GABAergic/Glutamatergic–Glial/Neuronal Interaction Contributes to Rapid Adaptation in Pacinian Corpuscles

Abstract

Pacinian corpuscles (PCs) are tactile receptors composed of a nerve ending (neurite) that is encapsulated by layers of lamellar cells. PCs are classified as primary mechanoreceptors because there is no synapse between the transductive membrane and the site of actionpotential generation. These touch receptors respond in a rapidly adapting manner to sustained pressure (indentation or displacement), which until now was believed to be attributable solely to the mechanical properties of the capsule. However, evidence of positive immunoreactivity for GABA receptors on the neurite, as well as evidence for gene expression of synaptobrevin in the lamellar cells led to the hypothesis that GABAergic inhibition originating from the lamellar cells is involved in the rapid adaptation process of PCs. Electrophysiological data from isolated PCs demonstrates that, in the presence of either gabazine or picrotoxin (GABA receptor antagonists), many action potentials appear during the static portion of a sustained indentation stimulus (similar to slowly adapting receptors) and that these "static" spikes completely disappear in the presence of GABA. It was consequently hypothesized that glutamate, released by either the neurite itself or the lamellar cells, caused these action potentials. Indeed, the glutamate receptor blocker kynurenate either decreased or totally eliminated the static spikes. Together, these results suggest that GABA, emanating from the modified Schwann cells of the capsule, inhibits glutamatergic excitation during the static portion of sustained pressure, thus forming a "mechanochemical," rather than purely mechanical, rapid adaptation response. This glial-neuronal interaction is a completely novel finding for the PC.

Tissue mechanics govern the rapidly adapting and symmetrical response to touch

“…4 and 5), we can use the model to speculate on the mechanical filter that shapes the response of C. elegans TRNs to time-varying, sinusoidal mechanical loads (i.e., vibration). General considerations on passive viscoelastic materials suggest that the force needed to generate a fixed-amplitude indentation of the cuticle should increase with frequency at high frequencies (9,12,13,19,26,28). In this scenario the amplitude of the resulting indentations would be expected to decrease as their frequency increases.…”

“…This multilayered accessory structure has been proposed to function as a purely mechanical filter (14,17,30) or as a mechanochemical filter embodied in a feedback loop in which GABAergic signals from the lamellar capsule are thought to suppress action potentials during a sustained stimulus (12,13,16,18,20,25,28). But, rapidly adapting MeT currents are found in other mammalian sensory afferents…”

Effects of passive and active movement on vibrotactile detection thresholds of the Pacinian channel and forward masking

“…These subjective sensations refer to the afferent inputs by Meissner corpuscles and Merkel discs, respectively. We specifically focused on the P channel because of its high sensitivity and relatively sharp frequency tuning, which makes it easier to isolate for vibrotactile detection Zwislocki 1984a, 1984b;Bensmaia et al 2005;Gescheider et al 2005;Güçlü et al 2005Güçlü et al , 2006Güçlü and Ö ztek 2007;Pawson et al 2009;Yıldız and Güçlü 2013). By applying forward masking to elevate the thresholds of the P channel, the effects of suprathreshold stimuli can also be studied (Gescheider et al 1995;Güçlü and Bolanowski 2005a;Güçlü and Ö ztek 2007).…”

Evolutionary Specialization of Tactile Perception in Vertebrates

“…Strong evidence suggests that, in the Merkel cellneurite complex, the process relies on a synapselike mechanism (31,34,48,58), but the details are pending investigation. Similarly, a synapse-like communication between the neuron and lamellar cells also has been proposed to explain mechanosensitivity of Pacinian corpuscles (60,61).…”

“…Similarly, lamellar cells in the Pacinian corpuscles (detectors of transient touch and high-frequency vibration) were proposed to influence excitability of the encapsulated afferent, which normally has a rapidly adapting firing pattern (60,61). The multi-component organization of sensory afferent and end-organs provides room for evolutionary changes to fine-tune mechanosensitivity to the species' needs.…”