MOTONEURON PROPERTIES AFTER OPERANTLY CONDITIONED INCREASE IN PRIMATE H-REFLEX

1. Monkeys can increase (HRup conditioning mode) or decrease (HRdown conditioning mode) the triceps surae (TS) H-reflex in response to an operant conditioning task. This conditioning modifies the spinal cord. To define this spinal cord plasticity and its role in the behavioral change (H-reflex increase or decrease), we have recorded intracellularly from TS motoneurons in conditioned animals. The present report describes data from HRup animals and compares them with data from previously studied naive (NV; i.e., unconditioned) animals. 2. Thirteen monkeys (Macaca nemestrina, male, 3.8-7.1 kg) were exposed to the HRup conditioning mode, in which reward occurred when H-reflex size in one leg (i.e., the trained leg) was above a criterion value. Conditioning was successful (i.e., increase of greater than or equal to 20%) in 12 of the 13 animals. At the end of conditioning, H-reflex size in the trained leg averaged 188% of its initial value, whereas size in the control leg averaged 134% of its initial value. 3. Intracellular recordings were obtained from 136 TS motoneurons on trained (UT + motoneurons) and control (UCS motoneurons) sides of the successful animals. Measurements included axonal conduction velocity, input resistance, time constant, electrotonic length, rheobase, firing threshold to current injection, afterhyperpolarization duration and amplitude, and composite homonymous and heteronymous excitatory postsynaptic potential (EPSP) size and shape. Results were compared with intracellular data from NV animals. 4. Although HRup motoneurons displayed several significant differences from NV motoneurons, analysis of these and other intracellular properties alone or in combination did not explain the behavioral change evident in the awake behaving animal (i.e., a much larger H-reflex in the trained leg). Firing threshold to current injection was more positive (i.e., depolarized; P < 0.01) in UT + motoneurons than in NV motoneurons and tended to be more negative (P < 0.05) in UC + motoneurons than in NV motoneurons. Non-TS heteronymous EPSPs were much smaller in both UT + and UC + motoneurons than in NV motoneurons. 5. These results from HRup animals combined with earlier data from HRdown animals indicate that H-reflex increase under the HRup mode and H-reflex decrease under the HRdown mode are not mirror images of each other, but rather depend on different mechanisms. Although conditioned H-reflex decrease appears ascribable to changes in motoneuron properties and EPSPs, conditioned If-reflex increase is due either to motoneuron or EPSP changes that went undetected by the present intracellular methods or to changes elsewhere in the spinal cord. One possibility is that H-reflex increase was caused by a negative shift in threshold to synaptic input that was not accompanied by a corresponding shift in threshold to current injection. A second possibility is that HRup increase was caused by a change in the interneurons that mediate group I disynaptic input from TS muscles to TS motoneurons. Such disynaptic input could reach the motoneuron quickly enough to affect the H-reflex. 6. The intracellular data from HRup animals add to the evidence indicating that both HRup and HRdown conditioning involve changes at multiple spinal and supraspinal sites. These changes probably comprise primary changes that are responsible for the mode-appropriate H-reflex change and secondary changes that are consequences of the primary changes.