SystemReviewExploring the role of the substantia nigra pars reticulata in eye movements
Highlights
▶Substantia nigra pars reticulata—a saccadic gate? ▶The substantia nigra—movement or cognition? ▶Eye movements—beyond the substantia nigra.
Section snippets
Overview
Saccadic eye movements are rapid movements of the eyes that reorient the line of sight. Many regions within the forebrain, midbrain, and hindbrain are involved in the generation and control of saccades. Information from the cerebral cortex is sent to the midbrain superior colliculus (colliculus) and pontine nuclei through at least two pathways. One pathway arises from cerebral cortical neurons and targets the colliculus and pons directly (Fries, 1984, Harting et al., 1992). These cortical
Substantia nigra pars reticulata—a saccadic gate?
The relationship between saccadic eye movements and neuronal activity in the nigra was first documented with recordings performed in cat and monkey (Hikosaka and Wurtz, 1983a, Hikosaka and Wurtz, 1983b, Hikosaka and Wurtz, 1983c, Hikosaka and Wurtz, 1983d, Joseph and Boussaoud, 1985). Based on this work, the standard model is that the role of the nigra in saccades is to provide tonic inhibition to the superior colliculus, which when released, permits collicular output neurons to send command
The substantia nigra—movement and cognition?
A larger question is the extent to which the basal ganglia should be considered a motor circuit, as opposed to a cognitive circuit. In light of the nigra's putative preference for memory-guided saccades, and related lines of evidence that the basal ganglia may be preferentially involved in movements that are generated by internal rather than external cues (Wichmann and Kliem, 2004, Turner and Anderson, 2005), it may be more accurate to think of the network as communicating cognitive goals to
Eye movements—beyond the nigra
Many advances in our knowledge of basal ganglia circuitry have taken place in recent years. Anatomically based models emphasizing the dichotomy between the direct and indirect striato-nigral/pallidal pathways are being updated with models that emphasize the reciprocal and branching nature of the projections between basal ganglia structures. Similarly, physiological models based on increases and decreases in discharge rates are being replaced with models emphasizing the temporal structure of
Conclusions and future directions
A recurring theme in this review has been the diversity of signals found in the nigra and other basal ganglia structures. It is clear that the system is more complex than described in early articles. A major challenge is to understand the implications of this diversity at the structure-function level. Is it a general rule that different signals go to different targets, as suggested by the elegant work of Jiang et al. (2003)? This is attractive in that it implies a simple channeling of like
Acknowledgments
The work in our laboratories is supported by NIH EY13692, EY019663, NS065776 (M.A.B.), EY017592 (M.A.S.), NCRR P51 RR000167 awarded to the Wisconsin National Primate Research Center and an NIH core grant in Vision Research P30 EY0166665.
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Threat history controls flexible escape behavior in mice
2022, Current BiologyOptogenetic activation of the inhibitory nigro-collicular circuit evokes contralateral orienting movements in mice
2022, Cell ReportsCitation Excerpt :To activate the nigro-collicular circuit optogenetically, we obtained slices from mice receiving nigral injections with Chronos-GFP. We used Chronos to activate nigral terminals, due to its fast kinetics (Klapoetke et al., 2014) and our desire to more closely match the in vivo discharge rates of nigral neurons which range from 50 to 125 spikes/sec (reviewed in (Basso and Sommer, 2011)). We illuminated the SC in slices through the 40X objective with a 470 nm LED light (∼5 mW light output, Mightex).
The Pause-then-Cancel model of human action-stopping: Theoretical considerations and empirical evidence
2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :For movement to occur, the cortico-basal ganglia direct pathway net-disinhibits brain areas responsible for movement execution, such as primary motor cortex or the frontal eye fields (Chevalier and Deniau, 1990). This is accomplished by GABAergic drive from the striatum to the substantia nigra pars reticulata (SNr), which results in reduced inhibition from SNr to motor regions (Hikosaka and Wurtz, 1985; Basso and Sommer, 2011). During movement initiation in the SST (and other tasks) in rats, this sequence of events can be directly observed – neuronal activity patterns in striatal subpopulations distinguish between contra- and ipsilateral movements at least 130 ms prior to movement initiation (Schmidt et al., 2013).
Neuropsychiatric aspects of Parkinson disease psychopharmacology: Insights from circuit dynamics
2019, Handbook of Clinical NeurologyCitation Excerpt :As the SNpr inhibits the SC, the effect is prosaccadic (Neggers et al., 2012; Yamamoto et al., 2012) (e.g., lesion of top-down dlPFC control facilitates erroneous antisaccades, aka “intrusive saccades” (Condy et al., 2004)). In contrast, the indirect pathway passes through the striatum, globus pallidus interna (GPi) to the STN and SNpr—the net activity disinhibits the SNpr, which suppresses saccades (Alexander et al., 1990; Basso and Sommer, 2011). A concurrent, hyperdirect, pathway (CEF → STN → SNpr) exerts ultimate cognitive control, hypothesized to cancel saccades in a context-dependent fashion (Muri and Nyffeler, 2008).
The Substantia Nigra Pars Reticulata
2016, Handbook of Behavioral NeuroscienceCitation Excerpt :The above results, together with the fact that SNr GABA neurons fire spontaneous high frequency spikes, have led to the following canonical model for a function of SNr outputs: The GABAergic nigral projection tonically inhibits the SC neurons and this tonic inhibition is temporarily removed when the nigral GABA neurons are inhibited or paused by the GABAergic signal from the striatum, thus releasing the SC neurons, eventually triggering eye movements (Chevalier and Deniau, 1990; Hikosaka et al., 2000, 2014). However, evidence also indicates that the nigral GABA projection innervates both glutamatergic neurons that project to the brainstem gaze center and local GABAergic interneurons that innervate the glutamatergic projection neurons (Kaneda et al., 2008); this may lead to SC neuron responses to SNr stimulation that are more complex than the canonical SNr-inhibits-SC response model (Basso et al., 2005; Basso and Sommer, 2011). Since SNr GABA neurons fire sustained high frequency spikes (Fig. 15.8B), one obvious question is: Can the axon terminals of the SNr GABA neurons faithfully follow the high frequency spike input and release GABA vesicles at a high frequency?
The Basal Ganglia
2015, The Rat Nervous System: Fourth Edition