The neural basis of meta-volition

Volition is the power to act beyond simple, automatic responses. We can act voluntarily because we can choose to act otherwise than immediate, external circumstances dictate. But we can also choose to allow ourselves to be led automatically by events around us. The neural basis of this higher power to suspend volition— which we term meta-volition—is unknown. Here we show that inter-individual differences in meta-volition are reflected in extensive, highly lateralised differences in right frontal white matter as indexed by diffusion tensor imaging. Paradoxically, participants with enhanced white matter optimality in these regions are less able to exercise meta-volition, finding it harder to suspend volition. This suggests volition is dependent less on any hierarchical system of meta-volitional control than on the extent to which an extensive network subserving higher volitional powers is competitively dominant over others. A fundamentally parallel neural organisation of human voluntary action at the highest level is thereby implied

Human hippocampal CA3 damage disrupts both recent and remote episodic memories

Neocortical-hippocampal interactions support new episodic (event) memories, but there is conflicting evidence about the dependence of remote episodic memories on the hippocampus. In line with systems consolidation and computational theories of episodic memory, evidence from model organisms suggests that the cornu ammonis 3 (CA3) hippocampal subfield supports recent, but not remote, episodic retrieval. In this study, we demonstrated that recent and remote memories were susceptible to a loss of episodic detail in human participants with focal bilateral damage to CA3. Graph theoretic analyses of 7.0-Tesla resting-state fMRI data revealed that CA3 damage disrupted functional integration across the medial temporal lobe (MTL) subsystem of the default network. The loss of functional integration in MTL subsystem regions was predictive of autobiographical episodic retrieval performance. We conclude that human CA3 is necessary for the retrieval of episodic memories long after their initial acquisition and functional integration of the default network is important for autobiographical episodic memory performance

Distractor-dependent frontal neglect.

The effect of distractor load on visual search was examined in a patient with visual neglect following infarction of the right frontal lobe. The spatial extent of his left-sided neglect was modified greatly by changing stimulus attributes. When targets were highly discriminable compared to distractors, or distractor density was low, or when the subject was asked to cancel distractors as well as targets, he was able to direct his search to the extreme left of search arrays and there was little or no evidence of neglect. By contrast, similar changes in distractor load had little or no effect on the neglect of a patient with a fronto-parietal lesion. These findings suggest that distractability towards ipsilesional stimuli may be an important component of neglect in individuals with only frontal lobe injury

Volition and eye movements.

Although the conceptual distinction between voluntary and automatic acts seems intuitively obvious, its neural basis remains opaque. Assigning volition--or some paraphrase such as action selection--to discrete parts of the brain arguably tells us nothing about what volition actually is in neural terms. Equally, exploring the relative sensitivity of discrete brain areas to manipulations of action choice, including its asymptote--free choice--would only be informative if voluntary processes could thereby be reliably isolated. Unfortunately, such manipulations are subject to ineliminable confounds, such as the complexity of the underlying condition-action associations. Here we propose an adaptation of a classic oculomotor task--saccadic choice with asynchronous targets--where the processes engaged in free choice manifest as interference in the performance of an automatic task, thereby circumventing the difficulties in parameterising volition. We suggest that this task may be useful in probing deficits in voluntary action in pathological states

The role of visual salience in directing eye movements in visual object agnosia

When we look at a scene our scanning eye movements are not random [1]. Remarkably, different observers look at similar points in a given image. One explanation is that our understanding of the scene controls the paths our eyes take - so called 'top-down' control. An alternative possibility is that the visual system uses low-level 'bottom-up' features, such as edges, contrast or boundaries, to determine where the eyes land [2-4]. Fixated locations have been shown to contain higher values of 'low-level' visual features than non-fixated ones [2,3,5]. Moreover, biologically-plausible, low-level computational saliency maps produce scanpaths similar to those traced by human eye movements [4]. However, there is controversy about the role of bottom-up versus top-down control of eye movements [6,7]. To test between these possibilities, we measured the eye movements of two patients with visual agnosia who are severely impaired at recognizing objects or scenes, and therefore diverge from healthy volunteers in their understanding of the scene. Despite this, we found that, when inspecting a picture, their eyes look at the same locations as healthy individuals for the first few fixations. Initial eye movements, during a recognition task, therefore, are not affected by an impaired explicit understanding of the scene. © 2009 Elsevier Ltd. All rights reserved

Eye movements in visual search indicate impaired saliency processing in Parkinson's disease

Previous studies have produced contradictory evidence on the nature of the visual search impairment in patients with Parkinson's disease (PD). Eye movements were measured during multi-target search in nine individuals with mild-to-moderate PD. Subjects were asked to click on a response button whenever they judged they were fixating a target for the first time. Compared to age-matched healthy volunteers, PD patients were impaired at efficient search (detecting “+”s amongst “L”s) but not inefficient search (“T”s amongst “L”s). However, these patients had normal memory for locations as indexed by their rate of re-clicking on previously inspected locations. We suggest that the pattern of gaze for efficient search may reflect impaired saliency processing in PD

Control of voluntary and reflexive saccades.

The latency of 'reflexive' saccades (made in response to peripheral visual stimuli) was compared to that of 'voluntary' saccades performed in anti-saccade and symbolically cued paradigms. Manipulation of visual events at fixation was carefully controlled across all conditions. Reflexive saccade latency was significantly faster than the latency of all forms of voluntary saccades. Importantly, the latency of saccades made after presentation of a symbolic cue at central fixation (voluntary arrow-cue condition) was greater than that made in the anti-saccade paradigm that requires suppression of a reflexive response. It is suggested that the increase in latency of saccades made in the voluntary arrow-cue condition may reflect differences in programming a 'When' trigger signal for saccades made in the absence of a peripheral stimulus

Motor role of human inferior parietal lobe revealed in unilateral neglect patients.

The exact role of the parietal lobe in spatial cognition is controversial. One influential hypothesis proposes that it subserves spatial perception, whereas other accounts suggest that its primary role is to direct spatial movement. For humans, it has been suggested that these functions may be divided between inferior and superior parietal lobes, respectively. In apparent support of a purely perceptual function for the inferior parietal lobe (IPL), patients with lesions to this structure, particularly in the right hemisphere, exhibit unilateral spatial neglect (deficient awareness for the side of space opposite to that of their lesion). Here we show that patients with right IPL lesions also have a specific difficulty in initiating leftward movements towards visual targets on the left side of space. This motor impairment was not found in neglect patients with frontal lesions, contrary to previous proposals that motor aspects of neglect are particularly associated with anterior damage. Our results suggest that the human IPL operates as a sensorimotor interface, rather than subserving only perceptual functions

Distinguishing sensory and motor biases in parietal and frontal neglect.

Left neglect after right-hemisphere damage may involve perceptual and/or motor impairments. Here we discuss the limitations of previous attempts to separate these components, and introduce a new method. Six neglect patients (three with right inferior parietal lesions and three with right inferior frontal lesions) moved their right hand to a target light, which appeared unpredictably on either the left or the right of central fixation. The target appeared alone or with a distractor light in the opposite hemifield. Any directional motoric bias was measured by comparing reaches from a central start position with those for the same visual displays, but starting from the left of both possible targets (thus requiring only rightward reaches) or from the right (requiring only leftward reaches). All patients were slower to initiate reaches to left than right targets from a central start, which could reflect perceptual and/or motor biases. Critically, in the parietal neglect group only, initiation speed for left targets improved when a rightward reach was required to these (from a left start) rather than a leftward reach. This suggests a deficit in programming leftward movements into left hemispace, in addition to any visual impairment, for parietal neglect. A control task confirmed that this effect of start position was due to the associated change in reach direction and not to afferent inputs from the hand as it rested at the start position. Frontal neglect patients were slow to execute reaches to left targets, regardless of movement direction. Right visual distractors slowed visual reaction times to left targets more than vice versa in frontal neglect patients, and likewise for reach execution times in parietal neglect patients, suggesting that visual distractors on the neglected side have less impact. Distractor effects were unaffected by start position in the frontal neglect group (suggesting a perceptual basis), but distractors slowed reach initiation in the parietal neglect group only from left and central starts. Taken together, these findings demonstrate a directional motor component to parietal but not frontal neglect, and suggest that in man the inferior parietal lobe plays a role not only in perception but also in the programming of selective reaches. These conclusions are related to recent single-unit data from the monkey parietal lobe