Time course of the rabbit's conditioned nictitating membrane movements during acquisition, extinction, and reacquisition

Abstract

The present experiment tested whether or not the time course of a conditioned eyeblink response, particularly its duration, would expand and contract, as the magnitude of the conditioned response (CR) changed massively during acquisition, extinction, and reacquisition. The CR duration remained largely constant throughout the experiment, while CR onset and peak time occurred slightly later during extinction. The results suggest that computational models can account for these results by using two layers of plasticity conforming to the sequence of synapses in the cerebellar pathways that mediate eyeblink conditioning.Computational models of eyeblink conditioning generally predict that, during the pairings of a conditioned stimulus (CS) with the unconditioned stimulus (US), the conditioned response (CR) should expand in magnitude and duration around the point of US delivery. Thus, during acquisition, the CR should roughly resemble the changes in the height and width of the sun's rising across the horizon, as depicted schematically in the top panel of Figure 1. Conversely, during the successive CS-alone presentations in extinction, the CR should contract like a setting sun.These predictions flow from the shared assumption that the CS onset initiates a spectrum of microstimuli, whose intensities increase and decrease at different rates (Desmond and Moore 1988;Grossberg and Schmajuk 1989;Machado 1997;Ludvig et al. 2012). At a neural level, the spectrum of microstimuli appears to start with the projection of mossy fibers into the cerebellar cortex (Buonomano and Mauk 1994;Moore and Choi 1997;Mauk et al. 2000;Lepora et al. 2010). In turn, these mossy fiber inputs are refined as temporal codes by interactions among Golgi and granule cells that are active at different times (Kalmbach et al. 2011). Experimentally, asynchronous stimulation of two populations of mossy fibers can act as a CS for acquisition of welltimed eyeblink CRs in rabbits, and post-acquisition manipulations of the relative stimulus durations can predictably alter the CR timing (Kalmbach et al. 2011). In turn, the outputs of these cells activate parallel fibers that converge near the base of Purkinje cells. As a result of pairing stimulation of these microstimulus-like pathways with stimulation of ascending US pathways, CR-like activity has, in fact, been observed in individual Purkinje cells (Jirenhed et al. 2007;Jirenhed and Hesslow 2011).According to the behavioral and neural models described above, each microstimulus gains associative strength in proportion to its level of activation during the US. Thus, the microstimulus whose maximum intensity occurs during the US will gain the greatest associative strength, although microstimuli that are weaker at the time of US will gain less associative strength. During subsequent CS presentations, the magnitude of a CR at any point in time reflects the sum of the associative strengths of the microstimuli multiplied by their level of activity at that moment.Hence, a CR's peak occurs near the time of US delivery, a...