Organization of ascending pathways to the forelimb area of the dorsal accessory olive in the cat

Abstract

The purpose of these experiments was to define the topography of cuneate and spinal projections to the forelimb representation in the rostral dorsal accessory olive (rDAO). We were interested in determining whether the spinal and cuneate inputs constitute a homogeneous afferent source, and whether there is evidence that they serve different functional roles. We were also interested in determining whether the somatotopy of rDAO is the result of a point-to-point projection from its afferent sources, or whether the projection suggests a reorganization of afferents at the olive. Single unit recording was used to identify specific regions of rDAO, and the topography of inputs to the identified regions was determined by using wheat germ agglutinin-horseradish peroxidase (WGA-HRP) as a tracer. The results from retrograde tracing were confirmed by using WGA-HRP as an anterograde tracer from input sources. The cuneate and spinal neurons providing input to rDAO constitute two distinct neural populations. One consists of cells in the caudal cuneate nucleus and lamina VI of the rostral two cervical segments, the other consists of cells in the rostral cuneate nucleus. The cells in the caudal cuneate nucleus and the rostral cervical segments are large, multipolar neurons that form a single column of rDAO input cells. The column of cells projects to the contralateral rDAO in a topographic fashion with rostral regions of the column projecting to rostral rDAO, which contains cells that respond to somatosensory stimulation of the contralateral shoulder, trunk, and proximal forelimb. Caudal regions of the column project to caudal rDAO, which contains cells that respond to stimulation of the distal forelimb. Despite this topography, there is a large degree of overlap in the terminations from neighboring regions of the input column, indicating that a major reorganization occurs at the rDAO. The projection from the rostral cuneate nucleus arises from small neurons that project bilaterally to rDAO, and the input from the rostral cuneate nucleus lacks a clear topography. We propose that input from the cell column is responsible for the somatosensory sensitivity of rDAO neurons, whereas input from rostral cuneate is most likely modulatory, probably inhibitory, in nature.

Stimulation within the cuneate nucleus suppresses synaptic activation of climbing fibers

“…Roughly in parallel to the developing reduction of the suppression of the pyramidal tract response over time, also the climbing fiber field response evoked from the skin was reduced (peak reduction 94% ± 6% SD at 152 min) (Figure 7). This is in concert with that there are both excitatory and inhibitory connections from the cuneate to the IO (McCurdy et al, 1992, 1998). In contrast, the direct response evoked by the pyramidal tract was unaffected.…”

“…McCurdy et al (1992, 1998) found two ventral termination sites within the cuneate, one rostral, and one caudal, for the rubral fibers. Interestingly, in our case the suppression was most effective from sites located in the dorsal parts of the cuneate.…”

“…This pathway could be responsible for the inhibition of inferior olivary neuron firing that follows red nucleus stimulation (Weiss et al, 1990; Horn et al, 1998), compatible with the findings that fibers of the RNm terminate within specific regions of the cuneate nucleus and that these parts of the cuneate nucleus projects to the IO. Also pyramidal tract fibers terminate in this part of the cuneate (McCurdy et al, 1992, 1998), meaning that the depression of climbing fiber excitability observed during the initial phase of reaching movements (Horn et al, 1996; Gibson et al, 2002) could potentially involve this pathway. Leicht et al (1973) found that stimulation of the pericruciate area of the cerebral cortex evoked inhibition of peripherally evoked climbing fiber responses at low thresholds and that the same stimulation evoked excitation of the IO at higher thresholds.…”

“…The electrode was then left in a position where the recorded cells showed characteristic responses of cuneate cells (see Figure 2D). Two loci in the cuneate nucleus, one rostro-ventral and one caudo-ventral, have been reported for the termination of the fibers originating in the red nucleus (McCurdy et al, 1992, 1998). Here we focused on stimulation of the caudo-ventral locus.…”

“…However, a possible candidate has been identified: descending fibers from the red nucleus and the cerebral cortex converge in a specific region of the cuneate nucleus in which the neurons have efferent projections to the rDAO (Kuypers and Tuerk, 1964; Holstege and Kuypers, 1982; McCurdy et al, 1992, 1998). The purpose of the present study is to investigate directly if this region of the cuneate nucleus has inhibitory effects on inferior olivary neurons.…”