The selectivity of rostroventral medulla descending control of spinal sensory inputs shifts postnatally from A fibre to C fibre evoked activity

Key points Brainstem descending pathways control the balance of excitation and inhibition in spinal sensory networks. In adult rodents, descending inhibition is targeted to spinal neurons with a strong afferent C fibre input. Descending inhibitory control matures slowly; the first postnatal weeks are characterized by greater descending facilitation than inhibition. We report that, in contrast to adults, brainstem descending facilitation of spinal sensory neurons in young rats (postnatal day 21) is targeted to A fibre inputs. The selective inhibition of C fibre inputs observed in adults is absent at postnatal day 21. In both young and adult rats, descending inhibition or facilitation is correlated with the excitability of individual neurons, as measured by ‘wind‐up’ to repeated C fibre stimulation. The facilitation of A fibre input in early life is likely to enhance innocuous, tactile sensory inputs to the dorsal horn in the critical early postnatal weeks and thus promote activity‐dependent development of sensory networks. Brainstem descending control is crucial in maintaining the balance of excitation and inhibition in spinal sensory networks. In the adult, descending inhibition of spinal dorsal horn circuits arising from the brainstem rostroventral medial medulla (RVM) is targeted to neurons with a strong nociceptive C fibre input. Before the fourth postnatal week, the RVM exerts a net facilitation of spinal networks but it is not known if this is targeted to specific dorsal horn neuronal inputs. As the maturation from descending facilitation to inhibition occurs only after C fibre central synaptic maturation is complete, we hypothesized that RVM facilitation in young animals is targeted to A fibre afferent inputs. To test this, the RVM was stimulated while recording dorsal horn neuronal activity in vivo under isoflurane anaesthesia at postnatal day (P) 21 and P40 (adult). Electrical thresholds for A and C fibre evoked activity, spike counts and wind‐up characteristics at baseline and during RVM stimulation (10–100 µA, 10 Hz) were compared. In adults, RVM stimulation selectively increased the threshold for C fibre evoked activity while at P21, it selectively decreased the threshold for A fibre evoked activity and these effects were correlated to the wind‐up characteristics of the neuron. Thus, the postnatal shift in RVM control of dorsal horn circuits is not only directional but also modality specific, from facilitation of A fibre input in the young anima