Tactile roughness: neural codes that account for psychophysical magnitude estimates

Connor, Charles E.; Hsiao, SS; Phillips, J. R.; Johnson, K. O.

doi:10.1523/jneurosci.10-12-03823.1990

Cited by 287 publications

(305 citation statements)

References 22 publications

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“…is like an inverted tent (with two supports) with deformation extending 3-4 mm in all directions from each of the dots (Phillips and Johnson, 1981b;Srinivasan, 1989;Connor et al, 1990;Phillips et al, 1992;Blake et al, 1997b). Both SA1 and R A afferents are much more sensitive to the rate of change of deformation than its absolute value (Pubols and Pubols, 1976).…”

Section: Primary Afferent Rf Propertiesmentioning

confidence: 99%

Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey

DiCarlo

Johnson

1999

J. Neurosci.

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This is the second in a series of studies of the neural representation of tactile spatial form in cortical area 3b of the alert monkey. We previously studied the spatial structure of 330 area 3b neuronal receptive fields (RFs) on the fingerpad with random dot patterns scanned at one velocity (40 mm/sec; DiCarlo et al., 1998). Here, we analyze the temporal structure of 84 neuronal RFs by studying their spatial structure at three scanning velocities (20, 40, and 80 mm/sec). As in the previous study, most RFs contained a single, central, excitatory region and one or more surrounding or flanking inhibitory regions. The mean time delay between skin stimulation and its excitatory effect was 15.5 msec. Except for differences in mean rate, each neuron's response and the spatial structure of its RF were essentially unaffected by scanning velocity. This is the expected outcome when excitatory and inhibitory effects are brief and synchronous. However, that interpretation is consistent neither with the reported timing of excitation and inhibition in somatosensory cortex nor with the third study in this series, which investigates the effect of scanning direction and shows that one component of inhibition lags behind excitation. We reconcile these observations by showing that overlapping (in-field) inhibition delayed relative to excitation can produce RF spatial structure that is unaffected by changes in scanning velocity. Regardless of the mechanisms, the velocity invariance of area 3b RF structure is consistent with the velocity invariance of tactile spatial perception (e.g., roughness estimation and form recognition). Key words: receptive field; somatosensory; cortex; area 3b; SI; tactile; velocity; monkey; reverse correlationThe study reported here concerns the temporal and spatial response properties of neurons in area 3b of primary somatosensory cortex. Previous studies of area 3b have shown that each point in a neuron's cutaneous receptive field (RF) may give rise to excitation, inhibition, or both (Mountcastle and Powell, 1959;Laskin and Spencer, 1979; Gardner and Costanzo, 1980b,c;DiCarlo et al., 1998), that there is a delay between the cutaneous stimulus and the response (Mountcastle and Powell, 1959;Laskin and Spencer, 1979;Gardner and Costanzo, 1980a), that the excitatory and inhibitory effects may persist for variable periods (Laskin and Spencer, 1979;Gardner and Costanzo, 1980b), and that the timing of excitation and inhibition arising from a single cutaneous site may be different (Laskin and Spencer, 1979;Gardner and Costanzo, 1980b). Thus, area 3b RFs have temporal, as well as spatial structure. Although the precise relationship between the spatial and temporal parameters of a neuron's response and the RF estimated with a scanned stimulus is complex (see Appendix A), the general effects of temporal delay between the stimulus and response are as follows. Because we do not initially know the delay between the stimulus and each response component, our RF estimation procedure assigns each response component to the...

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Section: Primary Afferent Rf Propertiesmentioning

confidence: 99%

Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey

DiCarlo

Johnson

1999

J. Neurosci.

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“…psychophysics | somatosensory cortex | vibration | whisker | finger A n effective approach to uncover how neuronal activity leads to sensation is to vary stimulation parameters while correlating changes in firing with changes in the percept (1)(2)(3)(4)(5). In the present work, we measured changes in neuronal activity in rat somatosensory ("barrel") cortex induced by variation in vibration parameters and correlated these changes with perceptual reports from human subjects.…”

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confidence: 96%

Correlated physiological and perceptual effects of noise in a tactile stimulus

Lak

Arabzadeh²,

Harris³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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We investigated connections between the physiology of rat barrel cortex neurons and the sensation of vibration in humans. One set of experiments measured neuronal responses in anesthetized rats to trains of whisker deflections, each train characterized either by constant amplitude across all deflections or by variable amplitude ("amplitude noise"). Firing rate and firing synchrony were, on average, boosted by the presence of noise. However, neurons were not uniform in their responses to noise. Barrel cortex neurons have been categorized as regular-spiking units (putative excitatory neurons) and fast-spiking units (putative inhibitory neurons). Among regular-spiking units, amplitude noise caused a higher firing rate and increased cross-neuron synchrony. Among fast-spiking units, noise had the opposite effect: It led to a lower firing rate and decreased cross-neuron synchrony. This finding suggests that amplitude noise affects the interaction between inhibitory and excitatory neurons. From these physiological effects, we expected that noise would lead to an increase in the perceived intensity of a vibration. We tested this notion using psychophysical measurements in humans. As predicted, subjects overestimated the intensity of noisy vibrations. Thus the physiological mechanisms present in barrel cortex also appear to be at work in the human tactile system, where they affect vibration perception.psychophysics | somatosensory cortex | vibration | whisker | finger A n effective approach to uncover how neuronal activity leads to sensation is to vary stimulation parameters while correlating changes in firing with changes in the percept (1-5). In the present work, we measured changes in neuronal activity in rat somatosensory ("barrel") cortex induced by variation in vibration parameters and correlated these changes with perceptual reports from human subjects. The stimuli in the two cases were trains of whisker and skin vibration, respectively.Isolated neurons respond more robustly to unpredictable (noisy) patterns of electrical stimulation than to repeating, periodic patterns (6) or constant inputs (7). Synaptic transmission also can be enhanced by noise (8). In a recent study of the effects of stimulus noise in rat barrel cortex, we found that whisker vibration trains containing temporal noise (irregularity in the sequence of interdeflection intervals) evoked a larger and more synchronous cortical response than did periodic vibration trains (9). In the present work, to verify that response amplification by noise is a general property of the sensory system, we explored another stimulus feature: We compared cortical responses to trains that had constant amplitude vs. trains that had varying amplitude. We then investigated the perceptual impact of noise using psychophysical experiments in humans. We predicted that noise, by enhancing neuronal firing rates and/or firing synchrony in somatosensory cortex, would produce a systematic bias in the perceived intensity of noisy vibrations compared with noise-free vibrations. Resu...

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“…A series of studies by Johnson and colleagues (summarized by Johnson & Hsiao, 1992) has made it clear that perception of such properties (e.g., identification ofraised letters) depends largely on the processing of signals from slowly adapting Type I (SA I) mechanoreceptors; from primary afferents (Phillips, Johansson, & Johnson, 1990) to cortical neurons (Phillips, Johnson, & Hsiao, 1988), this mechanoreceptive system demonstrates a remarkable ability to register and extract information about the spatial arrangement offeatures that are large enough to be individually discerned. Moreover, Connor, Hsiao, Phillips, and Johnson (1990;Connor & Johnson, 1992) have shown explicitly that people use this system to judge the roughness of coarse surfaces and that their judgments reflect computations, apparently made in somatosensory cortex, using spatial algorithms.…”

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confidence: 99%

Evidence for the duplex theory of tactile texture perception

Hollins

Risner

2000

Perception & Psychophysics

376

269

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Three experiments are reported bearing on Katz's hypothesis that tactile texture perception is mediated by vibrational cues in the case of fine textures and by spatial cues in the case of coarse textures. Psychophysical responses when abrasive surfaces moved across the skin were compared with those obtained during static touch, which does not provide vibrational cues. Experiment 1 used two-interval forced-choice procedures to measure discrimination of surfaces. Fine surfaces that were readily discriminated when moved across the skin became indistinguishable in the absence of movement; coarse surfaces, however, were equally discriminable in movingand stationary conditions. This was shown not to result from any inherently greater difficulty of fine-texture discrimination. Experiments 2 and 3 used free magnitude estimation to obtain a more comprehensive picture of the effect of movement on texture (roughness) perception. Without movement, perception was seriously degraded (the psychophysical magnitude function was flattened) for textures with element sizes below 100 llm; above this point, however, the elimination of movement produced an overall decrease in roughness, but not in the slope of the magnitude function. Thus, two components of stimulation (presumably vibrational and spatial) contribute to texture perception, as Katz maintained; mechanisms for responding to the latter appear to be engaged at texture element sizes down to 100llm, a surprisingly small value.In his classic treatise The World of Touch, David Katz (1925 advanced the view that the tactile perception of the texture of surfaces is a complex process, depending on a "spatial sense" for discernment of coarse textures and a "vibration sense" for an appreciation offiner textures. Katz offered a number of ingenious observations to support his theory: For example, he demonstrated that papers can be discriminated by an observer drawing a wooden rod across them but that wrapping the rod in cloth greatly impairs performance (p. 115). These results suggest the use of vibrational cues. Katz's view, referred to here as the duplex theory oftactile texture perception, is succinctly captured in his statement that surfaces touched very lightly could not be clearly perceived, because "the spatial sense ofthe skin could no longer discern the coarse texture of the materials, and the vibrations necessary for the recognition of fine texture were lost as a result of the minimal friction" (p. 138).

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Tactile roughness: neural codes that account for psychophysical magnitude estimates

Cited by 287 publications

References 22 publications

Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey

Velocity Invariance of Receptive Field Structure in Somatosensory Cortical Area 3b of the Alert Monkey

Correlated physiological and perceptual effects of noise in a tactile stimulus

Evidence for the duplex theory of tactile texture perception

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