Intracellular recordings were made from antidromically-identified somatosensory projection neurons in the spinal dorsal horn of anesthetized cats. These neurons belonged to the dorsal column postsynaptic tract (DCPS), spinocervical tract (SCT), or spinothalamic tract (STT). Each neuron's responses to electrical and natural stimulation of its cutaneous receptive field were examined; the cells were thus classified as either low-threshold mechanoreceptive (responsive only to innocuous mechanical stimuli) or wide-dynamic-range (responsive to both innocuous mechanical and painful stimuli). Electric stimulation of an appropriate peripheral nerve at an intensity that was just strong enough to excite touch-responsive primary afferents produced an excitatory postsynaptic potential (EPSP) followed by an inhibitory postsynaptic potential (IPSP) in nearly every neuron. The IPSPs were distinguished from other types of hyperpolarizing intracellular potentials by intracellular current injection, intracellular injection of chloride ions, and by direct measurements of membrane resistance. The EPSP and IPSP had practically identical thresholds, indicating that they were both evoked by the same afferents. The amplitude of the IPSP was constant when stimuli were delivered at 1 Hz or less, but decreased progressively in a step-like manner with frequencies of 2-30 Hz. The IPSP amplitude was virtually zero at frequencies of 30 Hz or more. These results show that the IPSP evoked by low-threshold mechanoreceptive afferents is unusually sensitive to stimulus frequencies and suggest that the output of the interneuron that causes the IPSP is similarly frequency dependent. A search of the dorsal horn revealed a population of small interneurons in lamina III that exhibited such a frequency dependency. Intracellular injection of horseradish peroxidase has established the morphology of these cells and shown that their axonal terminations are found in laminae III-V. These laminae also include the dendrites of DCPS, SCT and STT neurons, thus a direct synaptic linkage of interneuron to projection neuron is plausible.
