An intact peripheral nerve preparation for monitoring the activity of single, periosteal afferent nerve fibres

doi:10.1016/j.jneumeth.2006.02.019

Journal of Neuroscience Methods

Volume 156, Issues 1–2, 30 September 2006, Pages 140-144

https://doi.org/10.1016/j.jneumeth.2006.02.019 Get rights and content

Abstract

A preparation is described in which it is possible to selectively activate and monitor the activity of the individual periosteal afferent nerve fibres arising from the humerus bone of the cat. The nerve is a fine branch of the median nerve that accompanies the small artery and vein that enter the nutrient foramen of the humerus. By freeing this fine nerve from nearby tissue over a length of ∼1–2 cm and placing it over a silver hook recording electrode, it becomes possible to identify and monitor electrophysiologically, the impulse activity of individual periosteal afferent fibres activated by focal mechanical stimulation of the periosteum. With this preparation it will be possible to examine the central actions and security of transmission at central synaptic targets for single, small-diameter afferent fibres arising from bone.

Introduction

Most studies on the processing of sensory information within the central nervous system (CNS) have been based upon inputs derived from indeterminate numbers of sensory nerve fibres. However, for certain studies of sensory transmission and processing it can be essential to monitor and define the exact number and nature of the recruited afferent fibres. One of the earliest instances of this was achieved in the study by McIntyre et al. (1967) in which they were able to selectively activate, and record from, single Pacinian corpuscle (PC)-related afferent fibres of the intact interosseous nerve in the cat hindlimb. We have used this preparation in a paired-recording paradigm for monitoring single PC fibre activity while recording simultaneously with a microelectrode from the PC fibres’ central target neurons in the dorsal column nuclei (DCN), in quantitative studies of the efficacy of transmission between single PC fibres and their DCN target neurones (Ferrington et al., 1986, Ferrington et al., 1987a, Ferrington et al., 1987b, Rowe, 1990, Rowe, 2002). We have also extended this methodological approach to develop other peripheral nerve preparations that retain continuity with the CNS and permit selective activation and monitoring of the activity of single sensory fibres of other tactile or kinaesthetic classes (e.g. Coleman et al., 1998, Mackie et al., 1995, Mackie and Rowe, 1997). This has now allowed us to quantitatively analyse central synaptic transmission characteristics for these fibre classes, which include slowly adapting type I and II fibres (SAI and SAII fibres), Hair Follicle Afferent fibres (HFA fibres), and kinaesthetic afferent fibres of both joint and muscle origin (Coleman et al., 2003a, Coleman et al., 2003b, Gynther et al., 1995, Rowe, 2002, Rowe et al., 2004, Vickery et al., 1994, Zachariah et al., 2001). Other approaches for examining the central actions of individual afferent fibres have been based on monitoring the activity of fine dorsal root filaments that are left in continuity (e.g. Kirkwood and Sears, 1982, Tracey and Walmsley, 1984), or upon intracellular stimulation of single dorsal root ganglion cells (e.g., Brown et al., 1987, De Koninck and Henry, 1994). However, a major limitation with the latter procedures is that it is not possible to verify the selectivity of single fibre activation when natural stimulation is applied at the periphery.

In the present study we report a further peripheral nerve preparation that represents an important advance, as it permits the selective activation and monitoring of individual sensory fibres of fine diameter that may be nociceptive in function. The peripheral nerve we have identified for this purpose is the fine branch of the median nerve that supplies the humerus bone of the cat forearm. We have already established that this nerve is free of large fibre (Group I or II) components and exhibits a unimodal fibre distribution of Group III fibres (1–7 μm in range of diameters, with a median value of ∼2 μm), with approximately twice that number of unmyelinated (Group IV) fibres (Ivanusic et al., 2006). In the present report, we show that these individual, fine-diameter bone-associated afferent fibres can be selectively activated and monitored with high signal-to-noise ratio from the intact nerve. The preparation therefore should prove ideal for analysing central transmission characteristics for identified, individual fine afferent fibres, free of any concurrent activation of large fibre input to the central nervous system.

Section snippets

Single fibre recording from the intact nerve to the humerus

Experiments, which were approved by the University of New South Wales Animal Care and Ethics Committee (approval number C2/148), were performed in adult cats anaesthetised initially with chloralose (70 mg/kg, i.p.). Full surgical anaesthesia was maintained throughout with supplementary (i.v.) doses of this agent. The medial aspect of the humerus bone was exposed by reflecting the overlying biceps and triceps muscles of the upper arm. This procedure exposed the median nerve and a fine branch of

Nerve supply to the humerus bone

As the path taken by the nerve after separating from the parent median nerve is a perivascular one that does not involve passage through muscle or other nearby tissue, it is free of any contaminating, larger-diameter nerve fibres associated with muscle, tendons or joints (Fig. 1A; and Ivanusic et al., 2006). This was confirmed in the present study by the absence of any responses in electrophysiological recordings from the nerve in association with mechanical probing of muscle and tendons in the

Discussion

Previous electrophysiological studies of the nerve supply to bone have revealed mechanosensitive afferent fibres associated with, for example, the mandible and tibia (Sakada and Aida, 1971, Sakada and Maeda, 1967, Tokunaga, 1967). However, in each case, large diameter fibres from closely associated muscle or interosseous tissues are present in the nerve filaments. Furthermore, it has not been possible at these locations to examine electrophysiologically the periosteal afferents with the nerve

Acknowledgements

This work was supported by the National Health and Medical Research Council of Australia. The technical assistance of C. Riordan and D. Sarno is acknowledged.

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An intact peripheral nerve preparation for monitoring the activity of single, periosteal afferent nerve fibres

Abstract

Introduction

Section snippets

Single fibre recording from the intact nerve to the humerus

Nerve supply to the humerus bone

Discussion

Acknowledgements

Neurosci. Lett.

J. Neurosci. Methods

Behav. Brain Res.

Excitatory actions of single impulses in single hair follicle afferent fibres on spinocervical tract neurones in the cat

J. Physiol. (Lond.)

An intact peripheral nerve preparation for examining the central actions of single kinaesthetic afferent fibres arising in the wrist joint

Prim. Sens. Neuron

Impulse propagation over tactile and kinaesthetic sensory axons to central target neurones of the cuneate nucleus in cat

J. Physiol. (Lond.)

Transmission security for single kinesthetic afferent fibers of joint origin and their target cuneate neurons in the cat

J. Neurosci.

Prolonged GABAA-mediated inhibition following single hair afferent input to single spinal dorsal horn neurones in cats

J. Physiol. (Lond.)

Actions of single sensory fibres on cat dorsal column nuclei neurones: vibratory signalling in a one-to-one linkage

J. Physiol. (Lond.)

Integrative processing of vibratory information in cat dorsal column nuclei neurones driven by identified sensory fibres

J. Physiol. (Lond.)

Response of sensory units with unmyelinated fibres to mechanical, thermal and chemical stimulation of the cat's cornea

J. Physiol. (Lond.)

Transmission characteristics for the 1:1 linkage between slowly adapting type II fibers and their cuneate target neurons in cat

Exp. Brain Res.

Absence of large diameter sensory fibres in a nerve to the cat humerus

J. Anat.

Cold stimulation of teeth: a comparison between the responses of cat intradental A delta and C fibres and human sensation

J. Physiol. (Lond.)

Prolonged GABA_A-mediated inhibition following single hair afferent input to single spinal dorsal horn neurones in cats