Visuomotor control in mice and primates

Abstract

We conduct a comparative evaluation of the visual systems from the retina to the muscles of the mouse and the macaque monkey noting the differences and similarities between these two species. The topics covered include (1) visual-field overlap, (2) visual spatial resolution, (3) V1 cortical point-image [i.e., V1 tissue dedicated to analyzing a unit receptive field], (4) object versus motion encoding, (5) oculomotor range, (6) eye, head, and body movement coordination, and (7) neocortical and cerebellar function. We also discuss blindsight in rodents and primates which provides insights on how the neocortex mediates conscious vision in these species. This review is timely because the field of visuomotor neurophysiology is expanding beyond the macaque monkey to include the mouse; there is therefore a need for a comparative analysis between these two species on how the brain generates visuomotor responses.

Keywords: Blindsight; Cerebellum; Cortical point-image; Macaque monkey; Motion; Mouse; Neocortex; Objects; Oculomotor range.

Figure 1.

On the left is shown the field of view of the rodent (e.g. the mouse) and on the right is shown the field of view of the primate (e.g., the macaque monkey/human). Shown is the innervation scheme between the retina and V1, which is the first major station of the neocortex that receives visual information in these animals (from Priebe and McGee 2014).

Figure 2.

The layout of area V1 of the macaque monkey and the mouse as it pertains to the operculum (i.e., the exposed area of neocortex) is shown. In the case of the macaque monkey only 7 degrees of the visual field of one hemifield is represented in the operculum (top panel)(derived from Schiller and Tehovnik 2008); in the case of the mouse the arrangement is different (bottom panel): the entire visual field is encoded by the operculum and the center of gaze marked by ‘f’ is situated in the center of the map with ‘n’ representing the nasal field and ‘t’ representing temporal field (derived from Fig. 1G,H & Fig. 7A,D of Garret et al. 2014). One operculum in the mouse encodes the entire visual field from a viewing eye as illustrated. Notice the slight magnification of the visual representation beyond the center of gaze ‘f’ for the nasal representation of the mouse; for the macaque monkey the magnification is more extreme which accounts for its superior visual spatial resolution. The magnification is a rough approximation. For precise depictions see Schiller and Tehovnik (2008) and Garret et al. (2014).

Figure 3.

Contrast sensitivity functions plotted as a function of spatial frequency in cycles per degree for primates (e.g., the macaque monkey and human) and rodents (e.g., rats, mice, gerbils, etc.; derived from Souza et al. 2011).

Figure 4.

(A) Extrastriate areas of the mouse are listed from top to bottom according to the density of innervation from V1 from maximal to minimal as derived from Froudarakis et al. (2019): the anterolateral area (AL), the lateromedial area (LM), the rostrolateral area (RL), the lateral intermediate area (LI), the posteromedial area (PM), the posterior area (P), the anteromedial area (AM), the postrhinal area (PR), and the anterior area (A). (B) Neurons that are modulated by objects have been identified in the anterolateral (AL), lateromedial (LM), and lateral intermediate (LI) areas (defined in blue); neurons modulated by complex motion stimuli (e.g. flow fields) have be identified in the rostrolateral (RL) and anteromedial (AM) areas (defined in red). Regions of the extrastriate cortex that encode objects are located lateral to the regions that encode motion. Complete details of the mouse visual cortex can be found in Froudarakis et al. (2019, 2020), Garrett et al. (2014), Marshel et al. (2011), Rasmussen et al. (2020), and Wang et al. (2012).

Figure 5.

The visual areas of the neocortex of the macaque monkey and the mouse are summarized. Both species have homologous areas for processing visual information starting at V1 which process stationary and moving oriented lines. Object encoding has been described for V4 in the macaque monkey and for areas AL (anterolateral), LM (lateromedial) and LI (lateral intermediate) in the mouse. V4 of the macaque monkey ultimately innervates the IT (inferior temporal) cortex which contains cells that respond to faces and other complex objects. The object encoding areas of both the mouse and the macaque monkey contain a central-field representation. Motion encoding has been described for MT/MST (middle temporal cortex/middle superior temporal cortex) in the macaque monkey and for areas AM (anteromedial) and RL (rostrolateral) in the mouse. MT and MST ultimately innervate LIP (the lateral interparietal area) which is an oculomotor area that mediates eye movements and active fixation in macaque monkeys (Andersen and Mountcastle 1983; Mountcastle et al. 1975). Area A (anterior) of the mouse may be a homologue of LIP for eye movements can be evoked from this region (Itokazu et al. 2018) and this area has been implicated in spatial vision in rats (Kolb and Walkey 1987). In the macaque monkey, the visual signals of the posterior cortex eventually arrive in the frontal lobes at one of the two major oculomotor areas: the FEF (the frontal eye fields) and the MEF (the medial eye fields). The FEF is a central controller of eye movements (saccadic, smooth pursuit, and vergence) and the MEF is involved in eye, head, and body part coordination. Activation of the AMC (anteromedial cortex) in the mouse evokes eye movements (Itokazu et al. 2018) as well as head movements in rodents such as rats (Tehovnik and Yeomans 1987). Whether the AMC contains FEF and MEF homologues is not known. V2, V3, sts (superior temporal sulcus), and Cs (central sulcus) are indicated for the macaque monkey and areas PM (posteromedial), P (posterior), and PR (postrhinal) are indicated for the mouse. The remaining labels include M1, M2, the retrosplenial cortex, and the olfactory bulb (OB). The inset to the right color codes some of the areas according to function: objects (blue), motion (red), and oculomotor (orange). For further details see: Froudarakis et al. (2019), Garrett et al. (2014), Marshel et al. (2011), Rasmussen et al. (2020), and Schiller and Tehovnik (2015).

Figure 6.

Extrastriate areas of the mouse are listed from top to bottom according to the percent of the visual field represented as a fraction of that represented by the V1 map using the data of figures 5B,C of Garrett et al. (2014). All maps contained a central visual field encoding the primary optical axis. Regions are list from no topographic coverage (no map) to maximal coverage: the anterior area (A), the posterior area (P), postrhinal area (PR), the anteromedial area (AM), the anterolateral area (AL), the lateral intermediate area (LI), the rostrolateral area (RL), the lateromedial area (LM), the posteromedial area (PM), and area V1 (V1).

Figure 7.

The what-where scheme as originally proposed by Ingle and colleagues in 1967 with respect to the superior colliculus. In this scheme the neocortex is designated as a feature detector (cortico-centric ‘what’) which then sends information to the superior colliculus (SC) for orienting the eyes and head toward peripherally located objects using a retinotopic map in both the mouse and the macaque monkey. In order to move the eyes and head, the brain stem (which is innervated by the superior colliculus and the eye fields in the frontal cortex—FEF and MEF/AMC) contains neurons whose firing rate increases to bring about a precise orientation of the eyes and head to position a visual target in the center of gaze by contracting the muscles (Ingle 1973; Ingle et al. 1967; Schiller and Tehovnik 2015). For other details see the caption of Figure 5.

Figure 8.

Schematic of a top view of human cerebellum divided into three lobes: anterior, mediolateral, and posterior. According to the fMRI experiments of Boillat et al. (2020) who used a 7-tesla scanner, a somatotopy—for eye, tongue, hand, and foot—is found for anterior and posterior lobes, but an eye representation without a clear somatotopy is found for the mediolateral lobe. A head representation is found in lobule VI (Manni and Petrosini 2004) and vestibular control of the head is found in lobule X (Lisberger and Fuchs 1978). The text inset in the upper left defines the movement of the body part or sense that triggered a maximal response within the cerebellar cortex.