We recorded the responses of 20 SA1 and 11 RA afferents, and 92, 148, and 37 neurons in areas 3b, 1, and 2, respectively (peripheral afferents were tested only with scanned bars; only a subset of cortical neurons was tested with all stimuli) (see ). shows the responses of a neuron in area 1 to (A) scanned bars, (B) dot patterns and (C) random dot displays varying in coherence. The neuron responded most strongly when stimuli moved medial to lateral relative to the midline with a slight proximal to distal slant (preferred direction
20°). Importantly, its preferred direction was approximately the same across stimulus types, demonstrating that this neuron conveys information about stimulus direction that is invariant with respect to spatial form. Furthermore, the neuron's responses to all the random dot displays were equal when their coherence was 0% (cyan rasters and tuning curve in C) but direction tuning emerged and then sharpened as the motion coherence increased.
Fraction and percentage of neurons whose responses were significantly tuned to each type of stimulus.
To quantify the strength of tuning, we derived a direction selectivity index (DI) (see Materials and Methods
) that increased from 0 to 1 as tuning strength increased. shows the cumulative histogram of DI obtained from the responses of peripheral afferents and neurons in areas 3b, 1, and 2 to scanned bars. Responses of individual SA1 and RA afferents were not tuned for direction as evidenced by the fact that they yielded DIs near zero (; also see Figures S2
). In contrast, tuning for direction is evident at the earliest stage of cortical processing, namely in area 3b, which comprised a large proportion of neurons that were sensitive to the direction of motion of scanned bars. Direction tuning for bars was greater in areas 1 and 2, which contained a much larger proportion of neurons that exhibited strong direction tuning than did area 3b (). Although direction tuning in responses to dot patterns was present in areas 3b and 2, it was stronger for neurons in area 1 (, ) (note that, although the numerical value of DI derived from responses to dot patterns tended to be higher for neurons in area 2 than in area 3b, many of the DIs derived from area 2 responses were not statistically reliable, as shown in ). Finally, neurons in areas 3b and 2 exhibited only weak direction tuning in their responses to random dot displays at 100% coherence (), whereas the responses of a large proportion of area 1 neurons were strongly tuned for direction. Area 2 neurons exhibited particularly weak direction tuning to dot patterns, suggesting that these neurons are sensitive to edges; indeed, a large proportion of area 2 neurons are orientation selective (unpublished data). Despite the fact that area 2 is higher in the somatosensory pathway than area 1, it seems that the latter comprises a more robust representation of direction of motion than does the former.
Direction tuning in primary somatosensory cortex.
Next, we examined the effect of motion coherence on direction tuning in direction-sensitive neurons. We found that the increase in tuning strength was marginal for neurons in area 3b, whereas it was substantial for neurons in area 1 (). The tuning strength of area 2 neurons exhibited an intermediate dependence on motion coherence, and direction tuning for these neurons only emerged at high levels of coherence (>70%).
We then wished to ascertain (1) whether individual neurons conveyed information about direction across stimulus types and (2) whether the direction signal conveyed by those neurons remained unchanged as the stimulus type changed. To this end, we identified a population of neurons that were significantly tuned for bars, dot patterns, and random dot displays. We found that no neurons in area 3b and 8% of the neurons (2 of 25 neurons) in area 2 that were tested with all three types of patterns exhibited significantly direction-tuned responses to all three stimulus types. In contrast, 30% (14 of 42) of the neurons in area 1 exhibited significant direction tuning independent of stimulus type, with a large majority having the same preferred direction for all three stimulus types ().
The direction signal conveyed by these neurons was also largely insensitive to changes in the stimulus amplitude (i.e., the indentation amplitude), or scanning speed over a wide range of behaviorally relevant amplitudes and speeds. The strength of direction tuning was not significantly modulated by stimulus amplitude (; F
>0.6). Furthermore, with few exceptions, the preferred direction was the same across stimulus amplitudes (, 84% of direction selective neurons yielded preferred directions that differed by less than 45° across the two amplitudes, in contrast to afferents; see Figure S3
). Similarly, while strength of tuning increased slightly but significantly with scanning speed across the population (; F
<.01), the strength of direction tuning of individual neurons exhibited a wide variety of relationships with scanning speed (Figure S4
), as did the strength of their responses (unpublished data). Importantly, the preferred direction of individual neurons was consistent across speeds ().
Invariance of direction tuning with respect to amplitude (A,B) and speed (C,D) for bars scanned across the fingertip.
As shown above, a subpopulation of neurons in areas 3b, 1, and 2 conveys significant information about direction of motion for each stimulus type (). Can the responses of these neurons account for our ability to discriminate direction of motion? We derived psychometric functions from clockwise-counterclockwise judgments obtained from human subjects and compared them to analogous “judgments” derived from the responses of individual neurons. Specifically, we used an ideal observer analysis to determine the extent to which stimuli moving in different directions could be discriminated on the basis of the responses these evoked in individual neurons. We found that the responses of the most direction-selective neurons in area 1 could account for psychophysical performance (). (We carried out this analysis using data only from neurons that were significantly direction selective for bars, dot patterns, and random dot displays. No neurons in area 3b and only 8% of neurons in area 2 met our selection criterion; see above.). Indeed, the direction of motion of bars, dot patterns, and random dots could be distinguished on the basis of the responses of a subpopulation of neurons in area 1 with the same accuracy as that observed in human psychophysical experiments (, also see Figure S5
). Furthermore, the sensitivity of the direction signal to motion coherence mirrored that of human subjects (). Our results are therefore consistent with the hypothesis that area 1 comprises a population of neurons whose responses underlie our ability to perceive the direction of tactile motion. However, the neuronal and behavioral data were obtained from different species; this hypothesis could be tested in future experiments by assessing whether electrically stimulating clusters of direction selective neurons systematically affects the animal's performance in a direction discrimination task 
or by ascertaining whether the responses of direction selective neurons are predictive of a monkey's behavior 
Psychometric functions and neurometric functions obtained from the clockwise-counterclockwise discrimination task with (A) bars, (B) dot patterns, and (C) random dot displays (with 100% coherence) delivered to the fingertip.
A hallmark of many visual neurons is that they are sensitive to both direction of motion and stimulus orientation. We ascertained the extent to which neurons exhibited this dual sensitivity by examining their responses to scanned and indented bars. Specifically, we gauged the strength of orientation and of direction tuning in the responses of each neuron in our sample to scanned bars. We found that these neurons spanned the spectrum of tuning properties (). Some neurons (15%) were sensitive to orientation and not direction (); others (36%) were sensitive to direction but not orientation (). A large proportion of neurons (32%), however, were sensitive to both; for example, the neuron shown in responded to a bar oriented perpendicular to the long axis of the finger regardless of whether the bar moved proximal to distal (90°) or distal to proximal (270°), but produced a more robust response in the latter direction than in the former. In area MT, the relative preferred directions and orientations vary widely. However, the preferred direction is often perpendicular to the preferred orientation 
. We tested whether this was the case for area 1 neurons by comparing the preferred orientation, measured from the responses to indented bars, to the preferred direction (measured from the responses to scanned dot patterns). We found that, indeed, neurons that were sensitive to both orientation and direction exhibited a variety of relative orientation and direction preferences, with a tendency for orthogonal preferences ().
Orientation sensitivity and direction sensitivity.
In summary, area 1 comprises a population of neurons that are strongly tuned for stimulus direction and whose tuning is invariant with respect to three major stimulus properties, namely spatial form, speed, or intensity. Furthermore, the responses of these neurons can account for the ability of human observers to discriminate the direction of moving stimuli across a range of conditions. Finally, a large population of neurons is tuned to both stimulus direction and orientation, with the preferred direction predominantly orthogonal to the preferred orientation. These neurons are specialized detectors for moving contours and thus have RF properties that are strongly analogous to those of neurons in primary visual cortex or area MT.
As individual mechanoreceptive afferents are not sensitive to stimulus motion, an explicit representation of motion must emerge at higher processing stages. Computational models have been proposed to describe how the isomorphic representation of the stimulus at the somatosensory periphery is processed to yield information about direction of motion. Direction selectivity has been thought to be conferred by asymmetries in the spatial layout of in-field inhibition (also referred to as replacing or lagging inhibition 
). However, in-field inhibition is stronger in area 3b than it is in area 1 
, while neurons in the former exhibit weaker tuning than neurons in the latter. Rather, we propose that direction tuning first emerges in area 3b, produced in part by in-field inhibition and perhaps by mechanisms such as those observed in early visual motion processing (see e.g. 
). This direction signal is then elaborated in area 1 to yield a more invariant representation of motion direction. Models of the neural mechanisms that produce increasingly invariant motion representations with respect to other stimulus properties at successive processing stages have been developed for the visual system (e.g., 
). The similarity in the visual and somatosensory representations of stimulus motion suggests that similar mechanisms may be involved in developing these representations in the two modalities 
Interestingly, complex processing of motion signals, in some ways analogous to that observed in area MT, occurs in a primary sensory area. Note, however, that area 1 is not strictly a primary somatosensory area 
. Indeed, thalamocortical projections to area 1 are sparser, target layer III rather than layer IV, and comprise finer fibers than do those to areas 3a and 3b 
. Furthermore, neurons in area 1 also receive strong projections from area 3b 
. Indeed, many neurons in area 1 have larger RFs than do neurons in area 3b and are thought to each receive convergent input from multiple 3b neurons 
. They are also less linear in the stimulus displacement profile than are their 3b counterparts 
, which may in part account for the invariance of the representation of motion direction they carry with respect to stimulus parameters such as spatial form and speed. Area 1 also comprises a strong representation of stimulus orientation 
and texture 
, which suggests that it serves other functions and is not a dedicated area for motion processing. The contiguity of form, texture, and motion representations in somatosensory cortex is not surprising given that motion is a hallmark of tactile exploration. Information about motion direction may indeed be necessary to resolve the spatial relationships between stimulus features during scanning