Double Dissociation of the roles of the left and right prefrontal cortices in anticipatory regulation of action

Authors:

• Stephanie Ries

• Ian Greenhouse

• Nina F. Dronkers

• Kathleen Y. Haaland

• Robert T. Knight

Date: 2014

DOI: 10.1016/j.neuropsychologia.2014.08.026

PubMed: 25201047

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Abstract:

Recent actions can benefit or disrupt our current actions and the prefrontal cortex (PFC) is thought to play a major role in the regulation of these actions before they occur. The left PFC has been associated with overcoming interference from past events in the context of language production and working memory. The right PFC, and especially the right IFG, has been associated with preparatory inhibition processes. But damage to the right PFC has also been associated with impairment in sustaining actions in motor intentional disorders. Moreover, bilateral dorsolateral PFC has been associated with the ability to maintain task-sets, and improve the performance of current actions based on previous experience. However, potential hemispheric asymmetries in anticipatory regulation of action have not yet been delineated. In the present study, patients with left (n=7) vs. right (n=6) PFC damage due to stroke and 14 aged- and education-matched controls performed a picture naming and a verbal Simon task (participants had to say "right" or "left" depending on the color of the picture while ignoring its position). In both tasks, performance depended on the nature of the preceding trial, but in different ways. In the naming task, performance decreased if previous pictures were from the same rather than from different semantic categories (i.e., semantic interference effect). In the Simon task, performance was better for both compatible (i.e., response matching the position of the stimulus) and incompatible trials when preceded by a trial of the same compatibility (i.e. Gratton effect) relative to sequential trials of different compatibility. Left PFC patients were selectively impaired in picture naming; they had an increased semantic interference effect compared to both right PFC patients and aged-matched controls. Conversely, right PFC patients were selectively impaired in the Simon task compared to controls or left PFC patients; they showed no benefit when sequential trials were compatible (cC vs. iC trials) or a decreased Gratton effect. These results provide evidence for a double dissociation between left and right PFC in the anticipatory regulation of action. Our results are in agreement with a preponderant role of the left PFC in overcoming proactive interference from competing memory representations and provide evidence that the right PFC, plays a role in sustaining goal-directed actions consistent with clinical data in right PFC patients with motor intentional disorders.

Role of the lateral prefrontal cortex in speech monitoring

Authors:

• Stephanie Ries

• Kira Xie

• Kathleen Y. Haaland

• Nina F. Dronkers

• Robert T. Knight

Date: 2013

DOI: 10.3389/fnhum.2013.00703

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Abstract:

The role of lateral prefrontal cortex (LPFC) in speech monitoring has not been delineated. Recent work suggests that medial frontal cortex (MFC) is involved in overt speech monitoring initiated before auditory feedback. This mechanism is reflected in an event- related potential (ERP), the error negativity (Ne), peaking within 100 ms after vocal-onset. Critically, in healthy individuals the Ne is sensitive to the accuracy of the response; it is larger for error than correct trials. By contrast, patients with LPFC damage are impaired in non-verbal monitoring tasks showing no amplitude difference between the Ne measured in correct vs. error trials. Interactions between the LPFC and the MFC are assumed to play a necessary role for normal action monitoring. We investigated whether the LPFC was involved in speech monitoring to the same extent as in non-linguistic actions by comparing performance and EEG activity in patients with LPFC damage and in aged-matched controls performing linguistic (Picture Naming) and non-linguistic (Simon) tasks. Controls did not produce enough errors to allow the comparison of the Ne or other ERP in error vs. correct trials. PFC patients had worse performance than controls in both tasks, but their Ne was larger for error than correct trials only in Naming. This task-dependent pattern can be explained by LPFC-dependent working-memory requirements present in non-linguistic tasks used to study action monitoring but absent in picture naming. This suggests that LPFC may not be necessary for speech monitoring as assessed by simple picture naming. In addition, bilateral temporal cortex activity starting before and peaking around vocal-onset was observed in LPFC and control groups in both tasks but was larger for error than correct trials only in Naming, suggesting the temporal cortex is associated with on-line monitoring of speech specifically when access to lexical representations is necessary.

Ipsilateral trajectory control is related to contralesional paralysis after left hemisphere damage

Authors:

• Kathleen Y. Haaland

• Sydney Y. Schaefer

• Robert T. Knight

• John Adair

• Alvaro Magalhaes

• Joseph Sadek

• Robert L. Sainburg

Date: 2009

DOI: 10.1007/s00221-009-1836-z

PubMed: 19479246

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Abstract:

We have recently shown ipsilateral dynamic deficits in trajectory control are present in left hemisphere damaged (LHD) patients with paresis, as evidenced by impaired modulation of torque amplitude as response amplitude increases. The purpose of the current study is to determine if these ipsilateral deficits are more common with contralateral hemiparesis and greater damage to the motor system, as evidenced by structural imaging. Three groups of right-handed subjects (healthy controls, LHD stroke patients with and without upper extremity paresis) performed single-joint elbow movements of varying amplitudes with their left arm in the left hemispace. Only the paretic group demonstrated dynamic deficits characterized by decreased modulation of peak torque (reflected by peak acceleration changes) as response amplitude increased. These results could not be attributed to lesion volume or peak velocity as neither variable differed across the groups. However, the paretic group had damage to a larger number of areas within the motor system than the non-paretic group suggesting that such damage increases the probability of ipsilesional deficits in dynamic control for modulating torque amplitude after left hemisphere damage.

Hemispheric asymmetries for kinematic and positional aspects of reaching

Authors:

• Kathleen Y. Haaland

• Jillian L. Prestopnik

• Robert T. Knight

• Roland R. Lee

Date: 2004

PubMed: 15033898

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Abstract:

Kinematic analyses of reaching have suggested that the left hemisphere is dominant for controlling the open loop component of the movement, which is more dependent on motor programmes; and the right hemisphere is dominant for controlling the closed loop component, which is more dependent on sensory feedback. This open and closed loop hypothesis of hemispheric asymmetry would also predict that advance planning should be dependent on the left hemisphere, and on-line response modification, which defines closed loop processes, should be dependent on the right hemisphere. Using kinematic analyses of reaching in patients with left or right hemisphere damage (LHD or RHD), we examined the ability: (i) to plan reaching movements in advance by examining changes in reaction time (RT) when response amplitude and visual feedback were cued prior to the response; and (ii) to modify the response during implementation when target location changed at the RT. Performance was compared between the stroke groups, using the ipsilesional arm, and age-matched control groups using their right (RNC) or left (LNC) arm. Aiming movements to a target that moved once or twice, with the second step occurring at the RT, were performed with or without visual feedback of hand position. There were no deficits in advance planning in either stroke group, as evidenced by comparable group changes in RT with changes in amplitude and visual feedback. Response modification deficits were seen for the LHD group in secondary velocity only. In addition, LHD produced slower initial peak velocity with prolongation of the deceleration phase and faster secondary peak velocities, and the RHD group produced deficits in final error only. These differences are more consistent with the dynamic dominance hypothesis, which links left hemisphere specialization to movement trajectory control and right hemisphere specialization to position control, rather than to global deficits in open and closed loop processing.

Neural representations of skilled movement

Authors:

• Kathleen Y. Haaland

• Deborah L. Harrington

• Robert T. Knight

Date: 2000

PubMed: 11050030

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Abstract:

The frontal and parietal cortex are intimately involved in the representation of goal-directed movements, but the crucial neuroanatomical sites are not well established in humans. In order to identify these sites more precisely, we studied stroke patients who had the classic syndrome of ideomotor limb apraxia, which disrupts goal-directed movements, such as writing or brushing teeth. Patients with and without limb apraxia were identified by assessing errors imitating gestures and specifying a cut-off for apraxia relative to a normal control group. We then used MRI or CT for lesion localization and compared areas of overlap in those patients with and without limb apraxia. Patients with ideomotor limb apraxia had damage lateralized to a left hemispheric network involving the middle frontal gyrus and intraparietal sulcus region. Thus, the results revealed that discrete areas in the left hemisphere of humans are critical for control of complex goal-directed movements.

Spatial deficits in ideomotor limb apraxia: a kinematic analysis of aiming movements

Authors:

• Kathleen Y. Haaland

• Deborah L. Harrington

• Robert T. Knight

Date: 1999

PubMed: 10356068

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Abstract:

Ideomotor limb apraxia is a classic neurological disorder manifesting as a breakdown in co-ordinated limb control with spatiotemporal deficits. We employed kinematic analyses of simple aiming movements in left hemisphere- damaged patients with and without limb apraxia and a normal control group to examine preprogramming and response implementation deficits in apraxia. Damage to the frontal and parietal lobes was more common in apraxics, but neither frontal nor parietal damage was associated with different arm movement deficits. Limb apraxia was associated with intact preprogramming but impaired response implementation. The response implementation deficits were characterized by spatial but not temporal deficits, consistent with decoupling of spatial and temporal features of movement in limb apraxia. While the apraxics’ accuracy was normal when visual feedback was available, it was impaired when visual feedback of either target location or hand position was unavailable. This finding suggests that ideomotor limb apraxia is associated with disruption of the neural representations for the extrapersonal (spatial location) and intrapersonal (hand position) features of movement. The non-apraxic group’s normal kinematic performance demonstrates that the deficits demonstrated in the apraxic group are not simply a reflection of left hemisphere damage per se.

Cortical networks underlying mechanisms of time perception

Authors:

• Deborah L. Harrington

• Kathleen Y. Haaland

• Robert T. Knight

Date: 1998

PubMed: 9437028

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Abstract:

Precise timing of sensory information from multiple sensory streams is essential for many aspects of human perception and action. Animal and human research implicates the basal ganglia and cerebellar systems in timekeeping operations, but investigations into the role of the cerebral cortex have been limited. Individuals with focal left (LHD) or right hemisphere (RHD) lesions and control subjects performed two time perception tasks (duration perception, wherein the standard tone pair interval was 300 or 600 msec) and a frequency perception task, which controlled for deficits in time-independent processes shared by both tasks. When frequency perception deficits were controlled, only patients with RHD showed time perception deficits. Time perception competency was correlated with an independent test of switching nonspatial attention in the RHD but not the LHD patients, despite attention deficits in both groups. Lesion overlays of patients with RHD and impaired timing showed that 100% of the patients with anterior damage had lesions in premotor and prefrontal cortex (Brodmann areas 6, 8, 9, and 46), and 100% with posterior damage had lesions in the inferior parietal cortex. All LHD patients with normal timing had damage in these same regions, whereas few, if any, RHD patients with normal timing had similar lesion distributions. These results implicate a right hemisphere prefrontal-inferior parietal network in timing. Time-dependent attention and working memory functions may contribute to temporal perception deficits observed after damage to this network.