Disentangling temporal and rate codes in primate somatosensory cortex

Millisecond-scale temporal spiking patterns encode sensory information in the periphery, but their role in cortex remains controversial. The sense of touch provides a window into temporal coding because tactile neurons often exhibit precise, repeatable, and informative temporal spiking patterns. In somatosensory cortex (S1), for example, responses to skin vibrations exhibit phase-locking that faithfully carries information about vibratory frequency. However, the respective roles of spike timing and rate in frequency coding are confounded because vibratory frequency shapes both the timing and rates of S1 responses. To disentangle the contributions of these two neural features, we measured S1 responses 1) as animals passively received vibratory stimuli across a wide range of frequencies and amplitudes, and 2) as animals performed a frequency discrimination task, in which differences in frequency were accompanied by behaviorally irrelevant variations in amplitude. We then assessed the degree to which the strength and timing of S1 responses could account for the animals’ performance on the task. First, we showed that animals can discriminate frequency, but their performance is biased by amplitude variations. Second, rate-based representations of frequency are susceptible to changes in amplitude, but in ways that are in the opposite direction of the animals’ behavioral biases, calling into question a rate-based neural code for frequency. In contrast, timing-based representations are highly informative about frequency but impervious to changes in amplitude, which is also inconsistent with the animals’ behavior. We account for the animals’ behavior with a model wherein frequency coding relies on a temporal code, but frequency judgments are biased by perceived magnitude. We conclude that information about vibratory frequency is not encoded in the firing rates of S1 neurons but primarily in the temporal patterning on millisecond time scales.