Abstract
Tactile nerve fibers fall into a few classes that can be readily distinguished based on their spatiotemporal response properties. Because nerve fibers reflect local skin deformations, they individually carry ambiguous signals about object features. In contrast, cortical neurons exhibit heterogeneous response properties that reflect computations applied to convergent input from multiple classes of afferents, which confer to them a selectivity for behaviorally relevant features of objects. The conventional view is that these complex response properties arise within the cortex itself, implying that sensory signals are not processed to any significant extent in the two intervening structures-the cuneate nucleus (CN) and the thalamus. To test this hypothesis, we recorded the responses evoked in the CN to a battery of stimuli that have been extensively used to characterize tactile coding in both the periphery and cortex, including skin indentations, vibrations, random dot patterns, and scanned edges. We found that CN responses are more similar to their cortical counterparts than they are to their inputs: CN neurons receive input from multiple classes of nerve fibers, they have spatially complex receptive fields, and they exhibit selectivity for object features. Contrary to consensus, then, the CN plays a key role in processing tactile information.
Highlights
The coding of tactile information has been extensively studied in the peripheral nerves and in the primary somatosensory cortex (S1, Brodmann’s area 3b) of nonhuman primates, leading to the conclusion that sensory representations in S1 differ from those at the periphery in at least two important ways
We found that cuneate nucleus (CN) responses more closely resemble those of cortical neurons than they do those of nerve fibers: CN neurons have spatially complex receptive fields reflecting convergent input from multiple classes of nerve fibers and exhibit a selectivity for object features, absent in the nerve
We found that 46% of CN neurons yielded ΔR2 that were more than one SD away from the mean ΔR2 obtained from nerve fibers, whereas only 10% of nerve fibers exceeded this threshold
Summary
The coding of tactile information has been extensively studied in the peripheral nerves and in the primary somatosensory cortex (S1, Brodmann’s area 3b) of nonhuman primates, leading to the conclusion that sensory representations in S1 differ from those at the periphery in at least two important ways. S1 neurons act as temporal filters, as evidenced by the fact that their responses to vibrations reflect both integration and differentiation of their inputs in time [10] These computations give rise to increasingly explicit rate-based representations of object features, such as the orientation of an edge indented into the skin or the texture of a surface scanned across the skin [5, 8]. This precludes a quantitative analysis of how tactile signals are transformed in this structure To fill this gap, we recorded the responses evoked in individual CN neurons to a battery of tactile stimuli that have been extensively used to characterize the response properties of tactile nerve fibers and of neurons in S1, including skin indentations, vibrations, embossed dot patterns, and scanned edges. The picture that emerges is one in which the CN plays an integral part in the transformation of tactile information as it ascends the neuraxis
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