Multiplexing stimulus information through rate and temporal codes in primate somatosensory cortex.
ABSTRACT: Our ability to perceive and discriminate textures relies on the transduction and processing of complex, high-frequency vibrations elicited in the fingertip as it is scanned across a surface. How naturalistic vibrations, and by extension texture, are encoded in the responses of neurons in primary somatosensory cortex (S1) is unknown. Combining single unit recordings in awake macaques and perceptual judgments obtained from human subjects, we show that vibratory amplitude is encoded in the strength of the response evoked in S1 neurons. In contrast, the frequency composition of the vibrations, up to 800 Hz, is not encoded in neuronal firing rates, but rather in the phase-locked responses of a subpopulation of neurons. Moreover, analysis of perceptual judgments suggests that spike timing not only conveys stimulus information but also shapes tactile perception. We conclude that information about the amplitude and frequency of natural vibrations is multiplexed at different time scales in S1, and encoded in the rate and temporal patterning of the response, respectively.
Project description:Plants limit the range of insect substrate-borne vibratory communication by their architecture and mechanical properties that change transmitted signal time, amplitude and frequency characteristics. Stinkbugs gain higher signal-to-noise ratio and increase communication distance by emitting narrowband low frequency vibratory signals that are tuned with transmission properties of plants. The objective of the present study was to investigate hitherto overlooked consequences of duetting with mutually overlapped narrowband vibratory signals. The overlapped vibrations of the model stinkbug species Eushistus heros, produced naturally or induced artificially on different plants, have been analysed. They represent female and male strategies to preserve information within a complex masked signal. The brown stinkbugs E. heros communicate with species and gender specific vibratory signals that constitute characteristic duets in the calling, courtship and rivalry phases of mating behaviour. The calling female pulse overlaps the male vibratory response when the latency of the latter is shorter than the duration of the female triggering signal or when the male response does not inhibit the following female pulse. Overlapping of signals induces interference that changes their amplitude pattern to a sequence of regularly repeated pulses in which their duration and the difference between frequencies of overlapped vibrations are related inversely. Interference does not occur in overlapped narrow band female calling pulses and broadband male courtship pulse trains. In a duet with overlapped signals females and males change time parameters and increase the frequency difference between signals by changing the frequency level and frequency modulation pattern of their calls.
Project description:INTRODUCTION: Female spiders are fine-tuned to detect and quickly respond to prey vibrations, presenting a challenge to courting males who must attract a female's attention but not be mistaken for prey. This is likely particularly important at the onset of courtship when a male enters a female's web. In web-dwelling spiders, little is known about how males solve this conundrum, or about their courtship signals. Here we used laser Doppler vibrometry to study the vibrations produced by males and prey (house flies and crickets) on tangle webs of the western black widow Latrodectus hesperus and on sheet webs of the hobo spider Tegenaria agrestis. We recorded the vibrations at the location typically occupied by a hunting female spider. We compared the vibrations produced by males and prey in terms of their waveform, dominant frequency, frequency bandwidth, amplitude and duration. We also played back recorded male and prey vibrations through the webs of female L. hesperus to determine the vibratory parameters that trigger a predatory response in females. RESULTS: We found overlap in waveform between male and prey vibrations in both L. hesperus and T. agrestis. In both species, male vibrations were continuous, of long duration (on average 6.35 s for T. agrestis and 9.31 s for L. hesperus), and lacked complex temporal patterning such as repeated motifs or syllables. Prey vibrations were shorter (1.38 - 2.59 s), sporadic and often percussive. Based on the parameters measured, courtship signals of male L. hesperus differed more markedly from prey cues than did those of T. agrestis. Courtship vibrations of L. hesperus males differed from prey vibrations in terms of dominant frequency, amplitude and duration. Vibrations of T. agrestis males differed from prey in terms of duration only. During a playback experiment, L. hesperus females did not respond aggressively to low-amplitude vibrations irrespective of whether the playback recording was from a prey or a male. CONCLUSIONS: Unlike courtship signals of other spider species, the courtship signals of L. hesperus and T. agrestis males do not have complex temporal patterning. The low-amplitude 'whispers' of L. hesperus males at the onset of courtship are less likely to trigger a predatory response in females than the high-amplitude vibrations of struggling prey.
Project description:The use of distinguishable complex vibrations that have multiple spectral components can improve the transfer of information by vibrotactile interfaces. We investigated the qualitative characteristics of dual-frequency vibrations as the simplest complex vibrations compared to single-frequency vibrations. Two psychophysical experiments were conducted to elucidate the perceptual characteristics of these vibrations by measuring the perceptual distances among single-frequency and dual-frequency vibrations. The perceptual distances of dual-frequency vibrations between their two frequency components along their relative intensity ratio were measured in Experiment I. The estimated perceptual spaces for three frequency conditions showed non-linear perceptual differences between the dual-frequency and single-frequency vibrations. A perceptual space was estimated from the measured perceptual distances among ten dual-frequency compositions and five single-frequency vibrations in Experiment II. The effect of the component frequency and the frequency ratio was revealed in the perceptual space. In a percept of dual-frequency vibration, the lower frequency component showed a dominant effect. Additionally, the perceptual difference among single-frequency and dual-frequency vibrations were increased with a low relative difference between two frequencies of a dual-frequency vibration. These results are expected to provide a fundamental understanding about the perception of complex vibrations to enrich the transfer of information using vibrotactile stimuli.
Project description:The stereociliary bundles of cochlear hair cells convert mechanical vibrations into the electrical signals required for auditory sensation. While the stiffness of the bundles strongly influences mechanotransduction, its influence on the vibratory response of the cochlear partition is unclear. To assess this, we measured cochlear vibrations in mutant mice with reduced bundle stiffness or with a tectorial membrane (TM) that is detached from the sensory epithelium. We found that reducing bundle stiffness decreased the high-frequency extent and sharpened the tuning of vibratory responses obtained postmortem. Detaching the TM further reduced the high-frequency extent of the vibrations but also lowered the partition's resonant frequency. Together, these results demonstrate that the bundle's stiffness and attachment to the TM contribute to passive longitudinal coupling in the cochlea. We conclude that the stereociliary bundles and TM interact to facilitate passive-wave propagation to more apical locations, possibly enhancing active-wave amplification in vivo.
Project description:The brain transforms physical sensory stimuli into meaningful perceptions. In animals making choices about sensory stimuli, neuronal activity in successive cortical stages reflects a progression from sensation to decision. Feedforward and feedback pathways connecting cortical areas are critical for this transformation. However, the computational functions of these pathways are poorly understood because pathway-specific activity has rarely been monitored during a perceptual task. Using cellular-resolution, pathway-specific imaging, we measured neuronal activity across primary (S1) and secondary (S2) somatosensory cortices of mice performing a tactile detection task. S1 encoded the stimulus better than S2, while S2 activity more strongly reflected perceptual choice. S1 neurons projecting to S2 fed forward activity that predicted choice. Activity encoding touch and choice propagated in an S1-S2 loop along feedforward and feedback axons. Our results suggest that sensory inputs converge into a perceptual outcome as feedforward computations are reinforced in a feedback loop.
Project description:Sound is encoded within the auditory portion of the inner ear, the cochlea, after propagating down its length as a traveling wave. For over half a century, vibratory measurements to study cochlear traveling waves have been made using invasive approaches such as laser Doppler vibrometry. Although these studies have provided critical information regarding the nonlinear processes within the living cochlea that increase the amplitude of vibration and sharpen frequency tuning, the data have typically been limited to point measurements of basilar membrane vibration. In addition, opening the cochlea may alter its function and affect the findings. Here we describe volumetric optical coherence tomography vibrometry, a technique that overcomes these limitations by providing depth-resolved displacement measurements at 200 kHz inside a 3D volume of tissue with picometer sensitivity. We studied the mouse cochlea by imaging noninvasively through the surrounding bone to measure sound-induced vibrations of the sensory structures in vivo, and report, to our knowledge, the first measures of tectorial membrane vibration within the unopened cochlea. We found that the tectorial membrane sustains traveling wave propagation. Compared with basilar membrane traveling waves, tectorial membrane traveling waves have larger dynamic ranges, sharper frequency tuning, and apically shifted positions of peak vibration. These findings explain discrepancies between previously published basilar membrane vibration and auditory nerve single unit data. Because the tectorial membrane directly overlies the inner hair cell stereociliary bundles, these data provide the most accurate characterization of the stimulus shaping the afferent auditory response available to date.
Project description:Judgments of whether a sinusoidal probe is higher or lower in frequency than the closest partial ("target") in a multi-partial complex are improved when the target is pulsed on and off. These experiments explored the contribution of reduction in perceptual confusion and recovery from adaptation to this effect. In experiment 1, all partials except the target were replaced by noise to reduce perceptual confusion. Performance was much better than when the background was composed of multiple partials. When the level of the target was reduced to avoid ceiling effects, no effect of pulsing the target occurred. In experiment 2, the target and background partials were irregularly and independently amplitude modulated. This gave a large effect of pulsing the target, suggesting that if recovery from adaptation contributes to the effect, amplitude fluctuations do not prevent this. In experiment 3, the background was composed of multiple steady partials, but the target was irregularly amplitude modulated. This gave better performance than when the target was unmodulated and a moderate effect of pulsing the target. It is argued that when the target and background are steady tones, pulsing the target may result both in reduction of perceptual confusion and recovery from adaptation.
Project description:Sensory judgments improve with practice. Such perceptual learning is often thought to reflect an increase in perceptual sensitivity. However, it may also represent a decrease in response bias, with unpracticed observers acting in part on a priori hunches rather than sensory evidence. To examine whether this is the case, 55 observers practiced making a basic auditory judgment (yes/no amplitude-modulation detection or forced-choice frequency/amplitude discrimination) over multiple days. With all tasks, bias was present initially, but decreased with practice. Notably, this was the case even on supposedly "bias-free," 2-alternative forced-choice, tasks. In those tasks, observers did not favor the same response throughout (stationary bias), but did favor whichever response had been correct on previous trials (nonstationary bias). Means of correcting for bias are described. When applied, these showed that at least 13% of perceptual learning on a forced-choice task was due to reduction in bias. In other situations, changes in bias were shown to obscure the true extent of learning, with changes in estimated sensitivity increasing once bias was corrected for. The possible causes of bias and the implications for our understanding of perceptual learning are discussed.
Project description:Sensory cortical systems often activate in parallel, even when stimulation is experienced through a single sensory modality [1-3]. Co-activations may reflect the interactive coupling between information-linked cortical systems or merely parallel but independent sensory processing. We report causal evidence consistent with the hypothesis that human somatosensory cortex (S1), which co-activates with auditory cortex during the processing of vibrations and textures [4-9], interactively couples to cortical systems that support auditory perception. In a series of behavioral experiments, we used transcranial magnetic stimulation (TMS) to probe interactions between the somatosensory and auditory perceptual systems as we manipulated attention state. Acute TMS over S1 impairs auditory frequency perception when subjects simultaneously attend to auditory and tactile frequency, but not when attention is directed to audition alone. Auditory frequency perception is unaffected by TMS over visual cortex, thus confirming the privileged interactions between the somatosensory and auditory systems in temporal frequency processing [10-13]. Our results provide a key demonstration that selective attention can modulate the functional properties of cortical systems thought to support specific sensory modalities. The gating of crossmodal coupling by selective attention may critically support multisensory interactions and feature-specific perception.
Project description:Perceptual illusions are usually thought to arise from the way sensory signals are encoded by the brain, and indeed are often used to infer the mechanisms of sensory encoding. But perceptual illusions might also result from the way the brain decodes sensory information, reflecting the strategies that optimize performance in particular tasks. In a fine discrimination task, the most accurate information comes from neurons tuned away from the discrimination boundary, and observers seem to use signals from these 'displaced' neurons to optimize their performance. We wondered whether using signals from these neurons might also bias perception. In a fine direction discrimination task using moving random-dot stimuli, we found that observers' perception of the direction of motion is indeed biased away from the boundary. This misperception can be accurately described by a decoding model that preferentially weights signals from neurons whose responses best discriminate those directions. In a coarse discrimination task, to which a different decoding rule applies, the same stimulus is not misperceived, suggesting that the illusion is a direct consequence of the decoding strategy that observers use to make fine perceptual judgments. The subjective experience of motion is therefore not mediated directly by the responses of sensory neurons, but is only developed after the responses of these neurons are decoded.