The Superior Colliculus/Tectum: Cell Types, Circuits, Computations, Behaviors

Editorial

03 June 2019

Editorial: The Superior Colliculus/Tectum: Cell Types, Circuits, Computations, Behaviors

Karl Farrow

Tadashi Isa

Harald Luksch

and

Keisuke Yonehara

4,786 views

7 citations

Editors

Keisuke Yonehara

National Institute of Genetics (Japan)

Karl Farrow

Neuroelectronics Research Flanders

Tadashi Isa

Kyoto University

Harald Luksch

Technical University of Munich

Impact

Sindbis virus injections into unilateral SC and the anterogradely labeled axon fibers. (A) Light grays on the drawing of the coronal plane indicate the central regions of injection sites. (B,C) PalGFP-expressing SC neurons. (D–I) Coronal sections at the level of the FN (D,E), IRt (F,G), and preBötC (H,I). Axonal density in each area was expressed as the axon density index (see section “Materials and Methods”). The coronal images at the bottom in panels D,F,H were overlaid with the corresponding schematic drawings from the top in those panels (Paxinos and Watson, 2007). Many axonal fibers from the SC were observed in the lower brainstem contralateral to the injection. The two photomicrographs in each row are from the same rat. Amb, ambiguus nucleus; Bo, Bötzinger complex; contra, side contralateral to the lesion; CPGs, central pattern generators; FN, facial nucleus; GiRt, gigantocellular reticular nucleus; ipsi, side ipsilateral to the lesion; IRt, intermediate reticular formation; LPG, lateral paragigantocellular nucleus; PAG, periaqueductal gray; PCRt, parvicellular reticular nucleus; preBötC, pre-Bötzinger complex; SC, superior colliculus; Sp5I, spinal trigeminal nucleus, interpolar part; Sp5O, spinal trigeminal nucleus, oral part.

Original Research

22 November 2018

A Descending Circuit Derived From the Superior Colliculus Modulates Vibrissal Movements

Miki Kaneshige

, 3 more and

Takahiro Furuta

3,928 views

11 citations

Photomicrographs of nissl-stained sections through the amygdala, superior colliculus (SC), and pulvinar. Panel (A) shows the location of panels (B–F) within the brain. Amygdala nuclei (B) are outlined and labeled according to Amaral et al. (1992). AB, accessory basal; B, basal; L, lateral; M, medial; PL, paralaminar. SC nuclei (C) are outlined and labeled according to May (2006). SZ/SGS, stratum zonale/stratum griseum superficiale; SO, stratum opticum; SGI/SAI, stratum griseum intermedium/stratum album intermedium; SGP, stratum griseum profundum; SAP, stratum album profundum. Thalamic nuclei (D–F) are outlined and labeled according to the delineations of the Olszewski (1952). CM, centromedial nucleus; H, habenula; L, nucleus limitans; LGN, lateral geniculate nucleus; LP, lateral posterior nucleus; MD, mediodorsal nucleus; MG, medial geniculate nucleus; PI, inferior pulvinar; PL, lateral pulvinar; PM, medial pulvinar; PO, oral pulvinar; SG, suprageniculate nucleus; VPL, ventroposteriolateral nucleus.

Original Research

24 October 2018

Colocalization of Tectal Inputs With Amygdala-Projecting Neurons in the Macaque Pulvinar

Catherine Elorette

, 2 more and

Ludise Malkova

3,775 views

32 citations

Temporal (A,B) and spatial (C,D) aspects of the behavioral tasks. (A) Vertical gaze position toward an upward target (dashed red horizontal line) plotted as a function of time for example trials in the reactive task. Results from this task are reported in Sadeh et al. (2018). (B) Similar gaze traces for the same target, but obtained from the memory delay task. Note that the memory delay is variable, so the “go” signal (extinction of the fixation point) occurred at different time points (green arrow heads). Results from this task were reported in detail previously (Sadeh et al., 2015). (C) Two-dimensional gaze trajectories (gray lines) from the reactive task for an example target in monkey M2. Also shown are the range of initial fixation positions (green square), the tolerance window (red circle) and the other possible targets used in this experimental session (gray circles) to map a neuron’s receptive field. The identical spatial layouts were used for both tasks to test each neuron. (D) Target-Gaze (TG) continuum constructed between and beyond target position (red dot) and gaze end point (blue dot) for each trial, and used to determine best fits for neural receptive fields.

Original Research

22 October 2018

The Influence of a Memory Delay on Spatial Coding in the Superior Colliculus: Is Visual Always Visual and Motor Always Motor?

Morteza Sadeh

, 3 more and

John Douglas Crawford

3,062 views

20 citations

Original Research

24 July 2018

Orientation and Contrast Tuning Properties and Temporal Flicker Fusion Characteristics of Primate Superior Colliculus Neurons

Chih-Yang Chen

and

Ziad M. Hafed

The primate superior colliculus is traditionally studied from the perspectives of gaze control, target selection, and selective attention. However, this structure is also visually responsive, and it is the primary visual structure in several species. Thus, understanding the visual tuning properties of the primate superior colliculus is important, especially given that the superior colliculus is part of an alternative visual pathway running in parallel to the predominant geniculo-cortical pathway. In recent previous studies, we have characterized receptive field organization and spatial frequency tuning properties in the primate (rhesus macaque) superior colliculus. Here, we explored additional aspects like orientation tuning, putative center-surround interactions, and temporal frequency tuning characteristics of visually-responsive superior colliculus neurons. We found that orientation tuning exists in the primate superior colliculus, but that such tuning is relatively moderate in strength. We also used stimuli of different sizes to explore contrast sensitivity and center-surround interactions. We found that stimulus size within a visual receptive field primarily affects the slope of contrast sensitivity curves without altering maximal firing rate. Additionally, sustained firing rates, long after stimulus onset, strongly depend on stimulus size, and this is also reflected in local field potentials. This suggests the presence of inhibitory interactions within and around classical receptive fields. Finally, primate superior colliculus neurons exhibit temporal frequency tuning for frequencies lower than 30 Hz, with critical flicker fusion frequencies of <20 Hz. These results support the hypothesis that the primate superior colliculus might contribute to visual performance, likely by mediating coarse, but rapid, object detection and identification capabilities for the purpose of facilitating or inhibiting orienting responses. Such mediation may be particularly amplified in blindsight subjects who lose portions of their primary visual cortex and therefore rely on alternative visual pathways including the pathway through the superior colliculus.

5,718 views

48 citations

Optogenetic approach to elucidating the role of the FEF-SC pathway in oculomotor behavior. (A) Experimental design. In order to deliver the channelrhodopsin-2 (ChR2) gene into FEF neurons, adeno-associated virus type 2 vector (AAV2-CMV-ChR2-EYFP) was injected unilaterally into the FEF. Using optrodes (an optic fiber attached to a recording electrode), 473-nm blue laser light was emitted into the SC and single-unit activity was simultaneously recorded. (B) ChR2-EYFP expression in the SC. Top, wide-field immunofluorescent image of a coronal section through the SC. Bottom, immunofluorescence of YFP-expressing axons in the ipsilateral and contralateral SC. NeuN-expressing SC neurons are shown in red. Asterisks in the above panel indicate the locations of the ipsilateral and contralateral images in the SC. PAG, periaqueductal gray; SGI, stratum griseum intermediale; SGP, stratum griseum profundum; SGS, stratum griseum superficiale; SO, stratum opticum. (C) Activity of two neuron examples that were excited (left) and inhibited (right) during laser light emission in the ipsilateral SC. Gray areas indicate the period of laser light emission. (D) Saccadic eye movements evoked by optical stimulation at a representative site in the ipsilateral SC. Left, trajectories of eye positions. Black and gray crosses indicate the fixation point (FIX) and the center of the response field (RF) at the stimulation site in the SC. The FIX was kept on during laser light emission. Right, horizontal and vertical eye traces. (E) Polar plot of the magnitude (r) and direction (θ) of evoked saccades relative to the RF center of the stimulation sites. Red lines indicate the averaged vector of evoked saccades at each stimulation site (n = 15). Saccade toward the RF center is denoted with (r, θ) = (1.0, 0). (F) Effect of optical stimulation at a representative site in the ipsilateral SC on saccade latency. Top, horizontal eye traces. Bottom, cumulative distribution of the latency of saccades toward the RF (left) and those away from the RF (right). Purple and black curves indicate stimulated and non-stimulated saccades, respectively. Reproduced with permission from Inoue et al. (2015).

Mini Review

28 August 2018

Causal Role of Neural Signals Transmitted From the Frontal Eye Field to the Superior Colliculus in Saccade Generation

Masayuki Matsumoto

, 1 more and

Masahiko Takada

5,247 views

18 citations

Overview of the sSC cell types (Gale and Murphy, 2014; Inayat et al., 2015; Shang et al., 2015, 2018), potential inputs from retinal ganglion cell types (Sanes and Masland, 2015), relevant output brain targets, and behavioral roles. Note that the identity of the retinal ganglion cells projecting to each collicular cell type remains unknown. Abbreviations: DSGCs, direction-selective ganglion cells; αRGCs, alpha retinal ganglion cells; J-RGCs, JAM-B-expressing OFF retinal ganglion cells; PV+, parvalbumin-positive neurons; dSC, deep layers of the superior colliculus; PbG, parabigeminal nucleus; LP, lateral posterior nucleus of the thalamus; sSC, superficial layers of the superior colliculus; LGN, lateral geniculate nucleus of the thalamus; Cn, cuneiform nucleus; MLR, mesencephalic locomotor region.

Perspective

24 July 2018

The Mouse Superior Colliculus as a Model System for Investigating Cell Type-Based Mechanisms of Visual Motor Transformation

Ana F. Oliveira

and

Keisuke Yonehara

The mouse superior colliculus (SC) is a laminar midbrain structure involved in processing and transforming multimodal sensory stimuli into ethologically relevant behaviors such as escape, defense, and orienting movements. The SC is unique in that the sensory (visual, auditory, and somatosensory) and motor maps are overlaid. In the mouse, the SC receives inputs from more retinal ganglion cells than any other visual area. This makes the mouse SC an ideal model system for understanding how visual signals processed by retinal circuits are used to mediate visually guided behaviors. This Perspective provides an overview of the current understanding of visual motor transformations operated by the mouse SC and discusses the challenges to be overcome when investigating the input–output relationships in single collicular cell types.

7,011 views

34 citations

Review

21 June 2018

Principles of Functional Circuit Connectivity: Insights From Spontaneous Activity in the Zebrafish Optic Tectum

Emiliano Marachlian

, 2 more and

Germán Sumbre

6,385 views

25 citations

Original Research

19 June 2018

Transformation of Feature Selectivity From Membrane Potential to Spikes in the Mouse Superior Colliculus

Xuefeng Shi

, 1 more and

Jianhua Cang

4,357 views

7 citations

Original Research

04 May 2018

Parvalbumin and GABA Microcircuits in the Mouse Superior Colliculus

Claudio A. Villalobos

, 3 more and

Michele A. Basso

The mammalian superior colliculus (SC) is a sensorimotor midbrain structure responsible for orienting behaviors. Although many SC features are known, details of its intrinsic microcircuits are lacking. We used transgenic mice expressing reporter genes in parvalbumin-positive (PV⁺) and gamma aminobutyric acid-positive (GABA⁺) neurons to test the hypothesis that PV⁺ neurons co-localize GABA and form inhibitory circuits within the SC. We found more PV⁺ neurons in the superficial compared to the intermediate SC, although a larger percentage of PV⁺ neurons co-expressed GABA in the latter. Unlike PV⁺ neurons, PV⁺/GABA⁺ neurons showed predominantly rapidly inactivating spiking patterns. Optogenetic activation of PV⁺ neurons revealed direct and feedforward GABAergic inhibitory synaptic responses, as well as excitatory glutamatergic synapses. We propose that PV⁺ neurons in the SC may be specialized for a variety of circuit functions within the SC rather than forming a homogeneous, GABAergic neuronal subtype as they appear to in other regions of the brain.

12,773 views

66 citations

Monkeys showed behavioral bias to good objects. (A) Free Viewing task for behavioral test. Four objects pseudorandomly drawn from a set of eight objects were presented in one of two configurations (square or diamond) with all objects equidistant from center of screen (15°). Objects presented on any given trial could contain 0, 1, 2, 3, or 4 good objects. Subject was free to look anywhere on the screen for duration of object presentations. (B) Behavioral preference for good objects in the Free Viewing task. All subjects made significantly more first saccades to good objects than bad objects despite no associated reward (∗∗∗p < 0.001). (C) Behavioral preference for individual objects shown as first saccade rate to each object. Horizontal dashed lines represent group mean for good (red) and bad (blue) objects. Solid gray horizontal line represents chance rate (25%) for first saccade to one object among four objects.

Original Research

11 June 2018

Visual Neurons in the Superior Colliculus Discriminate Many Objects by Their Historical Values

Whitney S. Griggs

, 2 more and

Okihide Hikosaka

4,936 views

22 citations

Expression of Kaede in the Gal4s1113t ET line. (A–K) The mean intensity, resulting from registering and averaging the expression pattern across nine animals, of the genotype Gal4s1113t;UAS:Kaede is shown in magenta, overlaid with a pan-neuronal (HuC) H2B-RFP label (green). (A–E) Whole brain images at five dorsal-ventral depths separated by 15–21 microns. Arrows in (A,B) indicate expression in the spinal cord of these animals. (F) In the dorsal brain, Gal4s1113t axons are present in the tectal neuropil (TN; red outline), tectal periventricular layer (PVL; cyan outline), valvula (Va) cerebellum (arrowhead) and hindbrain (Hb; arrow). (G) Axonal expression in the tectal neuropil (red outline) and sparse expression is seen in tectal periventricular neurons (cyan outline). Axons are present in the hindbrain (arrows). (H) Further ventral, expression is seen in the neuropil areas medial to the torus semicircularis (arrow) and in hindbrain neuropil (Hbn) regions (blue outline). (I) Axonal expression in the diffuse nucleus of the intermediate hypothalamus (IH; gray outline), a hypothalamic Gad1b cluster (blue outline) and hypothalamic Vglut2 cluster (red outline), and the migrated posterior tubercular area (M2; green outline). (J) Axonal labeling (arrow) of neurons with cell bodies located in the rostral hypothalamus (RH; outlined in red in K). Scale bars equal 200 μm.

Original Research

17 January 2018

Hypothalamic Projections to the Optic Tectum in Larval Zebrafish

Lucy A. Heap

, 4 more and

Ethan K. Scott

The optic tectum of larval zebrafish is an important model for understanding visual processing in vertebrates. The tectum has been traditionally viewed as dominantly visual, with a majority of studies focusing on the processes by which tectal circuits receive and process retinally-derived visual information. Recently, a handful of studies have shown a much more complex role for the optic tectum in larval zebrafish, and anatomical and functional data from these studies suggest that this role extends beyond the visual system, and beyond the processing of exclusively retinal inputs. Consistent with this evolving view of the tectum, we have used a Gal4 enhancer trap line to identify direct projections from rostral hypothalamus (RH) to the tectal neuropil of larval zebrafish. These projections ramify within the deepest laminae of the tectal neuropil, the stratum album centrale (SAC)/stratum griseum periventriculare (SPV), and also innervate strata distinct from those innervated by retinal projections. Using optogenetic stimulation of the hypothalamic projection neurons paired with calcium imaging in the tectum, we find rebound firing in tectal neurons consistent with hypothalamic inhibitory input. Our results suggest that tectal processing in larval zebrafish is modulated by hypothalamic inhibitory inputs to the deep tectal neuropil.

11,835 views

34 citations