High-Frequency Whisker Vibration Is Encoded by Phase-Locked Responses of Neurons in the Rat's Barrel Cortex

Abstract

Rats perform texture discrimination during tactile exploration with their whiskers with high spatial and temporal precision. Although the peripheral mechanoreceptors provide tactile information with exquisite temporal resolution, physiological studies have suggested that this information might be lost at the cortical level. To address this discrepancy, multiunit and single-unit recordings were performed in the barrel cortex of isoflurane-anesthetized rats using continuous sinusoidal vibration of single whiskers at 15-700 Hz. In multiunit recordings, sustained phase-locked responses occurred up to vibration frequencies of 700 Hz, and 1:1 stimulus locking was observed up to 320 Hz. Wide-band responses of multiunits showed frequency encoding between 20 and 320 Hz. The discharge rates were not different for stimuli in the low-and high-frequency ranges, but they were significantly lower for non-phase-locked responses to high-frequency vibration. Response adaptation was present in only 25% of the cases, whereas in the majority of cases, entrainment to the vibratory frequency remained constant or even increased with stimulus duration. Increased entrainment to high-frequency stimulation was accompanied by the emergence of induced activity in the gamma-band range. Analysis of single-unit activity revealed that phase locking to vibratory stimuli was more precise than that observed for the multiunit responses. The results show that whisker vibrations at frequencies above 100 Hz are faithfully encoded by sustained phase-locked responses of cortical neurons under isoflurane anesthesia. It is conceivable that the awake animal makes use of the tactile signals at even much higher frequencies, which can be provided by the peripheral mechanoreceptors during texture discrimination.

Behavioral study of whisker-mediated vibration sensation in rats

“…Whereas the present behavioral results appear to be the logical consequence of the available neurometric functions for sinusoidal stimuli (22,23), our observation that rats cannot discriminate vibrations on the basis of frequency alone disagrees with the predictions from another physiological study (32), which reported that in rats under light fluorothane gas anesthesia, barrel cortex neurons fired in a phase-locked manner in response to whisker vibrations of up to 300 Hz. From this, it was argued that rats could extract vibration frequency from interspike intervals.…”

“…There are two possible explanations for the apparent discrepancy between the physiological results of Ewert et al and the current behavioral results. First, in the behaving rat neuronal firing may not in fact carry the temporal information seen under gaseous anesthetic (32). Second, in behaving rats temporal information may be present in barrel cortex spike trains, but such information is not "read out" or accessed in the construction of the percept.…”

Natural scenes in tactile texture

“…Thus vibrational cues play an important role in both human and rodent texture perception, which strengthens the proposition that similar neural codes might underlie texture perception at the somatosensory periphery of rodents and primates (see also Diamond 2010). Indeed, similar to their primate counterparts, peripheral afferents in the rodent whisker system respond to high-frequency whisker oscillations with precisely timed action potentials (Arabzadeh et al 2005;Jones et al 2004), and part of this temporal structure is preserved in barrel cortex (Ewert et al 2008).…”

Long-term In Vivo Calcium Imaging of Astrocytes Reveals Distinct Cellular Compartment Responses to Sensory Stimulation

“…During this type of pulsatile whisker stimulation neuronal adaptation occurs within the first few pulses and the number of spikes per pulse decreases, particularly at higher frequencies (Khatri et al 2004;Fraser et al 2006;Musall et al 2014). However, neuronal responses remain locked to the pulsatile stimulus (Ewert et al 2008) and are reproducible across many trials (Mayrhofer et al 2015). While we did not observe a decrease in astrocyte responses with increasing whisker stimulation frequencies, neuronal adaptation could explain why the astrocytic response was not directly proportional to the stimulation intensity (10-90 Hz stimulation; Figs.…”