Parashkev Nachev

Functional role of the supplementary and pre-supplementary motor areas

The supplementary motor complex consists of the supplementary motor area, the supplementary eye field and the pre-supplementary motor area. In recent years, these areas have come under increasing scrutiny from cognitive neuroscientists, motor physiologists and clinicians because they seem to be crucial for linking cognition to action. However, theories regarding their function vary widely. This Review brings together the data regarding the supplementary motor regions, highlighting outstanding issues and providing new perspectives for understanding their functions.

Space and the parietal cortex.

Current views of the parietal cortex have difficulty accommodating the human inferior parietal lobe (IPL) within a simple dorsal versus ventral stream dichotomy. In humans, lesions of the right IPL often lead to syndromes such as hemispatial neglect that are seemingly in accord with the proposal that this region has a crucial role in spatial processing. However, recent imaging and lesion studies have revealed that inferior parietal regions have non-spatial functions, such as in sustaining attention, detecting salient events embedded in a sequence of events and controlling attention over time. Here, we review these findings and show that spatial processes and the visual guidance of action are only part of the repertoire of parietal functions. Although sub-regions in the human superior parietal lobe and intraparietal sulcus contribute to vision-for-action and spatial functions, more inferior parietal regions have distinctly non-spatial attributes that are neither conventionally ‘dorsal’ nor conventionally ‘ventral’ in nature.

Human Medial Frontal Cortex Mediates Unconscious Inhibition of Voluntary Action

Summary Within the medial frontal cortex, the supplementary eye field (SEF), supplementary motor area (SMA), and pre-SMA have been implicated in the control of voluntary action, especially during motor sequences or tasks involving rapid choices between competing response plans. However, the precise roles of these areas remain controversial. Here, we study two extremely rare patients with microlesions of the SEF and SMA to demonstrate that these areas are critically involved in unconscious and involuntary motor control. We employed masked-prime stimuli that evoked automatic inhibition in healthy people and control patients with lateral premotor or pre-SMA damage. In contrast, our SEF/SMA patients showed a complete reversal of the normal inhibitory effect—ocular or manual—corresponding to the functional subregion lesioned. These findings imply that the SEF and SMA mediate automatic effector-specific suppression of motor plans. This automatic mechanism may contribute to the participation of these areas in the voluntary control of action.

The role of the pre-supplementary motor area in the control of action

Although regions within the medial frontal cortex are known to be active during voluntary movements their precise role remains unclear. Here we combine functional imaging localisation with psychophysics to demonstrate a strikingly selective contralesional impairment in the ability to inhibit ongoing movement plans in a patient with a rare lesion involving the right pre-supplementary motor area (pre-SMA), but sparing the supplementary motor area (SMA). We find no corresponding delay in simple reaction times, and show that the inhibitory deficit is sensitive to the presence of competition between responses. The findings demonstrate that the pre-SMA plays a critical role in exerting control over voluntary actions in situations of response conflict. We discuss these findings in the context of a unified framework of pre-SMA function, and explore the degree to which extant data on this region can be explained by this function alone.

Human brain lesion-deficit inference remapped

Much of our knowledge of functional brain anatomy is based on lesion-deficit studies. Mah et al. show that the established methodology for conducting these — voxel-wise mass univariate inference — mislocalises function owing to complex correlations in natural patterns of damage across the brain; a problem soluble only by high-dimensional multivariate inference.

Attentional modulation of sensorimotor processes in the absence of perceptual awareness

Attention modulates visual perception and is generally considered inextricably linked with conscious awareness: we become aware of stimuli as we attend to them, and we attend to stimuli as we become aware of them. Recent evidence suggests that attention can also modulate the effects of stimuli that remain invisible, and a natural explanation is that attention enhances weak perceptual representations, bringing them closer to conscious threshold even if they do not reach that threshold. However, there is also the possibility that attention may modulate neural processes that are entirely separate from those supporting conscious perception: sensorimotor mechanisms that do not create awareness however much they are enhanced. Here we provide evidence in support of this second hypothesis by showing that attentional cueing can modulate the behavioral response to invisible stimuli in a way that is distinct from enhancing their visibility. We used a masked-prime paradigm that produces a negative or positive compatibility effect depending on the perceptual strength (duration or brightness) of the prime. We found that attention enhanced the effect of both visible and invisible primes and also increased the likelihood of detecting the prime (i.e., boosted perceptual strength). Crucially, the pattern of attentional influence on priming could not be explained by attentional modulation of the prime’s perceptual strength but was predicted by a direct attentional influence on the nonconscious priming process itself. Therefore, in addition to regulating what we perceive, attention seems to influence our behavior through sensorimotor processes that are not involved in conscious awareness.

Distinct cortical and collicular mechanisms of inhibition of return revealed with S cone stimuli

Visual orienting of attention and gaze are widely considered to be mediated by shared neural pathways, with automatic phenomena such as inhibition of return (IOR)--the bias against returning to recently visited locations--being generated via the direct pathway from retina to superior colliculus (SC). Here, we show that IOR occurs without direct access to the SC, by using a technique that employs stimuli visible only to short-wave-sensitive (S) cones. We found that these stimuli, to which the SC is blind , were quite capable of eliciting IOR, measured by traditional manual responses. Critically, however, we found that S cone stimuli did not cause IOR when saccadic eye movement responses were required. This demonstrates that saccadic IOR is not the same as traditional IOR, providing support for two separate cortical and collicular mechanisms of IOR. These findings represent a clear dissociation between visual orienting of attention and gaze.

Control over Conflict during Movement Preparation: Role of Posterior Parietal Cortex

Summary Flexible behavior in humans often requires that rapid choices be made between conflicting action plans. Although much attention has focused on prefrontal regions, little is understood about the contribution of parietal cortex under situations of response conflict. Here we show that right parietal damage associated with spatial neglect leads to paradoxical facilitation (speeding) of rightward movements in the presence of conflicting leftward response plans. These findings indicate a critical role for parietal regions in action planning when there is response competition. In contrast, patients with prefrontal damage have an augmented cost of conflict for both leftward and rightward movements. The results suggest involvement of two independent systems in situations of response conflict, with right parietal cortex being a crucial site for automatic activation of competing motor plans and prefrontal regions acting independently to inhibit action plans irrelevant to current task goals.

Role of the human supplementary eye field in the control of saccadic eye movements.

The precise function of the supplementary eye field (SEF) is poorly understood. Although electrophysiological and functional imaging studies are important for demonstrating when SEF neurones are active, lesion studies are critical to establish the functions for which the SEF is essential. Here we report a series of investigations performed on an extremely rare individual with a highly focal lesion of the medial frontal cortex. High-resolution structural imaging demonstrated that his lesion was confined to the region of the left paracentral sulcus, the anatomical locus of the SEF. Behavioural testing revealed that the patient was significantly impaired when required to switch between anti- and pro-saccades, when there were conflicting rules governing stimulus–response mappings for saccades. Similarly, the results of an arbitrary stimulus–response associative learning task demonstrated that he was impaired when required to select the appropriate saccade from conflicting eye movement responses, but not for limb movements on an analogous manual task. When making memory-guided saccadic sequences, the patient demonstrated hypometria, like patients with Parkinsons disease, but had no significant difficulties in reproducing the order of saccades correctly on a task that emphasized accuracy with a wide temporal segregation between responses. These findings are consistent with the hypothesis that the SEF plays a key role in implementing control when there is conflict between several, ongoing competing saccadic responses, but not when eye movements need to be made accurately in sequence.

Cognition and medial frontal cortex in health and disease

Purpose of reviewRecent work on the role of the medial frontal cortex in cognition and its involvement in neurological disorders is critically reviewed. Recent findingsThe highly influential notion of conflict monitoring by the anterior cingulate has been called into question by monkey single-cell neurophysiology and lesion studies in monkeys and humans. An alternative role for this region in adapting behaviour in response to changing demands over time is gaining support. By contrast, the more dorsally placed presupplementary motor area and supplementary eye field have been implicated in direct executive control in situations of response conflict. Although more rostral medial areas have been linked to complex cognitive operations involving references to the self, conceptual obstacles make the evidence difficult to interpret. The role of the orbitofrontal cortex in guiding action based on value has been reinforced. SummaryThe role of the medial frontal cortex in cognition continues to generate both interest and controversy. A few striking discrepancies between data from functional imaging and interventional techniques illustrate the hazards of drawing strong conclusions from merely correlative evidence. More broadly, a case can be made for tempering the empirical enthusiasm here with a little more theoretical restraint.