Recruitment in retractor bulbi muscle during eyeblink conditioning: EMG analysis and common-drive model.

To analyze properly the role of the cerebellum in classical conditioning of the eyeblink and nictitating membrane (NM) response, the control of conditioned response dynamics must be better understood. Previous studies have suggested that the control signal is linearly related to the CR as a result of recruitment within the accessory abducens motoneuron pool, which acts to linearize retractor bulbi muscle and NM response mechanics. Here we investigate possible recruitment mechanisms. Data came from simultaneous recordings of NM position and multiunit electromyographic (EMG) activity from the retractor bulbi muscle of rabbits during eyeblink conditioning, in which tone and periocular shock act as conditional and unconditional stimuli, respectively. Action potentials (spikes) were extracted and classified by amplitude. Firing rates of spikes with different amplitudes were analyzed with respect to NM response temporal profiles and total EMG spike firing rate. Four main regularities were revealed and quantified: 1) spike amplitude increased with response amplitude; 2) smaller spikes always appeared before larger spikes; 3) subsequent firing rates covaried for spikes of different amplitude, with smaller spikes always firing at higher rates than larger ones; and 4) firing-rate profiles were approximately Gaussian for all amplitudes. These regularities suggest that recruitment does take place in the retractor bulbi muscle during conditioned NM responses and that all motoneurons receive the same command signal (common-drive hypothesis). To test this hypothesis, a model of the motoneuron pool was constructed in which motoneurons had a range of intrinsic thresholds distributed exponentially, with threshold linearly related to EMG spike amplitude. Each neuron received the same input signal as required by the common-drive assumption. This simple model reproduced the main features of the data, suggesting that conditioned NM responses are controlled by a common-drive mechanism that enables simple commands to determine response topography in a linear fashion.

Evidence from retractor bulbi EMG for linearized motor control of conditioned nictitating membrane responses.

Classical conditioning of nictitating membrane (NM) responses in rabbits is a robust model learning system, and experimental evidence indicates that conditioned responses (CRs) are controlled by the cerebellum. It is unknown whether cerebellar control signals deal directly with the complex nonlinearities of the plant (blink-related muscles and peripheral tissues) or whether the plant is linearized to ensure a simple relation between cerebellar neuronal firing and CR profile. To study this question, the retractor bulbi muscle EMG was recorded with implanted electrodes during NM conditioning. Pooled activity in accessory abducens motoneurons was estimated from spike trains extracted from the EMG traces, and its temporal profile was found to have an approximately Gaussian shape with peak amplitude linearly related to CR amplitude. The relation between motoneuron activity and CR profiles was accurately fitted by a first-order linear filter, with each spike input producing an exponentially decaying impulse response with time constant of order 0.1 s. Application of this first-order plant model to CR data from other laboratories suggested that, in these cases also, motoneuron activity had a Gaussian profile, with time-of-peak close to unconditioned stimulus (US) onset and SD proportional to the interval between conditioned stimulus and US onsets. These results suggest that for conditioned NM responses the cerebellum is presented with a simplified "virtual" plant that is a linearized version of the underlying nonlinear biological system. Analysis of a detailed plant model suggests that one method for linearising the plant would be appropriate recruitment of motor units.