The primate reticulospinal tract, hand function and functional recovery

Abstract

The primate reticulospinal tract is usually considered to control proximal and axial muscles, and to be involved mainly in gross movements such as locomotion, reaching and posture. This contrasts with the corticospinal tract, which is thought to be involved in fine control, particularly of independent finger movements. Recent data provide evidence that the reticulospinal tract can exert some influence over hand movements. Although clearly secondary to the corticospinal tract in healthy function, this could assume considerable importance after corticospinal lesion (such as following stroke), when reticulospinal systems could provide a substrate for some recovery of function. We need to understand more about the abilities of the reticular formation to process sensory input and guide motor output, so that rehabilitation strategies can be optimised to work with the innate capabilities of reticular motor control.

Figure 1. Primate cervical spinal motoneurons receive mono- and disynaptic reticulospinal input

A–D, example motoneuron projecting to forearm flexors that received disynaptic reticulospinal inputs.A, antidromic activation from median nerve above the elbow (overlain single sweeps); there was no activation from the median nerve at the wrist (not shown).BandC, disynaptic reticulospinal excitatory postsynaptic potentials (EPSPs) following a single 300 μA stimulus to the ipsilateral medial longitudinal fasciculus (MLF) (B), and a train of 3 stimuli (C).D, monosynaptic EPSP evoked in this cell following single 300 μA stimulus to the contralateral pyramidal tract (PT). Each panel shows averaged intracellular records (top) with simultaneously recorded epidural volleys below. Vertical dashed lines highlight the segmental latency of the response; EPSPs are shaded. Scale bars inBalso apply toAandC.E–G, example monosynaptic EPSP evoked following reticulospinal activation in a spinal motoneuron projecting to thenar muscles.E, antidromic activation from median nerve at the wrist.FandG, monosynaptic EPSPs following single (F) and train of three (G) stimuli to MLF.H, monosynaptic EPSP after stimulation of contralateral PT.I–L, bar graphs of incidence (left) and mean amplitude (right) of monosynaptic EPSPs from the contralateral PT (PT mono), monosynaptic EPSPs evoked from the ipsilateral MLF (MLF mono) and disynaptic EPSPs from the ipsilateral MLF (MLF di). The numbers above each column in the incidence plots give the raw numbers of motoneurons. Error bars in amplitude plots are SEM. Amplitude of disynaptic EPSPs are measured from the response to the last of a train of 3 or 4 shocks. Each panel illustrates results from motoneurons innervating different categories of muscles. Reproduced from Riddle et al. (2009).

Figure 2. Primate cervical spinal interneurons receive convergent excitatory corticospinal and brainstem input

AandB, single cell example of convergent facilitation. Each panel shows peri-stimulus time histogram (PSTH, left-hand ordinate) with overlain cumulative sum (CUSUM, right-hand ordinate). Stimulus delivery at time zero. Dashed grey line represents mean pre-stimulus baseline activity. PSTH bin width 0.5 ms. Stimulus artifact dead times are replaced by dark grey bars and corresponding regions of the CUSUM are blanked. Significant (P< 0.01, Ztest) changes from baseline are highlighted with filled (facilitation) or open (suppression) bars above the PSTH. Overlain spike waveforms shown in inset, scale bars 1 ms, 2 μV. Responses to:A, single 300 μA PT stimulus;B, single 300 μA stimulus to medial longitudinal fasciculus (MLF).CandD, similar responses in a different cell, also recorded in the intermediate zone of the cervical enlargement.E, pie chart showing the proportion of cells recorded in two monkeys which received convergent input, or input from only one pathway.F, similar display, but constructed only for cells recorded at spinal sites where intraspinal microstimulation (ISMS) yielded low threshold twitches of the digits or wrist.G, constructed only for cells which showed a facilitation of discharge during voluntary reaching movements.H, constructed only for cells with facilitated discharge during voluntary grasping movements. Reproduced from Riddle & Baker (2010).

Figure 3. Lack of effects on primate forearm muscles following stimulation of the ipsilateral pyramidal tract (PT)

A, example averaged intracellular recordings from a forearm flexor motoneuron in which an EPSP is evoked by a single stimulus to contralateral PT (300 μA, n = 36, black trace) but not to ipsilateral PT (300 μA, n = 37, grey trace).B, averaged intracellular recordings from a different forearm flexor motoneuron showing EPSPs evoked by multiple stimuli to contralateral PT (3 stimuli, n = 30) but not to ipsilateral PT (4 stimuli, n = 55). InAandBintracellular recordings are shown above cord dorsum records.C, bar graph showing the types of motoneurons tested with each stimulus (d: intrinsic hand muscles; f: forearm flexors; e: forearm extensors), and maximum number of stimuli used. Bars to the right of the dotted line correspond to contralateral PT (single stimulus). Grey bars indicate oligosynaptic responses, black bars monosynaptic responses, white bars no responses.D, distribution of postsynaptic response amplitudes from PT stimulation; black corresponds to contralateral PT effects, grey bars to the two ipsilateral PT effects seen.E, averages of rectified EMG from muscles ipsilateral or contralateral to the stimulating electrode, following stimulation of the PT at 500 μA. At this intensity, there was no spread to the contralateral pyramid. Arrows mark onset latency of responses in contralateral muscles, and have been duplicated at the same latency on ipsilateral traces for reference. Abbreviations: 1DI, first dorsal interosseous; AbPB, abductor pollicis brevis; EDC, extensor digitorum communis. Scale bars give amplitude of rectified EMG as a percentage of the pre-stimulus baseline level. Reproduced from Soteropoulos et al. (2011).