Differential roles for parietal and frontal cortices in fixed versus evolving temporal expectations: Dissociating prior from posterior temporal probabilities with fMRI.

The ability to predict when an event will occur allows us to respond optimally to that event. Temporal predictability can be either fixed (prior probability) or evolving (posterior probability), in which case it is dynamically updated as a function of the elapse of time itself ("hazard function"). We used fMRI to identify the brain regions involved in either form of temporal prediction, within a single experimental paradigm. Participants performed a cued reaction time (RT) task, in which the target appeared after one of four intervals ("foreperiods") that was either predictable (temporal condition) or variable (neutral condition). As expected, RTs were faster in temporal versus neutral conditions, indicating the behavioural benefit of fixed temporal predictability. RTs also got faster as a function of foreperiod in the neutral, but not temporal, condition, reflecting the evolving temporal predictability of the hazard function. We confirmed that left inferior parietal cortex was preferentially activated by the fixed temporal predictability of temporal (versus neutral) cues. Then, by directly comparing how activity varied as a function of foreperiod in the neutral versus time conditions, we identified the neural substrates of the changes in temporal probability defined by the hazard function, while simultaneously controlling for changes related simply to the elapse of time itself. Whole-brain fMRI analyses (independently confirmed by anatomically guided ROI analyses) showed that activity in left inferior parietal cortex tracked the evolving temporal probabilities of the hazard function. ROI analysis further revealed a similar role for right inferior frontal cortex. Our data highlight a key role for left parietal cortex in instantiating the behavioural benefits of temporal predictability, whether predictions are fixed or dynamically evolving.

Functionally dissociating temporal and motor components of response preparation in left intraparietal sulcus.

To optimise speed and accuracy of motor behaviour, we can prepare not only the type of movement to be made but also the time at which it will be executed. Previous cued reaction-time paradigms have shown that anticipating the moment in time at which this response will be made ("temporal orienting") or selectively preparing the motor effector with which an imminent response will be made (motor intention or "motor orienting") recruits similar regions of left intraparietal sulcus (IPS), raising the possibility that these two preparatory processes are inextricably co-activated. We used a factorial design to independently cue motor and temporal components of response preparation within the same experimental paradigm. By differentially cueing either ocular or manual response systems, rather than spatially lateralised responses within just one of these systems, potential spatial confounds were removed. We demonstrated that temporal and motor orienting were behaviourally dissociable, each capable of improving performance alone. Crucially, fMRI data revealed that temporal orienting activated the left IPS even if the motor effector that would be used to execute the response was unpredictable. Moreover, temporal orienting activated left IPS whether the target required a saccadic or manual response, and whether this response was left- or right-sided, thus confirming the ubiquity of left IPS activation for temporal orienting. Finally, a small region of left IPS was also activated by motor orienting for manual, though not saccadic, responses. Despite their functional independence therefore, temporal orienting and manual motor orienting nevertheless engage partially overlapping regions of left IPS, possibly reflecting their shared ontogenetic roots.

Hand-eye coordination relies on extra-retinal signals: evidence from reactive saccade adaptation.

Execution of a saccadic eye movement towards the goal of a hand pointing movement improves the accuracy of this hand movement. Still controversial is the role of extra-retinal signals, i.e. efference copy of the saccadic command and/or ocular proprioception, in the definition of the hand pointing target. We report here that hand pointing movements produced without visual feedback, with accompanying saccades and towards a target extinguished at saccade onset, were modified after gain change of reactive saccades through saccadic adaptation. As we have previously shown that the adaptation of reactive saccades does not influence the target representations that are common to the eye and the hand motor sub-systems (Cotti J, Guillaume A, Alahyane N, Pelisson D, Vercher JL. Adaptation of voluntary saccades, but not of reactive saccades. Transfers to hand pointing movements. J Neurophysiol 2007;98:602-12), the results of the present study demonstrate that extra-retinal signals participate in defining the target of hand pointing movements.

Adaptation of reactive and voluntary saccades: different patterns of adaptation revealed in the antisaccade task.

Sensorimotor adaptation restores and maintains the accuracy of goal-directed movements. It remains unclear whether these adaptive mechanisms modify actions by controlling peripheral premotor stages that send commands to the effectors and/or earlier processing stages involved in registration of target location. Here, we studied the effect of adaptation of saccadic eye movements, a well-established model of sensorimotor adaptation, in an antisaccade task. This task introduces a clear spatial dissociation between the actual target direction and the requested saccade direction because the correct movement direction is in the opposite direction from the target location. We used this requirement of a vector inversion to assess the level(s) of saccadic adaptation for two different types of adapted saccades. In two different experiments, we tested the transfer to antisaccades of the adaptation in one direction of reactive saccades to jumping targets and of scanning voluntary saccades within a target array. In the first experiment, we found that adaptation of reactive saccades transferred only to antisaccades in the adapted direction. In contrast, in the second experiment, adaptation of scanning voluntary saccades transferred to antisaccades in both the adapted and non-adapted directions. We conclude that adaptation of reactive saccades acts only downstream of the vector inversion required in the antisaccade task, whereas adaptation of voluntary saccades has a distributed influence, acting both upstream and downstream of vector inversion.

Adaptation of voluntary saccades, but not of reactive saccades, transfers to hand pointing movements.

Studying the transfer of visuomotor adaptation from a given effector (e.g., the eye) to another (e.g., the hand) allows us to question whether sensorimotor processes influenced by adaptation are common to both effector control systems and thus to address the level where adaptation takes place. Previous studies have shown only very weak transfer of the amplitude adaptation of reactive saccades--i.e., produced automatically in response to the sudden appearance of visual targets--to hand pointing movements. Here we compared the amplitude of hand pointing movements recorded before and after adaptation of either reactive or voluntary saccades, produced either in a saccade sequence task or in a single saccade task. No transfer to hand pointing movements was found after adaptation of reactive saccades. In contrast, a substantial transfer to the hand was obtained following adaptation of voluntary saccades produced in sequence. Large amounts of transfer between the two saccade types were also found. These results demonstrate that the visuomotor processes influenced by saccadic adaptation depend on the type of saccades and that, in the case of voluntary saccades, they are shared by hand pointing movements. Implications for the neurophysiological substrates of the adaptation of reactive and voluntary saccades are discussed.

Oculomotor plasticity: are mechanisms of adaptation for reactive and voluntary saccades separate?

Saccadic eye movements are permanently controlled and their accuracy maintained by adaptive mechanisms that compensate for physiological or pathological perturbations. In contrast to the adaptation of reactive saccades (RS) which are automatically triggered by the sudden appearance of a single target, little is known about the adaptation of voluntary saccades which allow us to intentionally scan our environment in nearly all our daily activities. In this study, we addressed this issue in human subjects by determining the properties of adaptation of scanning voluntary saccades (SVS) and comparing these features to those of RS. We also tested the reciprocal transfers of adaptation between the two saccade types. Our results revealed that SVS and RS adaptations disclosed similar adaptation fields, time course and recovery levels, with only a slightly lower after-effect for SVS. Moreover, RS and SVS main sequences both remained unaffected after adaptation. Finally and quite unexpectedly, the pattern of adaptation transfers was asymmetrical, with a much stronger transfer from SVS to RS (79%) than in the reverse direction (22%). These data demonstrate that adaptations of RS and SVS share several behavioural properties but at the same time rely on partially distinct processes. Based on these findings, it is proposed that adaptations of RS and SVS may involve a neural network including both a common site and two separate sites specifically recruited for each saccade type.