Signalling of static and dynamic features of muscle spindle input by cuneate neurones in the cat

The present experiments examined the capacity of external cuneate nucleus (ECN) neurones in the anaesthetized cat to respond to static and vibrotactile stretch of forearm extensor muscles. The aim was to compare their signalling capacities with the known properties of main cuneate neurones in order to determine whether there is differential processing of muscle spindle inputs at these parallel relay sites. Static stretch (≤ 2 mm in amplitude) and sinusoidal vibration were applied longitudinally to individual muscle tendons and responses recorded from single ECN neurones. The muscle-related ECN neurones that were sampled displayed a high sensitivity to both static and dynamic components of stretch, including muscle vibration at frequencies of 50-800 Hz, consistent with their dominant input being derived from primary spindle afferent fibres. In response to ramp-and-hold muscle stretch, ECN neurones resembled their main cuneate counterparts in the pattern of their responses and in quantitative response measures. Their coefficients of variation in interspike intervals during steady stretch ranged from ≈0.3 to 0.7, as they do in main cuneate responses, and their stimulus-response relations were graded as a function of stretch magnitude with low variability in responses at a fixed stretch amplitude. In response to muscle vibration, ECN activity was tightly phase locked to the vibration waveform, in particular at frequencies of ≤ 150 Hz, where vector strength measures (R) were high (R≥ 0.8) before declining as a function of frequency, with R values of ≈0.6 at 300 Hz and ≤ 0.4 at 800 Hz. Both the qualitative and quantitative aspects of ECN responsiveness to the vibro-stretch disturbances were indistinguishable from those of the main cuneate neurones. The results demonstrate a high transmission fidelity for muscle signals across the ECN and no evidence for differential synaptic transmission across the parallel main and external cuneate nuclei. Earlier limitations observed in the capacity of cerebellar Purkinje cells to respond to primary spindle inputs must therefore be imposed at synapses within the cerebellum. Inputs arising from a particular class of receptor may be directed to multiple targets within the central nervous system and utilized for a variety of processing tasks at the different sites. In the case of muscle receptors, the inputs are conveyed over segmental pathways at the spinal cord level for the reflex regulation of posture and movement. However, these muscle inputs are also directed over ascending pathways for processing at hierarchically higher levels of the nervous system, including the cerebral cortex, where they contribute to kinaesthetic sensation (McCloskey, 1978), and the cerebellum where they are presumably utilized for the regulation and control of voluntary movements (e.g. Cooke et al. 1971). Muscle inputs from the forelimb project to the cuneate and external cuneate nuclei which form parallel synaptic relays in these ascending pathways to the cerebral cortex and cerebellum, respectively (Cooke et al. 1971). The input to these parallel relay nuclei from muscle spindle afferents is known to contain precise information about both static and dynamic aspects of muscle length changes. Furthermore, the responses, in particular of primary spindle afferent fibres, to controlled forms of muscle vibration reveal their capacity for signalling, with great precision, information about high-frequency, low-amplitude perturbations in muscle length (e.g. Bianconi & Van der Meulen, 1963; Brown et al. 1967; Mackie et al. 1998). However, it is uncertain whether equivalent information is extracted from the muscle afferent inputs by neurones within the main and external cuneate nuclei, arranged as they are, in parallel, for conveying information rostrally, predominantly for the purpose of kinaesthesia in the case of the main cuneate nucleus and for motor control in the case of the external cuneate nucleus. Some of the early studies on neurones of both nuclei left some doubt over their capacities to retain the precision of impulse patterning evident in the responses of their spindle afferent inputs. Neurones of both the cuneate and external cuneate nuclei of the macaque monkey displayed responses to brief trains (2-8 cycles) of muscle vibration that were phase locked at frequencies up to 50-100 Hz, although contributions to these responses from other mechanoreceptors, including Pacinian corpuscles and joint receptors, could not be excluded (Hummelsheim & Wiesendanger, 1985). Both cuneate and external cuneate neurones in the cat were shown by Rosen & Sjolund (1973a) to respond with high discharge rates to muscle vibration but no assessment was made of how precisely the pattern of discharge could reflect the temporal detail in the vibratory stretch disturbance. However, our recent quantitative analysis of cat main cuneate responses to muscle vibration revealed that these neurones signal, with great precision, the temporal features of vibro-stretch perturbations up to frequencies of 400-500 Hz and display an overall bandwidth of vibration sensitivity that extends to ∼800 Hz (Mackie et al. 1998). These attributes enable the cuneate neurones to contribute accurate temporal information for kinaesthetic sensation in circumstances involving dynamic length changes in skeletal muscle. In the present study, in part reported in preliminary abstract form (Mackie et al. 1994), we have examined quantitatively the capacity of external cuneate neurones in the cat to respond to the same forms of static and vibrational stretch of forearm extensor muscles. The aim was to determine whether the information signalled by these neurones to the cerebellum for the purposes of motor control provides evidence for differential processing of muscle spindle inputs at the parallel synaptic relays of the main cuneate and external cuneate nuclei.