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).”

“Yet, following passage of time, and without presence of errors, the saccade endpoints revert back toward the previously adapted state [4,5].”

“Email: katharina.bey@ukbonn.de Backward and forward adaptation may rely on separate mechanisms (Catz et al., 2008; Ethier et al., 2008; Golla et al., 2008; Kojima et al., 2004; Panouillères et al., 2009).”

“The term ’savings’ refers to the ability to remember a previously-learned adaptation, 266 observed as an instant recall of the previously-learned adaptation [12,19], or as 267 accelerated re-learning [20]; in the case of instant recall, the phenomenon is often called 268 ’switching’.”

“…difficult and slower to develop than adaptive shortening (Miller et al., 1981; Straube and Deubel, 1995; Straube et al., 1997; Noto et al., 1999; Robinson et al., 2003; Alahyane and Pélisson, 2004; Kojima et al., 2004; Panouillères et al., 2009, 2012a,b, 2013, 2015; Zimmermann and Lappe, 2010).”

“(2006) is a simple descriptive model that can account for a series of motor learning features, like savings (Kojima et al., 2004; Ebbinghaus, 2013), anterograde interference (Sing and Smith, 2010), lack of adaptation (Krakauer et al.”

“when subjects are re-exposed to the same rotation or force field after some time interval, adaptation occurs more rapidly [29,30].”

“E) Double reversal paradigm with darkness, reprinted from [12].”

“This capacity, referred to as adaptation, has been demonstrated across a wide variety of behaviors including eye movements (Kojima et al., 2004; Wong & Shelhamer, 2011), reaching movements (Hadjiosif & Smith, 2015; Krakauer et al., 2000, 2005; Shadmehr & Mussa-Ivaldi, 1994; Smith et al., 2006),…”

“…(Ebbinghaus, 1913), savings has since come to be recognized as a rather ubiquitous phenomenon, including many examples in the motor learning literature (Milner, 1962; Medina et al., 2001; Walker et al., 2002; Kojima et al., 2004; Doyon et al., 2009; Mawase et al., 2014; Coltman et al., 2019).”

“Kojima et al. (2004) argue, based on consecutive size-decreasing and size-increasing STSAs, that size-increasing and size-decreasing STSA rely on distinct mechanisms.”

“Therefore, in later blocks, adaptation was facilitated by earlier blocks like described in [6].”

“First, an immediate fact also confirmed experimentally [11] is that they cannot arise from a first-order LTI model.”

“In non-human primate studies monkeys’ were sitting in a dark room where they were able to sleep [6] or their heads were covered [21].”

“Support for dual-rate learning has now been reported for adaptation of reaches in force fields [5–7] and under visuomotor perturbations [2,3,8] as well as for saccadic gain adaptation [9,10].”

“Examples include saccades with an intersaccadic step of the target [11]; the visuomotor rotation experiment with fast arm reaches [29]; and throwing darts while looking through prism glasses [18].”

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

“Third, meta-learning can occur in as little as minutes to hours of training 4, 20, 21 in experiment tasks, possibly because these tasks employ simple perturbation on familiar movements ( e.g. , learning how to change the direction of arm-reach to counteract visual rotation and touch a target…”

“Differences in adaptation levels between target step directions have been reported before [12, 26, 58, 59].”

“[ 19 ], monkeys learned to increase the gain of the saccade to a certain point and then decrease back to the original gain.”

“Therefore, the adaptation that brings the amplitude to the baseline state includes a component that modifies the amplitude according to visual error signals rather than being the consequence of a simple passive return to the baseline state (Ethier et al. 2008; Kojima et al. 2004).”

“Furthermore, their theoretical framework used error-dependent learning rate to explain the phenomenon of “savings” and “meta-learning,” where prior experience can facilitate re-adaptation (Kojima et al., 2004; Braun et al., 2009; Malone et al., 2011; Turnham et al., 2012; Sarwary et al., 2013; Herzfeld et al., 2014).”

“…that is observed across several motor effectors: the reaching system (Smith et al., 2006; Zarahn et al., 2008; Leow et al., 2013; Haith et al., 2015; Coltman et al., 2020; Yin & Wei, 2020), walking (Mawase et al., 2014; Day et al., 2018), and even the oculomotor system (Kojima et al., 2004).”

“Examples include saccades with an intersaccadic step of the target [121]; the visuomotor rotation experiment with fast arm reaches [122, 123]; and throwing darts while looking through prism glasses [124].”

“A key phenomenon observed in these adaptation paradigms is savings, wherein error reduction occurs more rapidly (i.e., in fewer trials) upon re-exposure to a previously experienced perturbation (Kojima et al. 2004 ; Krakauer et al. 2005 ; Smith et al. 2006 ; Zarahn et al. 2008).”

“By using this procedure, we followed the traditional notion of a gain adaptation (Deubel et al., 1986, 1987; Kojima et al., 2004).”

“This sudden jump is caused by the preserved 224 memory of motor compensated at the beginning of the relearning phase and the same 225 phenomenon in human adaptation is referred to as ‘savings’ [34, 35].”

“Many studies have shown that learning occurs faster when people experiences similar errors repeatedly (Herzfeld et al., 2014; Kojima et al., 2004; Leech et al., 2018; Malone et al., 2011; Medina et al., 2001; Roemmich and Bastian, 2015), a phenomenon termed ‘savings’ (or ‘retention’, if the…”

“, savings) has been reported in the earlier reports (Krakauer et al., 1999; Kojima et al., 2004; Burge et al., 2008; Huang et al., 2011; Leow et al., 2012).”

“These two processes, which together contribute to the update of the internal model, do not only explain spontaneous recovery (Ethier et al., 2008), but also behavioral observations such as faster re-relearning/re-adaptation (Kojima et al., 2004) and interference (Davidson & Wolpert, 2004).”

“The subsequent re-exposure to the original task with resistive pelvis force may have solidified the previously formulated internal model (Kojima et al., 2004; Krakauer & Shadmehr, 2006).”

“Savings suppression after a long washout of a special kind was observed earlier in (Kitago et al. 2013; Kojima, Iwamoto, and Yoshida 2004).”

“The idea that washout impacts savings qualitatively aligns with prior work by Kojima et al. 9 , which demonstrated that savings in the oculomotor system are sensitive to the duration of washout: when the duration of the washout phase is increased, the learning rate during the re-exposure phase…”

“4 However, cues have limitations.”

“An interesting approach was used by Kojima et al. (2004).”