HYSTERESIS REDUCTION IN PROPRIOCEPTION USING PRESYNAPTIC SHUNTING INHIBITION

1. The tonic responses of angular-position-sensitive afferents in the metathoracic chordontal organ of the locust leg exhibit much hysteresi s. For a given joint angle, the ratio of an afferent's tonic firing ra te after extension to its firing rate after flexion (or vice versa) is typically between 1.2:1 and 3:1 but can be as large as 10:1. Spiking local interneurons, that receive direct inputs from these afferents, c an, by contrast, exhibit much less hysteresis (between 1.1:1 and 1.2:1 ). We tested the hypothesis that presynaptic inhibitory interactions b etween afferent axons reduces the hysteresis of postsynaptic interneur ons by acting as an automatic gain control mechanism. 2. We used two k inds of neural models to test this hypothesis: 1) an abstract nonspiki ng neural model in which a multiplicative, shunting term reduced the ' 'firing rate'' of the afferent and 2) a more realistic compartmental m odel in which shunting inhibition presynaptically attenuated the ampli tude of the action potentials reaching the afferent terminals. 3. The abstract neural model demonstrated the automatic gain control capabili ty of a network of laterally inhibited afferent units. A postsynaptic unit, which was connected to the competitive network of afferents, cod ed for joint angle without saturating as the strength of the afferent input increased by two orders of magnitude. This was possible because shunting inhibition exactly balanced the increase in the excitatory in put. This compensatory mechanism required the sum of the excitatory an d inhibitory conductances to be much larger than the leak conductance. This requirement suggested a graded weighting scheme in which the aff erent recruited first (i.e., at a small joint angle) received the larg est inhibition from each of the other afferents because of the lack of active neighbors, and the afferent recruited last (i.e., at a large j oint angle) received the least inhibition because all the other affere nts were active. 4. The compartmental model demonstrated that presynap tic shunting inhibition between afferents could decrease the average s ynaptic conductance caused by the afferents onto the spiking interneur on, thereby counterbalancing the afferents' large average firing rates after movements in the preferred direction. Therefore the total posts ynaptic input per unit time did not differ much between the preferred and nonpreferred directions. Hysteresis in the response of the modeled postsynaptic interneuron was thereby reduced from ratios as high as 2 .5:1 to <1:1. In addition, shunting inhibition prevented the modeled i nterneuron From saturating and front failing to fire. A local, lateral interaction shunting scheme in which an afferent is shunted only by i ts nearest neighbors (i.e., those afferents that are recruited at simi lar angles) reduced hysteresis sis and maintained the dynamic range of the spiking interneuron better than a global interaction scheme, wher e all afferents are presynaptically connected to each other. 5. The re sults of these simulations demonstrate a potential role for the establ ished presynaptic inhibitory interactions between proprioceptive affer ent terminals. In addition, these results allow us to make several tes table predictions. First, if lateral shunting inhibition between affer ent terminals can be selectively blocked pharma cologically, hysteresi s in the tonic response of the spiking local interneuron should increa se. Second, presynaptic shunting inhibition should exist between affer ents with similar recruitment thresholds, if not between all afferents that innervate the same spiking interneuron. Finally, we should expec t a graded synaptic weighting scheme such that presynaptic inhibitory conductances are greater onto the afferents that are recruited early.