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Connections Between the Zona Incerta and Superior Colliculus in the Monkey and Squirrel

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Connections Between the Zona Incerta and Superior Colliculus in the Monkey and Squirrel UCLA UCLA Previously Published Works Title Connections between the zona incerta and superior colliculus in the monkey and squirrel. Permalink https://escholarship.org/uc/item/31k8f8q5 Journal Brain structure & function, 223(1) ISSN 1863-2653 Authors May, Paul J Basso, Michele A Publication Date 2018 DOI 10.1007/s00429-017-1503-2 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Brain Struct Funct DOI 10.1007/s00429-017-1503-2 ORIGINAL ARTICLE Connections between the zona incerta and superior colliculus in the monkey and squirrel 1,2,3 4,5 Paul J. May • Michele A. Basso Received: 16 June 2017 / Accepted: 18 August 2017 Ó Springer-Verlag GmbH Germany 2017 Abstract The zona incerta contains GABAergic neurons incerta injections produced retrogradely labeled neurons in that project to the superior colliculus in the cat and rat, the superior colliculus of both species. In the squirrel, most suggesting that it plays a role in gaze changes. However, cells inhabited the lower sublamina of the intermediate whether this incertal connection represents a general gray layer, but in the monkey, they were scattered mammalian pattern remains to be determined. We used throughout the deeper layers. Labeled cells were present neuronal tracers to examine the zona incerta connections among the pretectal nuclei in both species. Labeled ter- with the midbrain tectum in the gray squirrel and macaque minals were concentrated in the lower sublamina of the monkey. Collicular injections in both species revealed that intermediate gray layer of both species, but were dispersed most incertotectal neurons lay in the ventral layer, but among the pretectal nuclei. In summary, an incertal pro- anterogradely labeled tectoincertal terminals were found in jection that is concentrated on the collicular motor output both the dorsal and ventral layers. In the monkey, injec- layers and that originates in the ventral layer of the ipsi- tions of the pretectum also produced retrograde labeling, lateral zona incerta is a common mammalian feature, but mainly in the dorsal layer. The dendritic fields of suggesting an important role in collicular function. incertotectal and incertopretectal cells were generally contained within the layer inhabited by their somata. The Keywords Gaze Á Eye movements Á GABA Á Primate Á macaque, but not the squirrel, zona incerta extended dor- Pretectum Á Inhibition solaterally, within the external medullary lamina. Zona Abbreviations III Oculomotor nucleus & Paul J. May APt Anterior pretectal nucleus [email protected] BDA Biotinylated dextran amine 1 Department of Neurobiology and Anatomical Sciences, BP Basilar pons University of Mississippi Medical Center, Jackson, DLG Dorsal lateral geniculate nucleus MS 39216, USA EML External medullary lamina 2 Department of Ophthalmology, University of Mississippi GP Globus pallidus Medical Center, Jackson, MS 39216, USA HRP Horseradish peroxidase 3 Department of Neurology, University of Mississippi Medical IC Inferior colliculus Center, Jackson, MS 39216, USA ICa Internal capsule 4 Fuster Laboratory of Cognitive Neuroscience, Department of Lim Nucleus limitans Psychiatry and Biobehavioral Sciences and Neurobiology, MG Medial geniculate nucleus Semel Institute for Neuroscience and Human Behavior, MPt Medial pretectal nucleus University of California at Los Angeles, Los Angeles, CA 90095, USA nPC Nucleus of the posterior commissure nOT Nucleus of the optic tract 5 Brain Research Institute, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, Opt Stratum opticum CA 90095, USA OT Optic tract 123 Brain Struct Funct PAG Periaqueductal gray chosen from a host of possibilities, and the property of PB Parabrachial nucleus salience depends on the memory of the animal, species PG Pregeniculate specific behavioral presets (e.g., what is food and what is a Pul Pulvinar threat), previous reinforcements, and the internal state of Pt Pretectum the animal (Ingle 1971; Dean et al. 1989; Westby et al. PPt Posterior pretectal nucleus 1990; Sato and Hikosaka 2002; Yasuda et al. 2012). All of RT Reticular thalamic nucleus these decisions may involve inhibiting alternative choices. SAI Intermediate white layer Clearly, the roles of inhibition in the SC are various and SC Superior colliculus numerous. In line with this, GABAergic terminals are very SGS Stratum griseum superficiale numerous on the surface of collicular motor output neurons SGI Stratum griseum intermediale (Lu et al. 1985). Indeed, the deep layers contain a promi- lSGI SGI, lower sublamina nent collection of GABAergic local circuit interneurons uSGI SGI, upper sublamina (Mize 1988; Mize et al. 1991). In addition, they are tar- SGP Stratum griseum profundum geted by a variety of extrinsic GABAergic inputs (Appell SNc Substantia nigra pars compacta and Behan 1990). The best studied among these is the SNl Substantia nigra pars lateralis substantia nigra pars reticulata. The nigrotectal projection SNr Substantia nigra pars reticulata provides an extensive input to the motor output layers of SO Stratum opticum the SC (Jayaraman et al. 1977; May and Hall 1984; Harting STh Subthalamic nucleus et al. 1988; Bickford and Hall 1992; Redgrave et al. 1992). WGA-HRP Wheat germ agglutinin conjugated HRP It is likely that this projection plays an important role in VLG Ventral lateral geniculate nucleus releasing the burst of activity in collicular cells before VP Ventral posterior nucleus saccades, including those to remembered targets (Hikosaka ZI Zona incerta and Wurtz 1983b). Another major extrinsic source of dZI Dorsal layer of ZI GABAergic input is the central mesencephalic reticular vZI Ventral layer of ZI formation (cMRF). The cMRF receives direct input from collicular gaze output neurons and then provides a GABAergic feedback projection back onto these output Introduction cells (Moschovakis et al. 1988; Chen and May 2000; Zhou et al. 2008; Wang et al. 2010). While it is known that the Inhibitory processes help control the bursts of activity in cMRF contains neurons that display long lead, saccade- the superior colliculus (SC) that precede each saccade related bursts, the precise role of this feedback pathway has (Hikosaka and Wurtz 1985). Unlike the widespread activity yet to be ascertained (Waitzman et al. 1996; Cromer and present in the superficial, visuosensory layer, in the deeper Waitzman 2007). layers, activity needs to be concentrated at one location in Yet, another major extrinsic GABAergic projection to the motor map once a target has been selected, because the SC comes from the zona incerta (ZI). This projection only one saccade can be made at a time. There is evidence exists in both the rat and cat (Edwards et al. 1979; that the direct inputs from superficial to deep collicular Watanabe and Kawana 1982; Shammah-Lagnado et al. layers are modulated by inhibition to arrange this pattern of 1985; Ficalora and Mize 1989; Appell and Behan 1990). activation and that selective release of this inhibition may While some ZI neurons in monkeys display saccade-related be important in producing express saccades (Ozen et al. activity (Hikosaka and Wurtz 1983a;Ma1996), there is 2000; Isa and Saito 2001). Inhibition also plays a role in the evidence from non-primates that they modify movement relationship between the two colliculi, which have activity with respect to internal state and autonomic nervous system that codes for saccades to the left and the right, and activity levels (Mitrofanis 2005). Nevertheless, the ZI’s between the hemifields within each colliculus, which code precise role with respect to tectally generated gaze changes for upward and downward eye movements (Munoz and is poorly understood. Towards this end, we have endeav- Istvan 1998; Takahashi et al. 2005, 2007). Inhibition may ored to better define the pattern of connections between the even play a role in defining the duration of burst activity ZI and the SC. Previously, we demonstrated a number of and the location of cells activated within the collicular features of these connections in the cat (May et al. 1997; motor map (Kaneda et al. 2008). Since this activity pattern Perkins et al. 2006). These included the fact that the source results in both an orienting movement and a shift in of the incertotectal projection was largely confined to the attention by the animal (Basso and May 2017), one may ventral layer of ZI and that this layer extended dorsolat- argue that inhibition is critical to the primary roles of the erally between the reticular thalamic nucleus and the colliculus. Furthermore, the most salient target must be external medullary lamina. Within the SC, the incertotectal 123 Brain Struct Funct terminal field was concentrated in the lower sublamina of utilized stereotaxic coordinates developed from an in- the intermediate gray layer (SGI), and this same sublamina house atlas. These animals were deeply anesthetized with is the primary source of the tectoincertal projection. sodium pentobarbital (70 mg/kg, ip) 2–3 days later, and Finally, in the cat, we noted connections between the dorsal were perfused through the heart with a buffered saline sublamina of ZI and the pretectum, particularly the anterior rinse, followed by a fixative containing 0.5% pretectal nucleus. While connections between the ZI and paraformaldehyde and 2.5% glutaraldehyde in 0.1 M, pH the SC are also present in the rat, a number of the details of 7.2 phosphate buffer (PB). The brains were postfixed in the this projection differed from those seen in the
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