Edward S Boyden, Jennifer L Raymond  Neuron 

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Active Reversal of Motor Memories Reveals Rules Governing Memory Encoding  Edward S Boyden, Jennifer L Raymond  Neuron  Volume 39, Issue 6, Pages 1031-1042 (September 2003) DOI: 10.1016/S0896-6273(03)00562-2

Figure 1 Persistent Changes in VOR Induced by Gain-Up and Gain-Down Stimuli (A) Gain-up stimulus. Optokinetic drum (dashed circle) and head move sinusoidally in opposite directions, with peak drum velocity equal to 50% of peak head velocity. (B) Gain-down stimulus. The drum moves with the head. (C) Representative eye (top) and head (bottom) velocity traces recorded in darkness before and after 30 min of gain-up training. (D) Representative eye and head velocity traces as in (C), but for a gain-down training session. (E) Changes in VOR gain, induced by 30 min of gain-up (circles; n = 30) or gain-down (squares; n = 30) training. VOR was measured in the dark every 10 min, during a 30 min training session. In all figures, data points are plotted as mean ± SEM, and n refers to the number of mice (each used only once). Throughout the figures, VOR gain is normalized by the initial VOR gain, and error bars are omitted whenever they are smaller than the symbols. τ, time constant for learning. (F) Changes in VOR phase, induced by 30 min of gain-up and gain-down stimuli. Positive values represent an increase in phase lead. Symbols as in (E). (G) VOR gain measured at the end of a 30 min gain-up or gain-down training session (trained, white bars) and after an additional 24 hr in complete darkness (+24h, dark bars) (n = 9). Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)

Figure 2 Changes in VOR Gain Induced when Gain-Up and Gain-Down Training Sessions Are Concatenated (A) Increases in VOR gain induced by three 30 min gain-up training sessions (red symbols). Between training sessions, there were either 2 hr (filled circles) or 24 hr (open circles) rest periods in darkness, indicated by shaded bars (n = 14, n = 9, respectively). The x axis indicates the cumulative time of gain-up training experienced. (B) Oppositely directed changes in VOR gain induced by gain-down training (blue symbols) following gain-up training (n = 10, n = 9, respectively, through 1 hr of gain-down training; n = 5, n = 5, respectively, through 2 hr). The x axis time is reset to zero when the gain-down protocol begins. The solid curve starting at the 10 min point in gain-down training is the exponential fit to gain-down training from the naive state (Figure 1E) for comparison to the time courses shown here. ∇ marks the time point used for comparison to naive mice undergoing gain-down in the text. (C) Decreases in VOR gain induced by three 30 min gain-down training sessions (blue symbols), with either 2 hr (filled squares) or 24 hr (open squares) rest periods in between training sessions (n = 15, n = 9, respectively). (D) Oppositely directed changes in VOR gain induced by gain-up training (red symbols) following gain-down training with either 2 hr (filled squares) or 24 hr (open squares) rest periods (n = 14, n = 9, respectively, through 1 hr of gain-up training; n = 12, n = 6, respectively through 2 hr). The solid curve beginning at the 80 min point in gain-up training is the exponential fit to gain-up training from the naive state (Figure 1E). ∇∇ marks the time point at which the VOR is restored to its original gain, for mice pretrained with gain-down sessions with 2 hr rests. Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)

Figure 3 Retinal Image Slip during Training (A) Retinal image slip velocity, measured during gain-up (circles) and gain-down (squares) training sessions. Measurements were made at the beginning and end of every 10 min training block. (B) Retinal image slip velocity during gain-up training, for both naive mice (filled circle; n = 30) and mice pretrained with gain-down stimuli (squares; n = 12). ∇∇ marks the time point when the VOR is restored to its original gain. Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)

Figure 4 Changes in VOR Phase Induced when Gain-Up and Gain-Down Training Sessions Are Concatenated (A–D) Changes in VOR phase accompanying the changes in VOR gain shown in Figures 2A–2D, respectively. Symbols are as in Figure 2. (E) Phase change plotted versus gain change, during the experiments where gain-up training (red), with either 2 hr (top) or 24 hr (bottom) rests, is followed by gain-down training (blue). “Start” and “end” indicate the beginning and end of the entire protocol. Arrows indicate progression of time. (F) Phase change plotted versus gain change, during the experiments where gain-down training (blue), with either 2 hr (top) or 24 hr (bottom) rests, is followed by gain-up training (red). Hysteresis is prominent in the gain-phase relation. Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)

Figure 5 Dependence of Reversal of Decreases in VOR Gain on Amount of Training (A) Effects of extensive gain-up training and periods of normal visual experience following three gain-down sessions (n = 6). Time courses are shown for each of the six individual mice run on this protocol. Shaded bars indicate periods of darkness, whereas open bars indicate periods of normal light-dark cycles. (B) Changes in VOR gain observed during one (diamonds; n = 7) or two (triangles; n = 7) gain-down training sessions (blue symbols), followed by gain-up training (red symbols). The solid curves beginning at the 30 and 60 min points in gain-up training are the exponential fit to gain-up training from the naive state (Figure 1E), for comparison. (C) Changes in VOR phase, for one or two gain-down training sessions, followed by gain-up training. (D and E) Phase change plotted versus gain change, during the experiments in which one (D) or two (E) gain-down training sessions (blue symbols) are followed by gain-up training (red symbols). Asterisk marks the beginning of the second gain-up training session. Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)

Figure 6 Two Classes of Model for How an Increase and a Decrease in VOR Gain Are Each Encoded (A) A model using the same plasticity mechanism for both an increase and a decrease in VOR gain. For each behavioral training paradigm (gain-up, gain-down, gain-up then gain-down, and gain-down then gain-up), two parallel fibers are shown synapsing onto a single Purkinje cell dendrite. One parallel fiber fires during ipsiversive head turns (toward the side of the Purkinje cell), and the other fires during contraversive head turns (away from the side of the Purkinje cell). Lightning bolts indicate plasticity mechanisms being considered at the parallel fiber-Purkinje cell synapse. It has been proposed that LTD (open lightning bolts) of ipsiversive-responding parallel fibers induces an increase in VOR gain (gain-up), and LTD of contraversive-responding parallel fibers induces a decrease in VOR gain (gain-down) (Ito, 1972; Ito, 1982). When an increase and a decrease in VOR gain are concatenated in either order (gain-up then gain-down, gain-down then gain-up), the predicted changes mask but do not reverse each other. LTD is induced in both synapses, in either case. (B) A model using different plasticity mechanisms for an increase and a decrease in VOR gain. Parallel fiber-Purkinje LTD is expressed postsynaptically, but there are both pre- and postsynaptically expressed forms of LTP at this synapse (Hemart et al., 1994; Lev-Ram et al., 2002; Linden et al., 1991; Salin et al., 1996). Only ipsiversive-responding parallel fibers are needed, consistent with the observation that the majority of Purkinje cells increase their firing during ipsiversive head motion, when the eyes are held still (Lisberger and Fuchs, 1978). An increase in VOR gain is implemented as in the original cerebellar LTD model (gain-up), but in this model a decrease in VOR gain is mediated by both pre- and postsynaptic forms of LTP (gain-down). When an increase in VOR gain is followed by a decrease in gain, first postsynaptically expressed LTD is induced, followed by pre- and postsynaptically expressed LTP (gain-up then gain-down). Reversal is complete if the postsynaptic component of LTP erases postsynaptic LTD. When a decrease is followed by an increase, however, first pre- and postsynaptically expressed LTP are induced, followed by postsynaptically expressed LTD (gain-down then gain-up). Even if the postsynaptically expressed plasticity components reverse each other, the presynaptic component of LTP is not reversed. This general class of models could explain the asymmetry in reversibility of increases and decreases in VOR gain. Neuron 2003 39, 1031-1042DOI: (10.1016/S0896-6273(03)00562-2)