Primary- and Secondary-Like Jaw-Muscle Spindle Afferents Have Characteristic Topographic Distributions

Abstract

Single jaw-muscle spindle afferent axons were characterized physiologically and intracellularly stained to determine whether particular physiological types of spindle afferent show distinctive morphologies. Microelectrodes filled with either horseradish peroxidase (HRP) or biotinamide (Neurobiotin) were advanced into the mesencephalic trigeminal nucleus (Vme) in anesthetized rats. Intracellular recordings then were characterized by their response: to palpation of the jaw muscles; when pressure was applied to the teeth and during passive ramp and hold and sinusoidal jaw movement. Seventy-one afferents were characterized physiologically and injected with HRP; an additional 61 afferents were typed and injected with biotinamide. The response of 43 stained neurons was recorded in the presence of suxamethonium. The major projection areas of these afferents were the: trigeminal motor nucleus (Vmo); region dorsal to Vmo; reticular formation, spinal trigeminal nucleus, superior cerebellar peduncle and Vme. One afferent type was modulated strongly during stretching of the jaw-elevator muscles. Based on their high sensitivity during stretching of the jaw muscles and/or their silencing during the release phase of muscle stretch, these afferents were classified as primary-like spindle afferents. These afferents projected most strongly to Vmo. A second type of afferent was modulated only modestly during stretching of the jaw-elevator muscles. These tonic afferents were classified as secondary-like spindle afferents because of their low dynamic sensitivity during ramp muscle stretch and their continued discharge during the release phase of muscle stretch. Secondary-like afferents projected most strongly to the region dorsal to Vmo. Boutons (n = 3,834) from 11 afferents were studied in detail. Secondary-like afferents had statistically larger boutons within Vmo. In both secondary- and primary-like spindle afferents, only a small number of boutons were associated closely with the somata and proximal dendrites of trigeminal motoneurons. In these cases, however, two to five boutons appeared to contact individual motoneurons, implying multiple monosynaptic inputs to a selective subset of jaw-elevator motoneurons. Some "giant" boutons were present dorsal to Vmo and in Vme. These results demonstrate that dynamically sensitive and nondynamically sensitive jaw-elevator muscle spindle afferents project preferentially to different regions. Primary-like spindle afferents are capable of providing feedback related to the dynamic phases of muscle stretch and project most heavily to Vmo. Secondary-like spindle afferents can transmit a feedback signal associated with muscle length and project most strongly to the supratrigeminal region. Both types of afferent have projections caudal to Vmo that may serve longer latency jaw-muscle stretch reflexes and/or the projection of proprioceptive information to the thalamus and cerebellum.

Ultrastructural anatomy of physiologically identified jaw-muscle spindle afferent terminations onto retrogradely labeled jaw-elevator motoneurons in the rat

“…The wide variety of neuronal morphologies and central projections Luo and co-workers reported for these electrically activated neurons may reflect the nonspecific nature of this methodology. The anatomical and physiological characteristics found in the present study are consistent with those previously reported for mesencephalic trigeminal jaw-muscle spindle afferents identified by stretching of the jaw-elevator muscles (Dessem and Taylor, 1989;Luo et al, 1995a;Dessem et al, 1997). showing an asymmetric axosomatic synapse (dual arrows) between Bou2 and the HRP-labeled soma in A. Bou2 contacts both a somatic spine (Soma-sp) and a putative dendritic spine (Den-sp).…”

“…These neurons also responded with an increased firing when the jaw-elevator muscles were palpated. Afferents with significant dynamic sensitivity characteristic of primary muscle spindle afferents and afferents with little dynamic sensitivity indicative of secondary muscle spindle afferents (Inoue et al, 1981;Donga and Dessem, 1993;Dessem et al, 1997) were both encountered and intracellularly labeled in this study. No attempt was made to separately label these muscle spindle afferent types.…”

“…Combined retrograde and immunohistochemical studies (Turman and Chandler, 1994;Li et al, 1996;Rampon et al, 1996) have shown that the most prominent source of glycinergic input to the trigeminal motor nucleus arises from the supratri-geminal region and the alpha part of the parvocellular reticular formation. Both of these regions also receive strong jaw-muscle spindle afferent input (Dessem et al, 1997).…”

Illusion caused by vibration of muscle spindles reveals an involvement of muscle spindle inputs in regulating isometric contraction of masseter muscles

“…In human, the number of intrafusal fibers included in single muscle spindle of masseter muscles was found to be extremely large, up to 36 (Eriksson et al 1994), which is larger than those of any other muscles. However, the number of synapses made between a single spindle Ia afferent and an ␣-MN innervating masseter muscles is much smaller (rat, Dessem et al 1997;cat, Yabuta et al 1996) than that for limb muscles (cat, Redman and Walmsley 1983a, b). Thus it is likely that in limb muscles the spatial summation of Ia-excitatory postsynaptic potentials (EPSPs) would easily activate ␣-MNs, while in masseter muscles the temporal summation of Ia-EPSPs would be required to activate ␣-MNs, due to the insufficient spatial summation of Ia-EPSPs as reflected in the difficulty for single electrical stimulation to evoke H-reflex in resting masseter muscles (Fujii and Mitani 1973).…”

Physiological, Morphological and Neurochemical Characterization of Neurons Modulated by Movement

“…After you impale a neuron and the penetration is deemed stable, characterize the neuronal response using ramp and hold and sinusoidal jaw movement. 5 Map the receptive field of the neuron by probing the skin around the head and intra oral cavity with a non-conductive probe such as a wooden stick. If relevant to the study, examine the response of the neuron to other functionally relevant stimuli such as muscle contraction and noxious stimuli.…”