SELECTIVE CORTICAL AND SEGMENTAL CONTROL OF PRIMARY AFFERENT DEPOLARIZATION OF SINGLE MUSCLE AFFERENTS IN THE CAT SPINAL-CORD

This study was primarily aimed at investigating the selectivity of the cortico-spinal actions exerted on the pathways mediating primary affe rent depolarization (PAD) of muscle spindle and tendon organ afferents ending within the intermediate nucleus at the L6-L7 segmental level. To this end we analyzed, in the anesthetized cat, the effects produced by electrical stimulation of sensory nerves and of the cerebral corte x on (a) the intraspinal threshold of pairs of single group I afferent fibers belonging to the same or to different hindlimb muscles and (b) the intraspinal threshold of two collaterals of the same muscle affer ent fiber. Afferent fibers were das sified in three categories, accord ing to the effects produced by stimulation of segmental nerves and of the cerebral cortex. Twenty-five of 40 fibers (62.5%) were depolarized by stimulation of group I posterior biceps and semitendinosus (PBSt) or tibialis (Tib) fibers, but not by stimulation of the cerebral corte x or of cutaneous and joint nerves, which instead inhibited the PBSt- or Tib-induced PAD (type A PAD pattern, usually seen in Ia fibers). Th e remaining 15 fibers (37.5%) were all depolarized by stimulation of t he PBSt or Tib nerves and the cerebral cortex. Stimulation of cutaneou s and joint nerves produced PAD in 10 of those 15 fibers (type B PAD p attern) and inhibited the PBSt- or Tib-induced PAD in the 5 remaining fibers (type C PAD pattern). Fibers with a type B or C PAD pattern are likely to be Ib. Not all sites in the cerebral cortex inhibited with the same effectiveness the segmentally induced PAD of group I fibers w ith a type A PAD pattern. With the weakest stimulation of the cortical surface, the most effective sites that inhibited the PAD of individua l fibers were surrounded by less effective sites, scattered all along the motor cortex (area 4 gamma and 6) and sensory cortex (areas 3, 2 a nd 1), far beyond the area of projection of group I fibers from the hi ndlimb. With higher strengths of cortical stimulation, the magnitude o f the inhibition was also increased, and previously ineffective or wea kly effective sites became more effective. Maps obtained when using th e weakest cortical stimuli have indicated that the most effective regi ons that produced PAD of group I fibers with a type B or type C PAD pa ttern were also scattered throughout the sensory-motor cortex, in the same general area as those that inhibited the PAD of group I afferents with a type A PAD pattern. In eight fibers with a type A PAD pattern it was possible to examine the intraspinal threshold of two collateral s of the same single afferent fiber ending within the intermediate nuc leus at the L7 segmental level. In six fibers, stimulation of the PBSt nerve with trains of pulses between 1.5 and 1.86 times threshold (xT) produced a larger PAD in one collateral than in the other. In seven f ibers, stimulation of the sensory-motor cortex and of cutaneous nerves produced a larger inhibition of the PBSt-induced PAD in one collatera l than in the other. The ratio of the cortically induced inhibition of the PAD elicited in the two collaterals could be modified by changing the strength of cortical and of PBSt stimulation. In three fibers it was possible to inhibit almost completely the background PAD elicited in one collateral while having little or no effect on the PAD in the o ther collateral. Changes in the intraspinal threshold of pairs of coll aterals following electrical stimulation of segmental nerves and of th e somato-sensory cortex were examined in three fibers with a type B an d two fibers with a type C PAD pattern. In four fibers the PAD elicite d by stimulation of cutaneous (4-20xT) and muscle nerves (1.54-3. 7xT) , or by stimulation of the sensory-motor cortex, was of different magn itude in the two collaterals. In two experiments it was possible to fi nd cortical sites in which weak surface stimulation produced PAD in on e collateral only. The magnitude of the PAD elicited in pairs of colla terals of group I afferents with a type B or C PAD pattern, or the inh ibition of the PAD in pairs of collaterals of fibers with a type A PAD pattern, appeared not to be topographically related to the site of sp inal projection of the cutaneous and cortico-spinal fibers used for co nditioning stimulation. The present demonstration of a differential co ntrol of the PAD exerted on two collaterals of the same afferent fiber suggests that the profuse intraspinal branching of muscle spindle and tendon organs is a potentially rich substrate for information transmi ssion. By means of presynaptic control mechanisms, the terminal arbori zations of the afferent fibers could function either as a simple unit or in a fractionated manner, allowing funneling of information to sele cted groups of central neurons.