Intracortical connections between motor cortical zones controlling antagonistic muscles in the cat: a combined anatomical and physiological study

Abstract

Experiments were done on nine cats anaesthetized with pentobarbitone to determine whether motor cortical zones controlling antagonistic muscles are synaptically interconnected. Motor cortical zones controlling wrist flexors, or extensors, were identified by microstimulation and intramuscular electromyographic recordings (microstimulation: 11 pulses at 333 pulses/s, current 10-40 microA). The position of each zone of interest was marked by a small ink spot on the surface of the cortex and on a scaled drawing of the cortical surface (cruciate region). Following the identification of wrist flexor and extensor zones the anterograde tracer biocytin was injected into one, or two, wrist extensor zones at three depths (400, 800 and 1500 microm) from the cortical surface. A small injection of horseradish peroxidase (HRP)--producing a dark brown spot of approximately 300-500 microm--was made in layer II-III of one or more wrist flexor zones. Similar HRP injections were made in the deep layers of wrist extensor zones that were not labelled by biocytin. The HRP injections served to mark the position of potential targets of biocytin-labelled fibres. In some experiments the biocytin was injected into a wrist flexor zone and HRP was deposited in one or more wrist extensor zones. Biocytin-labelled fibres (blue) were found throughout the expanse of the forelimb representation zone, as has been previously reported. More specifically, in all animals biocytin-labelled fibres were found in identified cortical zones controlling the same muscle(s) as well as in zones controlling an antagonist(s). Club-like swellings, indicative of synaptic boutons, were observed on these fibres. The density of labelled fibres was greater in the upper cortical layers (II-III), but a large number of terminals were also present in the lower cortical layers (V-VI). We conclude that there exist intracortical circuits linking motor cortical zones controlling antagonistic muscles. Elucidating the nature and function of these circuits is likely to be important for understanding the mode of operation of the motor cortex.

Linear Summation of Cat Motor Cortex Outputs

“…Motor cortical points are known to be interconnected by intrinsic long-range axonal collaterals (Huntley and Jones, 1991;Keller, 1993;Capaday et al, 1998), and neural activity spreads over the range of these connections (Baker et al, 1998;Capaday, 2004). The observation is even more puzzling given the lack of effect of reducing inhibition at a cortical point, a condition in which it should have received the full brunt of inputs from the ICMS-activated cortical point.…”

“…Details on surgical procedures, electrophysiological methods, and homeostatic measures used in the present study can be found in previous reports from this laboratory (Capaday et al, 1998;Schneider et al, 2001Schneider et al, , 2002Capaday and Rasmusson, 2003). Briefly, the animals were anesthetized with an intramuscular injection of ketamine (33 mg/kg) and xylazine (1 mg/kg).…”

“…The evoked limb movements were made against gravity, as would natural movements. Additionally, activation of reflex pathways in the spinal cord likely contributed to the net motor output because, in the ketamine-anesthetized animals, stretch reflexes, flexion reflexes, and reciprocal inhibition between antagonistic muscles are manifest (Capaday et al, 1998;Schneider et al, 2001Schneider et al, , 2002. However, in this preparation, there is no discernible effect of proprioceptive inputs on motor cortex neurons and little if any from cutaneous inputs (Capaday and Rasmusson, 2003).…”

“…Studies involving the superposition of topographical maps of the motor cortex obtained by microstimulation and morphological connectivity maps obtained by tracer injections in physiologically identified sites have shown that motor cortical zones controlling various forelimb segments and those controlling antagonistic muscles are strongly interconnected by intrinsic horizontal collaterals (Huntley and Jones, 1991;Keller, 1993;Tokuno and Tanji, 1993;Capaday et al, 1998). These intracortical connections have been suggested to be the anatomical substrate of muscle synergies involved in coordinated multijoint movements (Huntley and Jones, 1991).…”

Cancellation of a planned movement in monkey motor cortex

“…Similarly, cross-correlational analyses of corticospinal neurons in MI reveal inhibitory connections between neuronal subpopulations with opposing muscle fields [16]. As the neuronal clusters representing antagonistic muscle actions are richly interconnected in MI [17], it appears likely that the connections exert an inhibitory influence, at least in part. Our results suggest that the relative juxtaposition of opposing direction representations may favor inhibitory interaction as a tool to shape overall population dynamics.…”