Role of primate magnocellular red nucleus neurons in controlling hand preshaping during reaching to grasp.

Reaching to grasp is of fundamental importance to primate motor behavior and requires coordinating hand preshaping with limb transport and grasping. We aimed to clarify the role of cerebellar output via the magnocellular red nucleus (RNm) to the control of reaching to grasp. Rubrospinal fibers originating from RNm constitute one pathway by which cerebellar output influences spinal circuitry directly. We recorded discharge from individual forelimb RNm neurons while monkeys performed a reach-to-grasp task and two tasks that were similar to the reach-to-grasp task in trajectory, amplitude, and direction but did not include a grasp. One of these, the device task, elicited reaches while holding a handle, and the other, the free-reach task, elicited reaches that did not require any specific hand use for task performance. The results demonstrate that coordinated whole-limb reaching movements are associated with large discharge modulations of RNm neurons predominantly when hand use is included. Therefore RNm neurons can at best only make a minor contribution to the control of reaching movements that lack hand use. We evaluated relations between the discharge of individual RNm neurons and electromyographic (EMG) activity of forelimb muscles during the reach-to-grasp task by comparing times of peak RNm discharge to times of peak EMG activity. The results are consistent with the view that RNm discharge may contribute to EMG activity of both distal and proximal muscles during reaching to grasp especially digit extensor and limb elevation muscles. Relations between the discharge of individual RNm neurons and movements of the metacarpi-phalangeal (MCP), wrist, elbow, and shoulder joints during individual trials of task performance were quantified by parametric correlation analyses on a subset of neurons studied during the reach-to-grasp and free-reach tasks. The results indicate that MCP extensions were consistently preceded by bursts of RNm discharge, and strong correlations were observed between parameters of discharge and the duration, velocity, and amplitude of corresponding MCP extensions. In contrast, relations between discharge and movements of proximal joints were poorly represented, and RNm discharge was not related to the speed of limb transport. Based on our data and those of others, we hypothesize that cerebellar output via RNm is specialized for controlling hand use and conclude that RNm may contribute to the control of hand preshaping during reaching to grasp by activating muscle synergies that produce the appropriate MCP extension at the appropriate phase of limb transport.

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

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.

Topography of recurrent inhibitory postsynaptic potentials between individual motoneurons in the cat.

1. The amplitude of recurrent inhibitory postsynaptic potentials (RIPSPs) was examined in pairs of lumbosacral motoneurons that were separated by a known distance and were identified by antidromic stimulation of muscle nerves. One motoneuron was stimulated by injecting depolarizing current pulses, and postsynaptic responses were recorded and averaged in the second motoneuron. Input resistance, rheobase, and conduction velocity were determined for many motoneurons. Most motoneurons innervated extensor muscles. 2. RIPSP values as large as -283 microV were recorded, but most were between -10 and -40 microV. RIPSPs from individual motoneurons of a pool are distributed to several heteronymous motor nuclei and have a range of amplitudes comparable with homonymous RIPSPs. 3. A specific spatial distribution of RIPSP amplitudes was found whereby the largest RIPSP amplitudes (> 40 microV) occurred in motoneurons located within +/- 1.4 mm of the stimulated motoneuron. A significant correlation was found between RIPSP amplitude and the distance between motoneurons for all motoneuron pairs. This correlation was also found within individual groups of motoneuron pairs that innervate the lateral gastrocnemius, medial gastrocnemius, anterior-middle biceps femoris, or soleus muscles. 4. The dependency of RIPSP amplitude on the motoneuron species, which is the particular muscle a motoneuron innervates, is less distinct than the dependency of RIPSP amplitude on topography. Pooling all motoneuron species of close motoneuron pairs indicated that RIPSPs measured in homonymous motoneuron pairs were greater in amplitude than RIPSPs measured in heteronymous pairs. In addition, homonymous RIPSPs of anterior middle biceps femoris or lateral gastrocnemius motoneurons were greater than heteronymous RIPSPs of those motoneurons in all heteronymous combinations. However, homonymous and heteronymous RIPSPs were not significantly different when heteronymous pairs were restricted to individual combinations of species. These findings indicate that RIPSP amplitudes within a set of motor nuclei interconnected by recurrent inhibition are dependent in some cases on the species of motoneurons, but this effect is less important than the effect of topography on RIPSP amplitude. 5. These results indicate that recurrent inhibition in motoneuron pools that innervate hindlimb extensor muscles has a strong topographic organization, such that the strongest recurrent inhibition is produced by each motoneuron in a restricted rostrocaudal zone that includes both homonymous and heteronymous motor nuclei. This suggests that recurrent inhibition is organized for the control of several motor nuclei engaged in common motor activity as well as regulation of activity within individual motor pools.

Spatial and temporal features of recurrent facilitation among motoneurons innervating synergistic muscles of the cat.

1. The temporal features and strength of recurrent facilitatory potentials were examined in pairs of lumbosacral motoneurons that were separated by a known distance and were identified by antidromic stimulation of muscle nerves. One motoneuron was stimulated by injecting depolarizing current pulses, and responses were recorded in the second motoneuron. The distance between motoneurons in pairs was also measured to assess the spatial distribution in strength of recurrent facilitation in motor pools. All motoneurons in these pairs innervated muscles that act as hip or ankle extensors. 2. Recurrent facilitatory potentials were found frequently among motoneurons innervating the hindlimb extensor muscles examined. Several categories of recurrent facilitatory responses were identified. One category was composed of facilitation responses that followed an inhibition response. A second category was composed of facilitation responses that were not preceded by a significant inhibition and consisted of a monophasic response. There was a considerable range of latencies in this category. 3. Responses in which recurrent facilitatory potentials were preceded by recurrent inhibitory postsynaptic potentials (RIPSPs) among close motoneuron pairs demonstrated an inverse correlation between the durations of the facilitatory and the inhibitory phases. In addition, the duration of inhibition responses without facilitation was longer on average, than the duration of inhibitory responses that were followed by facilitation. It was suggested that recurrent facilitation may restrict the time course of RIPSPs. 4. In contrast to the topographic distribution of RIPSPs described in the previous report, amplitudes of monophasic facilitations were directly correlated with the distance separating motoneurons in pairs, rather than inversely correlated as was the case for RIPSP amplitudes.(ABSTRACT TRUNCATED AT 250 WORDS)

Spatial overlap of rubrospinal and corticospinal terminals with input to the inferior olive.

Somatosensory responses of cells in the dorsal accessory olive are suppressed following stimulation of the magnocellular red nucleus. Since the magnocellular red nucleus of the cat does not project directly to the dorsal accessory olive, the present experiments were designed to identify indirect pathways that might mediate suppression of olivary responsiveness. Wheat germ agglutinin-horseradish peroxidase was used to compare the location of magnocellular red nucleus terminals with the locations of cells providing input to the rostral dorsal accessory olive. Cells projecting to forelimb rostral dorsal accessory olive can be divided into two main groups: one group comprises a column of large cells located in the ventral caudal cuneate nucleus extending into lamina VI of C1 and C2, and a second group comprises smaller cells located in the ventral rostral cuneate nucleus. Terminations of fibers originating in the magnocellular red nucleus were found to target both groups of cells projecting to the dorsal accessory olive. Therefore, it is possible that the responsiveness of olivary cells is influenced via these terminations. Stimulation of sensorimotor cortex has also been shown to inhibit olivary responsiveness. Terminations from sensorimotor cortex target the same regions of cells that project to the dorsal accessory olive as those of the magnocellular red nucleus, and a similar, perhaps identical, anatomical substrate may serve to modulate olivary sensitivity by the two descending systems.

Recurrent collaterals of motoneurons projecting to distal muscles in the cat hindlimb.

1. Recurrent collaterals of motoneurons innervating muscles that have a role in control of the hindlimb digits were studied with neuroanatomic tracing methods to determine whether these motoneurons have simple recurrent collateral arbors in comparison with those of hip, knee, and ankle muscles. 2. Motoneurons innervating the hindlimb muscles plantaris (Pln), flexor hallucis longus (FHL), or flexor digitorum longus (FDL) were injected with 10% horseradish peroxidase. Recurrent collaterals were reconstructed from serial transverse sections. 3. No recurrent collaterals were observed in a sample of 10 FDL motoneurons. 4. FHL motoneurons had simple recurrent collateral arbors as assessed by number of first-order collaterals, number of collateral swellings, number of end branches, and the highest-order branch of individual collateral trees. Recurrent collateral arbors of Pln motoneurons were more complex than those of FHL motoneurons. Pln and FHL recurrent collateral arbors were less complex than those described for gastrocnemius-soleus, anterior tibial, and posterior biceps motoneurons. 5. These anatomic findings correspond well with electrophysiological results indicating that the recurrent inhibition produced by FHL motoneurons is weak and that FDL motoneurons do not produce recurrent inhibition. In addition, Pln motoneurons are reported to produce stronger recurrent inhibition than FHL motoneurons in many motor pools. 6. Consideration of these results with respect to the mechanical actions and patterns of motor activity observed in FDL, FHL, and Pln suggests that the complexity of recurrent collaterals of a motoneuron pool and the extent of its contribution to recurrent inhibition diminish with its involvement in the individualized control of the digits.

Selective projections from the cat red nucleus to digit motor neurons.

Classical studies of the cat rubrospinal tract describe dense terminations in spinal laminae V-VII and an absence of any significant projection to lamina IX. In contrast, our recent studies, utilizing the anterograde transport of wheat germ agglutinin conjugated with horseradish peroxidase, have demonstrated a consistent and circumscribed area of label in lamina IX at caudal cervical segments. The present study was undertaken to determine the distribution of rubrospinal terminals among motor neurons in lamina IX as well as to identify the likely target muscles of those motor neurons located near rubrospinal terminals. We injected wheat germ agglutinin-horseradish peroxidase into the red nucleus and unconjugated horseradish peroxidase into selected forearm muscles of the same side of the body. The locations of rubrospinal terminals showing anterograde label on one side of the spinal cord could then be compared with the locations of motor neurons showing retrograde label on the opposite side of the cord. The results demonstrated a clear focus of rubrospinal terminals in the lateral and dorsal portions of the ventral horn beginning at C8 and extending through rostral T1. No other segments of the spinal cord showed a focus of rubrospinal terminations in lamina IX. Retrogradely labeled motor neurons from the muscle injections showed that the rubrospinal terminals overlap extensively with motor neuronal pools supplying distal forearm muscles. Several lines of evidence indicate that the terminals are from rubrospinal fibers and are not due to transneuronal transport.

Incentive relativity effects reduced by exogenous insulin.

In two experiments rats shifted from 32% to 4% sucrose consumed less of the 4% than rats maintained on the 4% solution. This negative contrast effect was eliminated if the rats were injected with insulin (5.4 U/kg) on the shift day. This insulin dose reduced blood glucose levels to less than 50% of control levels, but the brief access period to 4% sucrose just before blood sampling reliably increased blood glucose levels. The results were discussed in terms of the effects of deprivation conditions on incentive relativity.