Prefrontal Cortex Deactivation in Macaques Alters Activity in the Superior Colliculus and Impairs Voluntary Control of Saccades

Koval, Michael J.; Lomber, Stephen G.; Everling, Stefan

doi:10.1523/jneurosci.1258-11.2011

Cited by 49 publications

(57 citation statements)

References 78 publications

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“…The inhibition hypothesis predicts that PFC deactivation should lead to increased activity in the ipsilateral and decreased activity in the contralateral SC. We found that unilateral PFC deactivation resulted in the opposite pattern of results [67], and that bilateral deactivations resulted in decreases in preparatory activity in the SC [61]. These findings demonstrate that the caudal principal sulcus region provides a direct or indirect excitatory drive to saccade-related SC neurons, rather than activating ipsilaterally projecting intratectal inhibitory neurons or commissural intratectal inhibitory neurons.…”

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 56%

“…(c) Activity on prosaccade trials in the bilateral deactivation condition in a task that required monkeys to retain the task instruction for 500-700 ms [67]. ( rstb.royalsocietypublishing.org Phil Trans R Soc B 368: 20130068 motor burst [61]. We found no indication in the activity of SC saccade-related neurons that the antisaccade was prepared when monkeys made performance errors.…”

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 74%

“…Our deactivation experiments have shown that the increased errors have reaction times outside of the range of express saccades and that the initial stimulus-related response is not increased on error trials [61,67] (figure 4b,d). Unfortunately, almost none of the human lesion studies have reported the reaction times of response errors.…”

Section: If Not Inhibition Then What? Prefrontal Cortex Encodes the mentioning

confidence: 81%

“…To assess directly the inhibition model, we carried out a series of studies in which we cryogenically deactivated the PFC while simultaneously recording the activity of SC saccade-related neurons in monkeys performing pro-and antisaccades [61]. We found that unilateral deactivation of the PFC resulted in changes in SC activity, which were not consistent with the inhibition model [67].…”

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 95%

“…These changes in neural activity were mirrored by an increase in saccadic reaction times for contraversive saccades and a decrease for ipsiversive saccades. Error rates were increased on trials in which stimuli were presented in the hemifield ipsilateral to the cooled hemisphere and decreased for trials on which the stimulus was presented to the contralateral [60] and (b) saccade-related neurons in the superior colliculus (SC) on antisaccade (red/light) and prosaccade (blue/dark) trials when the stimulus is presented into the neuron's response field [61]. Activation waveforms were obtained by convolving each spike with an asymmetric function that resembled a postsynaptic potential [62,63].…”

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 99%

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Control of the superior colliculus by the lateral prefrontal cortex

Everling

Johnston

2013

Phil. Trans. R. Soc. B

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Several decades of patient, functional imaging and neurophysiological studies have supported a model in which the lateral prefrontal cortex (PFC) acts to suppress unwanted saccades by inhibiting activity in the oculomotor system. However, recent results from combined PFC deactivation and neural recordings of the superior colliculus in monkeys demonstrate that the primary influence of the PFC on the oculomotor system is excitatory, and stands in direct contradiction to the inhibitory model of PFC function. Although erroneous saccades towards a visual stimulus are commonly labelled reflexive in patients with PFC damage or dysfunction, the latencies of most of these saccades are outside of the range of express saccades, which are triggered directly by the visual stimulus. Deactivation and pharmacological manipulation studies in monkeys suggest that response errors following PFC damage or dysfunction are not the result of a failure in response suppression but can best be understood in the context of a failure to maintain and implement the proper task set.

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Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 56%

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 74%

Section: If Not Inhibition Then What? Prefrontal Cortex Encodes the mentioning

confidence: 81%

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 95%

Section: Challenging the Inhibitory Model: Prefrontal Cortex Deactivamentioning

confidence: 99%

See 3 more Smart Citations

Control of the superior colliculus by the lateral prefrontal cortex

Everling

Johnston

2013

Phil. Trans. R. Soc. B

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Alterations in intrinsic fronto‐thalamo‐parietal connectivity are associated with cognitive control deficits in psychotic disorders

Lencer

Yao

Reilly

et al. 2018

Human Brain Mapping

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Despite a growing number of reports about alterations in intrinsic/resting brain activity observed in patients with psychotic disorders, their relevance to well-established cognitive control deficits in this patient group is not well understood. Totally 88 clinically stabilized patients with a psychotic disorder and 50 healthy controls participated in a resting-state magnetic resonance imaging study (rs-MRI) and performed an antisaccade task in the laboratory to assess voluntary inhibitory control ability. Deficits on this task are a well-established biomarker across psychotic disorders as we found in the present patient sample. First, regional cerebral function was evaluated by measuring the amplitude of low frequency fluctuations (ALFF) in rs-MRI BOLD signals. We found reduced ALFF in patients in regions known to be relevant to antisaccade task performance including bilateral frontal eye fields (FEF), supplementary eye fields (SEF) and thalamus. Second, areas with ALFF alterations were used as seed areas in whole-brain functional connectivity (FC) analysis. Altered FC was observed in a fronto-thalamo-parietal network that was associated with inhibition error rate in patients but not in controls. In contrast, faster time to generate a correct antisaccade was associated with FC in FEF and SEF in controls but this effect was not seen in patients. These findings establish a behavioral relevance of resting-state fMRI findings in psychotic disorders, and extend previous reports of alterations in fronto-thalamo-parietal network activation during antisaccade performance seen in task-based fMRI studies.

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Dissociation of the rostral and dorsolateral prefrontal cortex during sequence learning in saccades: a TMS investigation

Burke

Coats

2015

Exp Brain Res

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This experiment sought to find if differences exist between the dorsolateral prefrontal cortex (DLPFC) and the medial rostral prefrontal cortex (MRPFC) for performing stimulus-independent and stimulusoriented tasks respectively. To find a causal relationship in these areas we employed the use of transcranial magnetic stimulation (TMS). Prefrontal areas were stimulated whilst participants performed random or predictable sequence learning tasks at stimulus onset (1 st presentation of the sequence only for both Random and Predictable), or during the inter-sequence interval. Overall, we found that during the predictable task a significant decrease in saccade latency, gain and duration was found when compared to the randomized conditions, as expected and observed previously. However, TMS stimulation in DLPFC during the delay in the predictive sequence learning task reduced this predictive ability by delaying the saccadic onset and generating abnormal reductions in saccadic gains during prediction. In contrast, we found that stimulation during a delay in MRPFC reversed the normal effects on peak velocity of the task with the predictive task revealing higher peak velocity than the randomized task. These findings provide causal evidence for independent functions of DLPFC and MRPFC in performing stimulus-independent processing during sequence learning in saccades.P a g e | 2

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Prefrontal Cortex Deactivation in Macaques Alters Activity in the Superior Colliculus and Impairs Voluntary Control of Saccades

Cited by 49 publications

References 78 publications

Control of the superior colliculus by the lateral prefrontal cortex

Control of the superior colliculus by the lateral prefrontal cortex

Alterations in intrinsic fronto‐thalamo‐parietal connectivity are associated with cognitive control deficits in psychotic disorders

Dissociation of the rostral and dorsolateral prefrontal cortex during sequence learning in saccades: a TMS investigation

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