INFLUENCE OF SYNAPTIC IDENTITY ON SINGLE-IA-AFFERENT CONNECTIVITY AND EPSP AMPLITUDE IN THE ADULT CAT - HOMONYMOUS VERSUS HETERONYMOUS CONNECTIONS

1. This study makes use of the pattern of synaptic connections between motoneurons and Ia afferents of triceps surae muscles in the cat to test the relative importance of synaptic identity, neuronal size, and neuronal topography as determinants of Ia-afferent connectivity and excitatory postsynaptic potential (EPSP) amplitude. 2. The synaptic actions of single-Ia medial gastrocnemius (MG) afferents were measured by intracellular recording in MG and lateral gastrocnemius (LG) motoneurons. The spike-triggered averaging technique was used to measure EPSPs generated by homonymous or heteronymous Ia afferents and motoneurons, i.e., neurons supplying the same or different muscles, respectively. In agreement with earlier studies, the pooled sample showed that the number of functional connections and the size of EPSPs were both significantly greater for homonymous than for heteronymous neurons. 3. Afferent conduction velocity, motoneuron conduction velocity, rheobase current, and position of the motoneuron relative to the spinal cord afferent entry were all correlated with EPSP amplitude, but the amplitude difference between homonymous and heteronymous connections remained significant after the statistical removal analysis of covariance (ANCOVA) of the contribution of these variables. Stepwise multiple-regression analysis showed that synaptic identity explained the greatest fraction of the variance in EPSP amplitude (9%), with significant but smaller fractions accounted for by rheobase current or motoneuron conduction velocity. 4. In a separate experiment, the monosynaptic affects from both homonymous and heteronymous single-Ia afferents were examined in each of 88 MG or LG motoneurons. The single-Ia afferents used in this portion of the study were sampled from both MG and LG muscles and selected for similar conduction velocities and spinal cord entry points. 5. With the contributions of neuronal size and topography experimentally minimized, for motoneurons in which both homonymous and heteronymous afferents produced an EPSP, the amplitudes of those EPSPs were similar. However, in 95% of the motoneurons where one afferent failed to produce an EPSP, it was the heteronymous EPSP that was absent. 6. These findings provide critical substantiation for the recently challenged assertion that the identity of Ia afferents and motoneurons, specified by whether they supply the same or different muscles, is important, apart from neuron size and central topography, in determining the frequency with which single neurons make functional monosynaptic connections in the spinal cord. In contrast, we conclude that the strength of functional connections is only weakly influenced, if at all, by the homonymous versus heteronymous identity of central monosynaptic connections made by neurons supplying muscles that are close synergists.