Descending Signals From the Pontomedullary Reticular Formation Are Bilateral, Asymmetric, and Gated During Reaching Movements in the Cat

Abstract

Schepens, Bénédicte and Trevor Drew. Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. J Neurophysiol 96: 2229 -2252, 2006. First published July 12, 2006 doi:10.1152/jn.00342.2006. We examined the contribution of neurons within the pontomedullary reticular formation (PMRF) to the control of reaching movements in the cat. We recorded the activity of 127 reticular neurons, including 56 reticulospinal neurons, during movements of each forelimb; 67/127 of these neurons discharged prior to the onset of activity in the prime flexor muscles during the reach of the ipsilateral limb and form the focus of this report. Most neurons (63/67) showed similar patterns and levels of discharge activity during reaches of either limb, although activity was slightly greater during reach of the ipsilateral limb. In 26/67 cells, the initial change in discharge activity was time-locked to the GO signal during reaches of either limb; we have argued that this early discharge contributes to the anticipatory postural adjustments that precede movement. In 11/26 cells, the initial change in activity was reciprocal for reaches with the left and right limbs, although activity during the movement was nonreciprocal. Spike-triggered averaging produced postspike facilitation or depression (PSD) in 12/50 cells during reaches of the limb ipsilateral to the recording site and in 17/49 cells during reach of the contralateral limb. Some cells produced PSD in ipsilateral extensor muscles before the start of the reach and during reaches made with the contralateral, but not the ipsilateral limb; this suggests the signal must be differentially gated. Overall, the results suggest a strong bilateral, albeit asymmetric, contribution from the PMRF to the control of posture and movement during voluntary movement.

Bilateral Spike-Triggered Average Effects in Arm and Shoulder Muscles from the Monkey Pontomedullary Reticular Formation

“…SpikeTA effects produced by cat PMRF neurons (Schepens and Drew, 2006), however, show four notable differences when compared with those observed in the monkey. First, PMRF neuron SpikeTA effects were more prevalent in the cat (ϳ40%; 21 of 50 for left arm reach trials or 17 of 49 for right arm reach trials) than in the monkey (ϳ5%, 14 of 292).…”

“…This general pattern of output effects would support concurrent flexion of the ipsilateral extremity and extension of the contralateral extremity, a pattern that likely developed in quadrupeds to help coordinate the forelimbs during locomotion or for postural adjustments (Drew and Rossignol, 1984). The same pattern could support reaching from a quadrupedal stance, in which additional weight is born on the extended forelimb as the other forelimb is lifted to reach (Schepens and Drew, 2006). In primates reaching from a seated position, we speculate that the premotor and motor cortices (Keizer and Kuypers, 1989;Matsuyama and Drew, 1997) also recruit PMRF neurons to coordinate postural adjustments between the forelimbs during reaching movements.…”

“…Cat reticulospinal neurons contribute to the control of locomotion and of forelimb reaching movements (Schepens and Drew, 2006). Previous evidence indicates that monkey PMRF neurons also show activity related to preparation and performance of reaching .…”

Neurons in the Pontomedullary Reticular Formation Signal Posture and Movement Both as an Integrated Behavior and Independently

“…Most frequently, as detailed in Schepens and Drew (2006), some cells with a tonic component were classified as tonic during one condition and phasic/tonic during the other (and vice versa). Similarly, in this study we found cells that were classified as bimodal in one condition and either tonic or phasic/tonic in the other (and vice versa).…”

“…Moreover, it is also known that RSNs innervate commissural interneurons that provide an indirect pathway to affect contralateral activity (Jankowska et al 2003;Matsuyama et al 1997Matsuyama et al , 2004Matsuyama et al , 2006. Given this widespread branching pattern, it is not surprising that both microstimulation and spike-triggered averaging (STA) studies show that the PMRF, in both cats (Drew 1991;Drew and Rossignol 1990a,b;Schepens and Drew 2006) and primates Buford 2004, 2006;Davidson et al 2007), may influence flexor and extensor muscles on both sides of the body as well as head movements and neck musculature (Cowie and Robinson 1994;Drew and Rossignol 1990a,b;Isa and Sasaki 1988;Quessy and Freedman 2004). However, during locomotion, the nonspecific pattern of activation of the limb muscles is reorganized (Drew 1991;Drew and Rossignol 1984;Orlovsky 1972;Perreault et al 1994) so that stimulation during ipsilateral swing activates primarily ipsilateral flexor muscles and contralateral extensor muscles.…”