Somatosensory properties of cuneocerebellar neurones in the main cuneate nucleus of the rat

Abstract

Cells in the main cuneate nucleus (MCN) are known to provide a direct projection to the cerebellum, but the precise nature of the information these cells transmit to the cerebellum is unknown. The present study employed anatomical and electrophysiological procedures to determine the location of cuneocerebellar cells in the MCN, and their somatosensory properties in the rat. The location of neurones projecting to the cerebellum was determined with injections of the retrograde tracers, horseradish peroxidase or Fluoro-Gold in vermal and paravermal regions of the cerebellum. Topographically, the majority of retrogradely labelled cells in the MCN were found to lie primarily ventrolateral in the nucleus and rostral to the level of the obex. Single unit recordings from 69 well characterized MCN cells, identified as projection cells by antidromic activation from stimulation of the inferior cerebellar peduncle, were classified according to their responses to cutaneous stimulation and manipulation of joints and muscles. A slight majority of cells (37.7%) responded only to manipulation/stimulation of joints, and 30.4% of cells responded only to cutaneous stimulation. The remaining cells received convergent input from joint and cutaneous receptors. Cutaneous responsive cells all rapidly adapted to maintained stimuli, and had large receptive fields (RFs) that were generally located over the joints. These cells could be activated by passive movements of the forelimb that deformed the RF. They only discharged during movements and were silent during maintained limb positions. Cells responsive to punctate mechanical stimuli applied to the joint capsules, responded to passive movements of the forelimb, but typically only discharged towards the limits of joint movement, and adapted within a few seconds. Once adapted, small perturbations of joint position resulted in vigorous dynamic responses. The results indicate that the neurones in the MCN of the rat which project directly to the cerebellum are localized in the rostral half of the nucleus. They transmit predominantly dynamic information from joint and cutaneous receptors that are likely to be normally activated as a result of limb movements. These cells could signal information about evolving movements or disturbances of forelimb posture or stance.

Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2

“…The dorsal column nuclei are comprised of the gracile, main cuneate, and external cuneate nuclei and are thought to be the functional equivalent of the spinocerebellar tract for the upper limbs (Ekerot and Larson 1972). They carry proprioceptive and cutaneous information mainly from the upper limbs to the cerebellum (Ekerot and Larson 1972;Haring et al 1984;Cerminara et al 2003;Quy et al 2011) and also terminate heavily within the AZ and PZ (Jasmin and Courville 1987;Massopust et al 1985;Berretta et al 1991;Tolbert and Gutting 1997;Quy et al 2011;Akintunde and Eisenman 1994). Experiments performed in rats suggested that the spinocerebellar and dorsal column nuclei pathways, namely the external cuneate projections that provide the largest source of cerebellar afferents from the dorsal column nuclei, terminate into complementary bands in the AZ and PZ (Ji and Hawkes 1994;Alisky and Tolbert 1997;Quy et al 2011).…”

The Dorsal Column Nuclei Complex Neuroanatomy Reveals a Complex Sensorimotor Integration and Distribution Hub

“…In the cat, the DCN-complex inputs are segregated in the cerebellum by their modalities, such that cutaneous and proprioceptive fibres project to superficial and deeper portions of the folia, respectively (Cerminara et al, 2003;Cooke, Larson, Oscarsson, et al, 1971;Ekerot & Larson, 1972;Rinvik & Walberg, 1975). However, proprioceptive and cutaneous inputs from Cu and ECu were found to be overlapping in the cerebellum of raccoons, suggesting that these animals do not have the same discrete modality segregation within folia (Haring & Rowinski, 1982).…”

“…The cerebellum is also the target of ipsilateral Cu projections ( Figure 5) (Cerminara, Makarabhirom, & Rawson, 2003;Cooke, Larson, Oscaesson, et al, 1971;Cooke, Larson, Oscarsson, & Sjölund, 1971;Quy et al, 2011). Cu-cerebellar neurons are found almost exclusively in CuR, with some in the CuM shell (Haring & Rowinski, 1982), and are typically much smaller than thalamic projecting Cu neurons (Cheek, Rustioni, & Trevino, 1975;Mantle-St. John & Tracey, 1987;Rinvik & Walberg, 1975;Somana & Walberg, 1980).…”

“…Cu-cerebellar neurons are found almost exclusively in CuR, with some in the CuM shell (Haring & Rowinski, 1982), and are typically much smaller than thalamic projecting Cu neurons (Cheek, Rustioni, & Trevino, 1975;Mantle-St. John & Tracey, 1987;Rinvik & Walberg, 1975;Somana & Walberg, 1980). These neurons have large RFs and receive inputs from muscle, joint, and cutaneous afferents (Cerminara et al, 2003;Cooke, Larson, Oscaesson, et al, 1971;Cooke, Larson, Oscarsson, et al, 1971;Leiras et al, 2010).…”

Functional Organisation and Connectivity of the Dorsal Column Nuclei Complex Reveals a Sensorimotor Integration and Distribution Hub

“…All four afferent types are classed as Aβ fibres, which are myelinated large diameter fibres with fast conduction velocities (16-100 m/s) (Abraira & Ginty, 2013). Conduction velocities are species-dependent, humans (Knibestöl, 1973), monkeys (Perl, 1968), and cats (Brown & Iggo, 1967;Burgess, Petit, & Warren, 1968) have fibres that reach the upper limits of this range, while rat Aβ fibres can conduct up to ~70 m/s (Handwerker, Kilo, & Reeh, 1991;Leem, Willis, & Chung, 1993;Sanders & Zimmermann, 1986). Slowly-adapting afferents respond best to maintained mechanical skin indentation with a characteristic sustained, slowly decreasing action potential firing rate.…”