Enhanced visual responses in the superior colliculus and subthalamic nucleus in an animal model of Parkinson’s disease

Rolland, Marta; Carcenac, Carole; Overton, Paul G.; Savasta, Marc; Coizet, Véronique

doi:10.1016/j.neuroscience.2013.07.047

Cited by 17 publications

(28 citation statements)

References 74 publications

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“…Fourteen percent of the subthalamic neurons responded in the alpha band firing activity during the early time window (0-500 ms), suggesting their connection with perceptual processing. Neuronal short-latency activity changes related to visual perception have already been found in animal STNs (72)(73)(74), and have been confirmed in humans by distortion of visual evoked potentials due to STN DBS (75). The difference in neural activity between the fixation and picture viewing periods is not necessarily evidence of visual processing, however; it also may reflect other processes, such as an engagement of selective attention, a shift from gaze fixation to scanning eye movements, or other cognitive functions intervening between vision and action, including memory involvement, target selection, Fig.…”

Section: Discussionmentioning

confidence: 80%

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Sieger

Serranová

Růžička

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Both animal studies and studies using deep brain stimulation in humans have demonstrated the involvement of the subthalamic nucleus (STN) in motivational and emotional processes; however, participation of this nucleus in processing human emotion has not been investigated directly at the single-neuron level. We analyzed the relationship between the neuronal firing from intraoperative microrecordings from the STN during affective picture presentation in patients with Parkinson's disease (PD) and the affective ratings of emotional valence and arousal performed subsequently. We observed that 17% of neurons responded to emotional valence and arousal of visual stimuli according to individual ratings. The activity of some neurons was related to emotional valence, whereas different neurons responded to arousal. In addition, 14% of neurons responded to visual stimuli. Our results suggest the existence of neurons involved in processing or transmission of visual and emotional information in the human STN, and provide evidence of separate processing of the affective dimensions of valence and arousal at the level of single neurons as well.emotion | basal ganglia | subthalamic nucleus | single neuron | arousal A t one time, the subthalamic nucleus (STN), which is an important target for deep brain stimulation (DBS) in the treatment of motor symptoms in Parkinson's disease (PD), was considered an important regulator of motor function (1, 2); however, the occurrence of postoperative neuropsychiatric complications has expanded interest in the nonmotor function of the STN (3, 4). Animal and human studies have already demonstrated the additional functional role of the STN in emotional and motivational processes (5-12). In addition, recent functional MRI studies found STN activation in response to emotional stimuli in healthy subjects (13,14). Therefore, we hypothesized that emotional activity-related neurons should exist in the STN. Participation of the STN in processing emotion has not yet been investigated directly at the single-neuron level in humans. Nonetheless, single-neuron activity related to a priori defined emotional categories (e.g., positive vs. negative) has been detected in a few human brain regions, including the hippocampus, amygdala, and prefrontal and subcallosal cortex (15-18).It has been proposed that emotional behavior is organized along two psychophysiological dimensions: emotional valence, varying from unpleasant to pleasant, and arousal, varying from low to high (19). The individual assessment of these dimensions is closely correlated with somatic and autonomic measures of emotions (20,21). Contrary to a priori categories, they can better reflect emotional characteristics of the stimulus in an individual context, and they take into account interindividual differences based on specific behavioral determinants, such as affective disposition and personality traits (22).In this study, we aimed to detect single-neuron firing pattern changes in the STN that are related to emotional arousal and valence from the in...

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Section: Discussionmentioning

confidence: 80%

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Sieger

Serranová

Růžička

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…We reported that bicuculline induced exaggerated light responses in the SC following the presentation of flashes in PD rats compared to controls. 12 This was a clear demonstration that a specific dopaminergic degeneration in the SNc induced a modification of visual responses recorded directly within a visual structure.…”

Section: Discussionmentioning

confidence: 92%

“…28,29 The role of the SC in parkinsonism has been previously investigated by our group in anesthetized PD rat models, testing the ability of the SC to respond to the presentation of bright flashes using electrophysiological protocols. 12 During general anesthesia, SC neurons are unresponsive to visual stimuli. However, SC sensitivity to visual events can be restored by injections of the GABA A antagonist bicuculline.…”

Section: Discussionmentioning

confidence: 99%

“…[8][9][10][11] In previous work, we found abnormal SC visual responses in PD rat models. 12 Parkinsonian rats showed exaggerated light responses compared to controls, suggesting an abnormal plasticity of the SC that could be linked to increased inhibition from the SNr. 12 We hypothesized that similar abnormalities of the SC may be found in patients with PD.…”

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confidence: 98%

“…12 Parkinsonian rats showed exaggerated light responses compared to controls, suggesting an abnormal plasticity of the SC that could be linked to increased inhibition from the SNr. 12 We hypothesized that similar abnormalities of the SC may be found in patients with PD. Moreover, due to the location in the brainstem, the SC could be affected very early within the course of the PD, likely before the onset of clinical motor signs.…”

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confidence: 98%

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Visual Dysfunction of the Superior Colliculus in De Novo Parkinsonian Patients

Moro

Bellot

Meoni

et al. 2020

Annals of Neurology

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Objective The dual hit hypothesis about the pathogenesis of Parkinson disease (PD) suggests that the brainstem is a convergent area for the propagation of pathological α‐synuclein from the periphery to the brain. Although brainstem structures are likely to be affected early in the course of the disease, detailed information regarding specific brainstem regions is lacking. The aim of our study was to investigate the function of the superior colliculus, a sensorimotor brainstem structure, in de novo PD patients compared to controls using brain functional magnetic imaging and visual stimulation paradigms. Methods De novo PD patients and controls were recruited. PD subjects were imaged before and after starting PD medications. A recently developed functional magnetic resonance imaging protocol was used to stimulate and visualize the superior colliculus and 2 other visual structures: the lateral geniculate nucleus and the primary visual cortex. Results In the 22 PD patients, there was no modulation of the superior colliculus responses to the luminance contrasts compared to controls. This implies a hypersensitivity to low luminance contrast and abnormal rapid blood oxygenation level–dependent signal saturation to high luminance contrasts. The lateral geniculate nucleus was only modulated by 3 to 9% luminance contrasts compared to controls. No major differences were found in the primary visual cortex between both groups. Interpretation Our findings suggest that pathological superior colliculus visual responses in de novo PD patients are present early in the course of the disease. Changes in imaging the superior colliculus could play an important role as a preclinical biomarker of the disease. ANN NEUROL 2020;87:533–546

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The Superior Colliculus: Cell Types, Connectivity, and Behavior

Huang

Snutch

et al. 2022

Neurosci. Bull.

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The superior colliculus (SC), one of the most well-characterized midbrain sensorimotor structures where visual, auditory, and somatosensory information are integrated to initiate motor commands, is highly conserved across vertebrate evolution. Moreover, cell-type-specific SC neurons integrate afferent signals within local networks to generate defined output related to innate and cognitive behaviors. This review focuses on the recent progress in understanding of phenotypic diversity amongst SC neurons and their intrinsic circuits and long-projection targets. We further describe relevant neural circuits and specific cell types in relation to behavioral outputs and cognitive functions. The systematic delineation of SC organization, cell types, and neural connections is further put into context across species as these depend upon laminar architecture. Moreover, we focus on SC neural circuitry involving saccadic eye movement, and cognitive and innate behaviors. Overall, the review provides insight into SC functioning and represents a basis for further understanding of the pathology associated with SC dysfunction.

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Enhanced visual responses in the superior colliculus and subthalamic nucleus in an animal model of Parkinson’s disease

Cited by 17 publications

References 74 publications

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Visual Dysfunction of the Superior Colliculus in De Novo Parkinsonian Patients

The Superior Colliculus: Cell Types, Connectivity, and Behavior

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