Using the McLaughlin (1967)
task, after fixation of a central visual target (T0) a saccade target was presented (T1). Upon saccade initiation this target was turned off and another target (T2) closer to (backward adaptation) or further from (forward adaptation) T0 was illuminated. The introduction of this visual error by moving surreptitiously the visual target during the primary saccade led to systematic reductions or increases in saccade amplitudes. Adaptive changes in saccade amplitudes persisted even when the second target was not illuminated (probe trials) and no visual feedback was provided to the subject. Predictions of two alternative hypotheses about the role of the superior colliculus in mediation of this change in motor output (despite identical sensory inputs) were tested. As described above, these alternatives make differential predictions concerning the locus of motor-related activity in the SC map of saccade vector. Data from 37 SC neurons in the deeper layers were recorded before and during backward adaptation. Thirteen neurons were recorded during forward adaptation. All data in our sample were consistent with the hypothesis that the locus of SC activity remained unchanged during adaptation despite changes in saccade amplitude. Data were inconsistent with the hypothesis that the locus of SC activity is re-mapped during adaptation. This is a strong indication that the motor command produced by the SC is not specifying the amplitude and direction of the observed saccade during short-term adaptation produced using the McLaughlin task. Instead the SC motor command appears to specify a desired movement to the location of the T1 target. Some additional signal must reshape or bypass the collicular output in order to alter the amplitudes of observed movements.
Based on differences in the kinematics of saccades during backward (‘gain-down’) but not during forward (‘gain-up’) adaptation Ethier and colleagues (Ethier et al. 2008
) suggest that different neural mechanisms produce the observed changes in saccade amplitude. These authors note that during backward adaptation, saccade velocities are reduced and durations slightly increased when compared to amplitude- and direction-matched movements made before adaptation (note that this is not a consistent finding across adaptation studies (for comparison see (Fitzgibbon et al. 1986
; Straube and Deubel 1995
; Frens and Van Opstal 1997
; Alahyane and Pelisson 2005
)). Ethier and colleagues suggest that reduction in adapted saccade velocity could indicate a change in the dynamic controller (saccadic burst generator) that is hypothesized to specify saccade kinematics. During forward adaptation they see no changes in saccade kinematics and suggest that amplitude changes in this case are the result of re-mapping: a change in the specification of the desired saccade vector. Our results indicating no change in SC activity during backward or forward adaptation are inconsistent with the hypothesis that the SC motor command is altered during either forward or backward adaptation.
Frens and van Opstal (1997)
reported that a subset (11/30) of neurons recorded in the deeper SC layers had activity that was unaltered during adaptation. In part due to small changes in movement amplitude during adaptation and the variability on saccade size during and after adaptation, results for the other reported neurons were ambiguous. It is less clear whether our data coincide with the results of another report of the role of the SC in saccadic adaptation (Takeichi et al. 2007
). In this report, two measures of neural activity were used to assess changes in the SC command during adaptation. In one measure the number of action potentials in the saccade-related burst (defined as action potentials that occurred when discharge rates were above 40 sp/s) was compared before and after both forward and backward adaptation. Due primarily to an increase in the number of spikes before movement onset during backward adaptation these authors report that SC activity is altered during adaptation. This measure of neural activity in the SC may not bear directly on the issue at hand: whether or not the SC is specifying the vector of the observed saccade or the vector of the planned saccade to the T1 location. The number of spikes in the motor-related burst could change without altering the location
of the active population within the map of saccade vector. If this were the case, the increased or decreased number of spikes would not necessarily contribute to an altered movement vector and no conclusions about whether the T1 location is ‘re-mapped’ in the SC or not would be possible. In a second measure of SC activity, Takeichi and colleagues analyzed movement fields before and after saccadic adaptation. During backward adaptation ~50% of their neurons had altered movement fields after adaptation. Note that in some examples the portion of the movement field that was altered after adaptation was not related to movements to the T1 location nor to the amplitude and direction of the post-adaptation saccades to T1. Nonetheless the authors interpret their altered movement fields as evidence that the SC is encoding the observed changes in saccade amplitude. However, as shown above, dramatic differences in movement fields before and after adaptation are predicted by the hypothesis that the SC does not
specify the vector of the observed (post-adaptation) saccade. Rather, altered movement fields (for example , and ) are consistent with the notion that despite large changes in saccade amplitude during adaptation, the locus of motor activity within the SC map of saccade vector does not
change systematically. The data presented here indicate that the SC continues to request a saccade to the T1 target location and that adaptation-induced changes in saccade amplitude are a result of altered activity elsewhere in the saccade generating circuitry.
One different method also employed to address the role of the SC in saccadic adaptation has been to evoke saccades by electrical stimulation. Movements evoked in this way have been reported to be unaltered by saccadic adaptation (Fitzgibbon et al. 1986
; Melis and vanGisbergen 1996
) suggesting that observed changes in saccade amplitude are not the result of an additional signal that is universally applied to the collicular output via some downstream change. This result appears to be in conflict with the results illustrated above. However, the interpretation of the electrical stimulation data depends on the assumption that stimulation of the SC recruits the identical network of neurons that is involved in producing the adapted movements. This is a difficult assumption to evaluate, and of course in its most rigorous incarnation is clearly false since visual pathways are not activated as part of a visuo-motor behavior during collicular electrical stimulation. Also, if the SC-NRTP-cerebellum-PPRF circuit is a critical loop in affecting adaptation of visual-motor behaviors, it may be that SC stimulation is failing to involve these circuits appropriately during adaptation. Additionally, using slightly different methods than those cited above, the opposite result of electrical stimulation during adaptation has also been reported (Edelman and Goldberg 2002
). In this case electrically evoked saccades were altered after saccade adaptation, suggesting that identical collicular output is altered by changes to downstream structures during the adaptive process. The data presented in the present report indicate that the SC does not alter its activity during saccade adaptation and that the observed changes either bypass the SC or are implemented downstream from the colliculus. The precise nature and location of these adaptive changes requires further study.
The data presented here are not the only examples of circumstances in which the locus of superior colliculus activity can be dissociated from the metrics of observed movements. During saccades to remember target locations there is a systematic upward shift in movement directions. Activity in the SC, however, apparently encodes the amplitude and direction of the desired movement and the additional upward component of observed movements is added below the level of the SC (Stanford and Sparks 1994
The cerebellum has been implicated as a key element in saccadic adaptation (Ritchie 1976
; Optican and Robinson 1980
; Robinson and Fuchs 2001
; Robinson et al. 2002
; Scudder and McGee 2003
). Cerebellar lobes VI and VII and the caudal fastigial nucleus (cFN) receive direct and indirect inputs from a variety of saccade related structures (for review see (Voogd and Barmack 2006
)). In turn, the cFN projects to brainstem regions involved in saccadic control. One route from the SC to cerebellum is via the nucleus reticularis tegmenti pontis (NRTP), and neural activity in NRTP has been reported to change during saccadic adaptation (Takeichi et al. 2005
). The cFN also projects directly back to the NRTP; NRTP also receives input from a variety of cortical and subcortical structures including the frontal and supplementary eye fields and parietal cortex (for review see (Thier and Mock 2006
)). Anatomically NRTP is well-placed to integrate sensory information related to target positions and affect the execution of saccades via the cerebellum and brainstem burst generator.
During adaptation an increase in discharge before the movement starts has been reported to occur in the SC (Takeichi et al. 2007
), in NRTP (Takeichi et al. 2005
) and in the caudal fastigial nucleus (Inaba et al. 2003
; Scudder and McGee 2003
). The mechanism for altering saccade vectors as a result of pre-movement activity, particularly in the SC is not clear as the locus of SC activity does not appear to change during adaptation. In contrast, an increase in pre-movement activity could result from repeated presentation of a single saccade target. In most saccade adaptation studies, once adaptation begins, only trials using T1 as the primary saccade target are presented. After several hundred presentations of the same target, without randomly interleaving trials to other locations, one might expect anticipatory activity in (for example) the SC. Increased early activity in SC, NRTP, and cFN might be a result of the target presentation scheme rather than an important element in producing the adaptive changes in saccade amplitude. The neural mechanisms that result in altered saccade metrics and the roles of NRTP, cFN and other saccade-related structures remain to be determined. The data presented above, however, are inconsistent with re-mapping of the saccade vector at the level of the superior colliculus.