Brain Research, 629 (1993) 319-322 319 Elsevier Science Publishers B.V. BRES 25900 Conversion of parasympathetic nerve function from prejunctional inhibition to postjunctional excitation following sympathectomy of rat periorbital smooth muscle Peter G. Smith *, Curtis L. Beauregard Department of Physiology, University of Kansas Medical Center, 3901 Rainbow Blvd., Kansas City, KS 66160-740L USA (Accepted 10 August 1993) Key words: Acetylcholine; Neuronal plasticity; Pterygopalatine ganglion; Superior cervical ganglionectomy; Superior sativatory nucleus; Superior tarsal muscle Parasympathetic innervation of rat periorbital smooth muscle normally inhibits excitatory sympathetic neurotransmission but does not directly affect muscle tone. Five weeks after sympathetic denervation, however, parasympathetic stimulation now elicits contractions. These are blocked by atropine, indicating establishment of muscarinic cholinergic neuromuscular transmission. Conversion to excitation is not accompanied by enhanced smooth muscle responsiveness to muscarinic stimulation, indicating that prejunctional alterations are responsible. Factors governing neuronal structure and function are not fully understood. While phenotype is deter- mined in part by genetic factors, the environment im- mediately surrounding the neuron is also important. A critical aspect of this microenvironment is the presence of heterologous innervation. Recent studies have shown that biochemical and structural features can be altered substantially by removal of co-projecting nerves. For example, sympathetic denervation can induce struc- tural changes in peripheral terminal arbors of remain- ing sensory and parasympathetic n e r v e s 1'6'13'z4'27. Molecular constituents are also affected, with changes occurring in expression of neuropeptides and transmit- ter enzymes of parasympathetic neurons 4,7'9,1°,25. Hence, ablation of one neuronal population can signifi- cantly alter structural and molecular features of other- wise unperturbed neurons. It has not been determined whether, in addition, heterologous denervation can affect neuronal function. To explore this possibility, we examined the effect of sympathetic denervation on parasympathetic neuro- transmission within the superior tarsal muscle (STM), a periorbital smooth muscle that elevates the upper eye- lid. This target is well suited to the objective, as sympa- thetic innervation can be surgically eliminated 19, parasympathetic nerves selectively activated 2'~6, and smooth muscle function assessed directly by measuring contractile force of the superior eyetid 5'15'w'18. While sympathetic nerves normally provide excitatory motor innervation, parasympathetic nerves influence STM function by attenuating sympathetic neurotransmission via prejunctional mechanisms; they do not themselves exert direct actions on the postjunctional smooth muscle 2A6. Orbital sympathetic innervation was eliminated uni- laterally in 8 young adult female Sprague-Dawley rats (Sasco) by aseptically excising a superior cervical gan- glion under isoflurane anesthesia s,t9. Five weeks later, rats were anesthetized with urethane (1.25 g/kg, i.p.), a cannula placed in the femoral vein, and the head positioned in a stereotaxic frame. Superior tarsal mus- cle tension was measured bilaterally by attaching force displacement transducers (FT03C, Grass Instruments) to the superior eyelids by silk suture with an initial loading tension of 1.0 g. To stimulate parasympathetic innervation to the intact or sympathectomized STM, a semi-micro bipolar concentric electrode (100/xm con- tact diameter) was placed in the ipsilateral superior * Corresponding author. Fax: (1) (913) 588-7430.