only differential neural activity in monkeys who performed a control task that was identical to the haptic-haptic task but did not require the animal to either actively memorize the sample or make a choice between two objects at the end of a trial. From these results, we infer that the differential activity recorded from cells in the primary somatosensory cortex in correct performance reflects the neural process of behavioral choice, and therefore, it is a neural correlate of decision-making when the animal has to make a haptic choice.

Persistent neuronal firing in primary somatosensory cortex in the absence of working memory of trial-specific features of the sample stimuli in a haptic working memory task.

Previous studies suggested that primary somatosensory (SI) neurons in well-trained monkeys participated in the haptic-haptic unimodal delayed matching-to-sample (DMS) task. In this study, 585 SI neurons were recorded in monkeys performing a task that was identical to that in the previous studies but without requiring discrimination and active memorization of specific features of a tactile or visual memorandum. A substantial number of those cells significantly changed their firing rate in the delay compared with the baseline, and some of them showed differential delay activity. These firing changes are similar to those recorded from monkeys engaged in active (working) memory. We conclude that the delay activity is not necessarily only observed as was generally thought in the situation of active memorization of different features between memoranda after those features have been actively discriminated. The delay activity observed in this study appears to be an intrinsic property of SI neurons and suggests that there exists a neural network in SI (the primary sensory cortex) for haptic working memory no matter whether the difference in features of memoranda needs to be memorized in the task or not. Over 400 SI neurons were also recorded in monkeys well-trained to discriminate two memoranda in the haptic-haptic DMS task for comparison of delay firing of SI neurons between the two different working memory tasks used in this study. The similarity observed in those two situations suggests that working memory uses already-existing memory apparatus by activating it temporarily. Our data also suggest that, through training (repetitive exposure to the stimulus), SI neurons may increase their involvement in the working memory of the memorandum.

Perceptual constancy of texture roughness in the tactile system.

Our tactual perception of roughness is independent of the manner in which we touch the surface. A brick surface feels rough no matter how slowly or how rapidly we move our fingers, despite the fluctuating sensory inputs that are transmitted to the finger. Current theories of roughness perception rely solely on inputs from the cutaneous afferents, which are highly affected by scan velocity and force. The question then is: how is roughness constancy achieved? To this end, we characterized the subject's perceived roughness in six scanning conditions. These included two modes of touch: direct touch, where the finger is in contact with the surface, and indirect touch, where the surface is scanned with a hand-held probe; and three scanning modes: active (moving the hand across a stationary surface), passive (moving the surface across a stationary hand), and pseudo-passive (subject's hand is moved by the experimenter across a stationary surface). Here, we show that roughness constancy is preserved during active but not passive scanning, indicating that the hand movement is necessary for roughness constancy in both direct and indirect touch. Roughness constancy is also preserved during pseudo-passive scanning, which stresses the importance of proprioceptive input. The results show that cutaneous input provides the signals necessary for roughness perception and that proprioceptive input resulting from hand movement-rather than a motor efference copy-is necessary to achieve roughness constancy. These findings have important implications in providing realistic sensory feedback for prosthetic-hand users.

Sensory feedback for upper limb prostheses.

In this chapter, we discuss the neurophysiological basis of how to provide sensory feedback to users with an upper limb prosthesis and discuss some of the theoretical issues that need to be considered when directly stimulating neurons in the somatosensory system. We focus on technologies that are currently available and discuss approaches that are most likely to succeed in providing natural perception from the artificial hand to the user. First, we discuss the advantages and disadvantages of providing feedback by stimulating directly the remaining afferents that originally innervated the arm and hand. In particular, we pay close attention to the normal functional roles that the peripheral afferents play in perception. What are the consequences and implications of stimulating these afferents? We then discuss whether it is reasonable to stimulate neurons in the ascending pathways that carry the information from the afferents to the cortex or directly in neurons in the primary somatosensory cortex. We show that for some modalities there are advantages for stimulating in the spinal cord, while for others it is advantageous to stimulate directly in the somatosensory cortex. Finally, we discuss results from a current experiment in which we used electrical stimuli in primary somatosensory cortex to restore the percept of the intensity of a mechanical probe indented into the hand. The results suggest that the simple percept of stimulus intensity can be provided to the animal from a single finger using four electrodes. We propose that significantly more electrodes will be needed to reproduce more complex aspects of tactile perception.

Neural mechanisms of tactile motion integration in somatosensory cortex.

How are local motion signals integrated to form a global motion percept? We investigate the neural mechanisms of tactile motion integration by presenting tactile gratings and plaids to the fingertips of monkeys, using the tactile analogue of a visual monitor and recording the responses evoked in somatosensory cortical neurons. The perceived directions of the gratings and plaids are measured in parallel psychophysical experiments. We identify a population of somatosensory neurons that exhibit integration properties comparable to those induced by analogous visual stimuli in area MT and find that these neural responses account for the perceived direction of the stimuli across all stimulus conditions tested. The preferred direction of the neurons and the perceived direction of the stimuli can be predicted from the weighted average of the directions of the individual stimulus features, highlighting that the somatosensory system implements a vector average mechanism to compute tactile motion direction that bears striking similarities to its visual counterpart.

Shape invariant coding of motion direction in somatosensory cortex.

Invariant representations of stimulus features are thought to play an important role in producing stable percepts of objects. In the present study, we assess the invariance of neural representations of tactile motion direction with respect to other stimulus properties. To this end, we record the responses evoked in individual neurons in somatosensory cortex of primates, including areas 3b, 1, and 2, by three types of motion stimuli, namely scanned bars and dot patterns, and random dot displays, presented to the fingertips of macaque monkeys. We identify a population of neurons in area 1 that is highly sensitive to the direction of stimulus motion and whose motion signals are invariant across stimulus types and conditions. The motion signals conveyed by individual neurons in area 1 can account for the ability of human observers to discriminate the direction of motion of these stimuli, as measured in paired psychophysical experiments. We conclude that area 1 contains a robust representation of motion and discuss similarities in the neural mechanisms of visual and tactile motion processing.

A tactile stimulator for studying passive shape perception.

We describe a computer-controlled tactile stimulator for use in human psychophysical and monkey neurophysiological studies of 3D shape perception. The stimulator is constructed primarily of commercially available parts, as well as a few custom-built pieces for which we will supply diagrams upon request. There are two components to the stimulator: a tactile component and a hand positioner component. The tactile component consists of multiple stimulating units that move about in a Cartesian plane above the restrained hand. Each stimulating unit contains a servo-controlled linear motor with an attached small rotary stepper motor, allowing arbitrary stimulus shapes to contact the skin through vibration, static indentation, or scanning. The hand positioner component modifies the conformation of the restrained hand through a set of mechanical linkages under motorized control. The present design controls the amount of spread between digits 2 and 3, the spread between digits 4 and 3, and the degree to which digit 3 is flexed or extended, thereby simulating different conformations of the hand in contact with objects. This design is easily modified to suit the needs of the experimenter. Because the two components of the stimulator are independently controlled, the stimulator allows for parametric study of the mechanoreceptive and proprioceptive contributions to 3D tactile shape perception.

Analogous intermediate shape coding in vision and touch.

We recognize, understand, and interact with objects through both vision and touch. Conceivably, these two sensory systems encode object shape in similar ways, which could facilitate cross-modal communication. To test this idea, we studied single neurons in macaque monkey intermediate visual (area V4) and somatosensory (area SII) cortex, using matched shape stimuli. We found similar patterns of shape sensitivity characterized by tuning for curvature direction. These parallel tuning patterns imply analogous shape coding mechanisms in intermediate visual and somatosensory cortex.

Convergence of submodality-specific input onto neurons in primary somatosensory cortex.

At the somatosensory periphery, slowly adapting type 1 (SA1) and rapidly adapting (RA) afferents respond very differently to step indentations: SA1 afferents respond throughout the entire stimulus interval (sustained response), whereas RA afferents respond only at stimulus onset (on response) and offset (off response). We recorded the responses of cortical neurons to step indentations and found many neurons in areas 3b and 1 to exhibit properties that are intermediate between these two extremes: These neurons responded during the sustained portion of the stimulus and also at the offset of the stimulus. Several lines of evidence indicate that these neurons, which exist in large proportions even at these early stages of somatosensory cortical processing, receive input from both populations of afferents. First, we show that many cortical neurons have both a significant sustained response and a significant off response. Second, the strength of the off response is uncorrelated with that of the sustained response, which is to be expected if sustained and off responses stem from different populations of afferent fibers. Third, the bulk of the variance in cortical responses to step indentations can be accounted for using a linear combination of both SA1 and RA responses. Finally, we show that the off response in cortical neurons does not reflect rebound from inhibition. We conclude that the convergence of modality specific input onto individual neurons is common in primary somatosensory cortex and discuss how this conclusion might be reconciled with previous findings.

Neural correlates of high-gamma oscillations (60-200 Hz) in macaque local field potentials and their potential implications in electrocorticography.

Recent studies using electrocorticographic (ECoG) recordings in humans have shown that functional activation of cortex is associated with an increase in power in the high-gamma frequency range ( approximately 60-200 Hz). Here we investigate the neural correlates of this high-gamma activity in local field potential (LFP). Single units and LFP were recorded with microelectrodes from the hand region of macaque secondary somatosensory cortex while vibrotactile stimuli of varying intensities were presented to the hand. We found that high-gamma power in the LFP was strongly correlated with the average firing rate recorded by the microelectrodes, both temporally and on a trial-by-trial basis. In comparison, the correlation between firing rate and low-gamma power (40-80 Hz) was much smaller. To explore the potential effects of neuronal firing on ECoG, we developed a model to estimate ECoG power generated by different firing patterns of the underlying cortical population and studied how ECoG power varies with changes in firing rate versus the degree of synchronous firing between neurons in the population. Both an increase in firing rate and neuronal synchrony increased high-gamma power in the simulated ECoG data. However, ECoG high-gamma activity was much more sensitive to increases in neuronal synchrony than firing rate.

Effect of stimulus intensity on the spike-local field potential relationship in the secondary somatosensory cortex.

Neuronal oscillations in the gamma frequency range have been reported in many cortical areas, but the role they play in cortical processing remains unclear. We tested a recently proposed hypothesis that the intensity of sensory input is coded in the timing of action potentials relative to the phase of gamma oscillations, thus converting amplitude information to a temporal code. We recorded spikes and local field potential (LFP) from secondary somatosensory (SII) cortex in awake monkeys while presenting a vibratory stimulus at different amplitudes. We developed a novel technique based on matching pursuit to study the interaction between the highly transient gamma oscillations and spikes with high time-frequency resolution. We found that spikes were weakly coupled to LFP oscillations in the gamma frequency range (40-80 Hz), and strongly coupled to oscillations in higher gamma frequencies. However, the phase relationship of neither low-gamma nor high-gamma oscillations changed with stimulus intensity, even with a 10-fold increase. We conclude that, in SII, gamma oscillations are synchronized with spikes, but their phase does not vary with stimulus intensity. Furthermore, high-gamma oscillations (>60 Hz) appear to be closely linked to the occurrence of action potentials, suggesting that LFP high-gamma power could be a sensitive index of the population firing rate near the microelectrode.