Memory of learning facilitates saccadic adaptation in the monkey

“Two rhesus monkeys (Macaca mulatta, male; 4.5 and 6.8 kg) were prepared for eye movement recording by the magnetic search coil method (Fuchs and Robinson, 1966).”

“The oculo - motor vermis and the fastigial oculomotor region ( FOR ) of the cerebellum have been shown to be key players in saccadic adap - tation ( Optican and Robinson , 1980 ; Takagi et al .”

“Adaptive changes in saccade amplitude were induced by a conventional intrasaccadic target step paradigm (McLaughlin, 1967).”

“The oculomotor vermis and the fastigial oculomotor region (FOR) of the cerebellum have been shown to be key players in saccadic adaptation (Optican and Robinson, 1980; Takagi et al., 1998; Barash et al., 1999; Scudder, 2002; Inaba et al., 2003; Scudder and McGee, 2003).”

“Recent results describe a previously unrecognized form of long-term potentiation in the cerebellar cortex (Lev-Ram et al., 2002) and a synaptic depotentiation in the hippocampus (Montgomery and Madison, 2002).”

“This is because the saccadic gain (saccade amplitude divided by target eccentricity) is constantly recalibrated by a learning mechanism called saccadic adaptation (for review, see Hopp and Fuchs, 2004).”

“The oculomotor vermis and the fastigial oculomotor region (FOR) of the cerebellum have been shown to be key players in saccadic adaptation (Optican and Robinson, 1980; Takagi et al., 1998; Barash et al., 1999; Scudder, 2002; Inaba et al., 2003; Scudder and McGee, 2003).”

“In the subsequent recovery block, the cortical plasticity decreases back to and possibly beyond the preadaptation level, as has been suggested for the extinction of eye blink conditioning (Medina et al., 2001), but the nuclear plasticity remains potentiated.”

“There is good evidence that saccadic adaptation is a form of motor learning driven by visual error immediately after the end of saccades (Wallman and Fuchs, 1998; Shafer et al., 2000; Noto and Robinson, 2001).”

“Adaptation is fairly specific to the amplitude and direction of adapted saccades and does not generalize fully to those with different vectors (Straube et al., 1997; Wallman and Fuchs, 1998; Noto et al., 1999; Watanabe et al., 2000).”

“It has been demonstrated that adaptation progresses more slowly when the subject is exposed to adapting target steps of a variety of sizes and directions in humans (Miller et al., 1981) and monkeys (Scudder et al.”

“Previous studies have shown that adaptation is relatively specific to the size and direction of target eccentricity (Deubel et al., 1987; Semmlow et al., 1989; Frens and van Opstal, 1994; Straube et al., 1997; Noto et al., 1999; Watanabe et al., 2000).”

“, 2002 ) and a synaptic depotentiation in the hippocampus ( Montgomery and Madison , 2002 ) .”

“Reexposure to paired stimuli after extinction induces reacquisition that is much faster than original acquisition (Frey and Ross, 1968; Napier et al., 1992), indicating that a memory of learning is formed to facilitate subsequent learning.”

“, 1995 ) and use of a novel behavioral paradigm in mice ( Boyden and Raymond , 2003 ) have both suggested separate plasticity mechanisms for increases and decreases in vestibuloocular reflex gain .”

“Previous studies have shown that adaptation is relatively specific to the size and direction of target eccentricity (Deubel et al., 1987; Semmlow et al., 1989; Frens and van Opstal, 1994; Straube et al., 1997; Noto et al., 1999; Watanabe et al., 2000).”

“There is good evidence that saccadic adaptation is a form of motor learning driven by visual error immediately after the end of saccades (Wallman and Fuchs, 1998; Shafer et al., 2000; Noto and Robinson, 2001).”

“Previous studies have shown that adaptation is relatively specific to the size and direction of target eccentricity (Deubel et al., 1987; Semmlow et al., 1989; Frens and van Opstal, 1994; Straube et al., 1997; Noto et al., 1999; Watanabe et al., 2000).”

“A recent study has further demonstrated that adaptation occurs upstream of the FOR (Robinson et al., 2002).”

“Adaptation elicited by an intrasaccadic step (ISS) of the target (McLaughlin, 1967) has an approximately exponential course with a rate constant of 100 – 800 saccades (Straube et al., 1997; Scudder et al., 1998).”

“, 2003 ; Scudder and McGee , 2003 ) .”

“Reexposure to paired stimuli after extinction induces reacquisition that is much faster than original acquisition (Frey and Ross, 1968; Napier et al., 1992), indicating that a memory of learning is formed to facilitate subsequent learning.”

“The amount and rate of adaptation are highly variable across animals and also across experiments in the same animal (Fuchs et al., 1996; Straube et al., 1997).”

“There is good evidence that saccadic adaptation is a form of motor learning driven by visual error immediately after the end of saccades (Wallman and Fuchs, 1998; Shafer et al., 2000; Noto and Robinson, 2001).”

“The oculomotor vermis and the fastigial oculomotor region (FOR) of the cerebellum have been shown to be key players in saccadic adaptation (Optican and Robinson, 1980; Takagi et al., 1998; Barash et al., 1999; Scudder, 2002; Inaba et al., 2003; Scudder and McGee, 2003).”

“, 1999 ; Scudder , 2002 ; Inaba et al .”

“Previous studies have shown that adaptation is relatively specific to the size and direction of target eccentricity (Deubel et al., 1987; Semmlow et al., 1989; Frens and van Opstal, 1994; Straube et al., 1997; Noto et al., 1999; Watanabe et al., 2000).”

“Previous studies have shown that adaptation is relatively specific to the size and direction of target eccentricity (Deubel et al., 1987; Semmlow et al., 1989; Frens and van Opstal, 1994; Straube et al., 1997; Noto et al., 1999; Watanabe et al., 2000).”

“This phenomenon has been observed in a wide range of paradigms (Rescorla, 2004;Kojima et al., 2004;Stollhoff et al., 2005).”

“A recent model 79 based on this idea of temporal credit assignment can account for a number of phenomena that are related to reach movement adaptation to perturbations as well as saccadic adaptation 98 .”

“observed in their saccade adaptation experiment following a period of darkness [3].”

“In particular, relearning of a given perturbation for a second time is faster than initial learning, a phenomenon known as savings (Ebbinghaus, 1913; Kojima et al., 2004; Krakauer et al., 2005; Smith et al., 2006; Zarahn et al., 2008), whereas a basic single-timescale SSM predicts that learning…”

“Memory in adaptation paradigms is also evident in the form of savings: when subjects are re-exposed to the same rotation or force field after some time interval, adaptation occurs more rapidly (Kojima et al., 2004; Krakauer et al., 2005; Smith et al., 2006; Zarahn et al., 2008).”

“…successfully accounts for a number of adaptation phenomena, including savings, wherein the second adaptation to a task is faster than the first (Kojima et al., 2004); anterograde interference, wherein learning a second task interferes with the recall of the first task (Miall et al., 2004); and…”

“We considered a common paradigm in which a long period of adaptation was followed by a brief period of deadaptation (Kojima et al., 2004; Criscimagna-Hemminger and Shadmehr, 2008; Ethier et al., 2008).”

“This picture changed when it became clear that motor memories exhibited a phenomenon termed spontaneous recovery (Kojima et al., 2004; Smith et al., 2006; Ethier et al., 2008).”

“Spontaneous recovery has also been observed with saccades (Kojima et al. 2004 ).”

“For example, a saccadic gain experiment using an A1BA2 learning paradigm found faster relearning of Task A during the second exposure, even though this second instance of Task A immediately followed exposure to Task B [3], and thus would require a switch between different internal models.”

“If saccades to target steps of one amplitude and direction experience an intrasaccadic target adapt jump, ϳ500 –1000 erroneous trials are required for nearly complete adaptation in the monkey (Straube et al., 1997; Kojima et al., 2004).”

“These include savings (Kojima et al., 2004), anterograde interference (Miall et al.”

“Importantly, such motor memories are also recalled even after participants unlearn the new motor pattern and return to baseline performance (Caithness et al. 2004; Kitago et al. 2013; Kojima et al. 2004; Krakauer et al. 2005; Malone et al. 2011; Shadmehr and Brashers-Krug 1997).”

“, extinction) phase [13, 43, 44] and improves the effectiveness of the reactive recovery component [17].”

“Moreover, our findings are consistent with previous studies and support the multiple-timescale model that drives motor adaptation while learning novel motor tasks (Hatada et al. 2006; Kojima et al. 2004; Smith et al. 2006).”

“in paradigms that are less likely to be influenced by time-consuming deliberate 756 strategies, such as saccadic adaptation (Kojima et al., 2004).”

“Moreover, immediately after a short-term adaptation has been completed and extinguished by actively deadapting saccade amplitude, a new learning sequence occurs at a faster rate (Kojima et al., 2004).”

“, an interlimb version of savings; Kojima et al. 2004; Sing and Smith 2010; Smith et al. 2006; Zarahn et al. 2008) compared with the condition in which the untrained limb was tested before prior training with the opposite limb. Both the present study and the Malfait and Ostry (2004) study were carefully designed so th…”

“Kojima et al. (2004) speculate that the observed increase in saccade adaptation speed might be due to activation of one mechanism and deactivation of the other taking place at the same”

“While evidence for savings has been accumulated from different systems [saccades, arm reaching, and locomotion (Kojima et al. 2004; Krakauer et al. 2005; Malone et al. 2011)] and across paradigms [saccades, visuomotor; and force filed adaptation (Kojima et al.”

“It is well established that when participants are re-exposed to the same perturbation, adaptation occurs more rapidly (Kojima et al. 2004; Smith et al. 2006; Huang et al. 2011; Herzfeld et al. 2014; Leow et al. 2016).”

“The idea was proposed by Smith et al. (2006) to account for data obtained during adaptation of saccadic eye movements (Kojima et al. 2004) and was further tested in adaptation of reaching movements in response to a force field perturbation (Smith et al. 2006) and visuomotor rotations (Lee and…”

“has been observed under a variety of conditions [25,26,27].”

“A different group of subjects was studied on each paradigm to avoid the effects of savings [27–29].”

“Savings of learning [28,32,45] can be tested by having participants adapt to a perturbation, wash out the effects of learning, and then re-adapt to the same or a similar distortion.”

“Like rapid reacquisition, spontaneous recovery has also been observed for habituation (Prosser and Hunter, 1936), instrumental learning (Rescorla, 1997), and visuomotor adaptation (Kojima et al., 2004).”

“Because behavior during adaptation exhibits numerous characteristics that are shared in both arm and eye movements, including multiple time-scales of learning, spontaneous recovery (Kojima et al., 2004; Smith et al., 2006; Ethier et al., 2008), and modulation of error sensitivity (Hanajima et al.”

“Research into saccadic adaptation by primates with either a block of catch trials or an equivalent period of rest without visual inputs suggests that actual practice under null conditions is required to cause active unlearning and relearning of the novel condition (Kojima et al., 2004).”

“The initial models assumed a single state; however, the observation of spontaneous recovery during saccade adaptation in monkeys (Kojima et al. 2004) suggested that experience of error engaged multiple learning processes.”

“…underpinned, at least in part, by different mechanisms that probably rely on separate neural substrates (Straube et al., 1997; Noto et al., 1999; Kojima et al., 2004; Ethier et al., 2008; Hernandez et al., 2008; Panouillères et al., 2009; Zimmermann and Lappe, 2010; Schnier and Lappe, 2011,…”

“Other recent indirect evidence suggests that saccade lengthening and shortening rely on separate plasticity processes [Catz et al., 2008; Golla et al., 2008; Hernandez et al., 2008; Kojima et al., 2004; Panouilleres et al., 2009; Zimmermann and Lappe, 2009].”

“Another problem with the rationale of this comparison method is that numerous studies have now demonstrated differences in shortening and lengthening adaptive processes (e.g. Semmlow et al. 1989; Straube et al. 1997; Scudder et al. 1998; Noto et al. 1999; Alahyane et al. 2004; Kojima et al. 2004; Golla et al. 2008).”

“The multi-rate model correctly predicted learning dynamics occurring before and after the consolidation process (Kojima et al., 2004).”

“Indeed, there is evidence that the changes in gain consist of several components with different rate constants (Chen-Harris et al. 2008; Kojima et al. 2004), implying that the gain at the moment does not completely describe the state of the saccade machinery.”

“, 1996) and faster rates of adaptation on subsequent exposures (Kojima et al., 2004).”

“The existence of multiple components in pursuit learning is consistent with behavioral and computational evidence from other cerebellardependent motor learning behaviors (Boyden et al., 2004; Ethier et al., 2008; Kojima et al., 2004; Kording et al., 2007; Lee and Schweighofer, 2009; Medina et al., 2000; Smith et al.,…”

“However, with passage of time the behavior spontaneously reverts back and they once again produce the motor commands that they had originally learned (Criscimagna-Hemminger and Shadmehr, 2008; Kojima et al., 2004; Sarwary et al., 2018; Smith et al., 2006).”

“The dissociation between saccade and CDV produces differences between inward and outward learning Another central question in studies of saccade learning is why saccade amplitude adapts more to inward target steps than to outward target steps (Kojima et al., 2004; Panouillères et al., 2009; Pélisson et al., 2010).”

“A similar increase in learning rates is also observed in monkeys during saccade adaptation paradigms, if the monkey is left in the dark for a period of time (Kojima et al., 2004).”

“Similar to visuomotor [12] and saccadic adaptation [13], adaptation to novel dynamics exhibits savings [13–15], the ability of prior learning to speed subsequent relearning, spontaneous recovery of an initially adapted state after de-adaptation [16,17] and interference, a conflict of adaptation between similar tasks […”

“These two interpretations are nearly the same as those originally given by Ito (1970) for the VOR adaptation and by McCormick and Thompson (1984) for the classical conditioning of an eye-blink response.”

“Classic experiments on animal learning (e.g. Bouton, 1993; Rescorla, 2004) and recent ones on motor adaptation (Kojima et al., 2004; Smith, Ghazizadeh, & Shadmehr, 2006) have demonstrated how to test for the presence of multiple temporally tuned mechanisms.”

“Furthermore,savingsisa universalmetricforalllearningsystems,includingsemantic,perceptual,andmotorsystems(Ebbinghaus,1913;LiuandWeinshall, 2000;Medinaetal.,2001;Kojimaetal.,2004;Lebro´netal.,2004; Krakaueretal.,2006).”

“There is evidence for meta-learning, that is, short-term adaptation becoming more rapid with repeated training (Kojima et al., 2004; Wong and Shelhamer, 2011); there are even contentions of ‘cognitive’ modulation of short-term saccadic adaptation (Cotti et al., 2009; Srimal and Curtis, 2010).”

“This rebound is known as spontaneous recovery (Kojima et al. 2004; Smith et al. 2006), which slowly declines to baseline performance.”

“, classical P, PI, and PID control) and two-state gain specific models [25], [26].”

“Savings is a fundamental property of memory which can occur in a motor adaptation task [9].”

“…associated with reassessments of adaptation capacity, including the as-yet poorly understood phenomena of savings (in which readaptation occurs more rapidly than learning during the initial exposure to the adaptation paradigm; Haith and Krakauer 2013; Huang et al. 2011; Kojima et al. 2004).”

“Yet, savings also occurs in adaptation paradigms less likely to be influenced by explicit cognitive control [e.g. eye blink conditioning (Medina et al., 2001), saccades (Kojima et al., 2004)].”

“Research in force-field and saccade adaptation also has suggested the existence of two learning systems that operate on timescales of seconds and minutes (Ethier et al. 2008; Kojima et al. 2004; Smith et al. 2006).”

“We also compared the gain changes observed in the present study in monkey I to those elicited by 35% ISS in the same monkey in our previous study (Kojima et al., 2004).”

“As an experimental proof of the existence of multiple timescales in the short-term motor learning of the rVOR, we specifically sought to investigate whether it would show the phenomenon of spontaneous recovery (Ethier et al. 2008; Kojima et al. 2004; Myers and Davis 2002).”

“However, training effects were small and were only present in the gradual adaptation component, consistent with the effects of repetition on classical saccade adaptation (Kojima et al., 2004).”

“Yoshiki Iwamoto reported studies that investigated the effects of preceding learning on the speed of saccadic adaptation in monkeys (46,47).”

“3F; two268 sample t-test on last 10 adaptation epochs: t(30)=2.”

“Behavioral and neurophysiological studies in humans and monkeys showed that adaptive shortening and lengthening of saccade amplitude rely on separate mechanisms (Kojima et al., 2004; Catz et al., 2008; Ethier et al., 2008a; Golla et al., 2008; Panouillères et al., 2009).”

“It remains an open question how these 1004 putative subprocesses may map on distinct or overlapping anatomical structures, such as 1005 cerebellar cortices, deep cerebellar nuclei and extracerebellar structures [55,57,59,60,64,76-80].”