Brainstem Control of Orienting Movements: Intrinsic Coordinate Systems and Underlying Circuitry

Abstract

A fundamental issue in the understanding of how the nervous system processes information is the way in which sensory information is used to initiate and guide movements. Recent progress has been made by taking an information processing approach in which information - for example, the spatial location of an object towards which an animal will orient - is tracked through the nervous system from sensory to motor levels. In this approach, neurally encoded information is characterized in terms of its representation within a neural or intrinsic coordinate system or set of neural coding parameters. For example, the retina codes spatial location in terms of the location of activity on the retinal surface, whereas motoneurons code spatial location in terms of the pulling directions of the muscles they activate. In between these two peripheral stages, the information passes through intermediate coordinate systems. These intermediate coordinate systems can be characterized by recording or altering the activity of small groups of neurons while an animal is performing a well-defined sensorimotor task. Spatial location information is used to guide orienting movements, those movements made by the eyes, ears, head, or body which function to center an object of interest in the animal's visual field. The optic tectum and forebrain, their connections to the medial mesencephalic and rhombencephalic brainstem tegmental cell groups, and subsequent connections to brainstem motor nuclei and spinal cord are employed to control fundamental aspects of this behavior. Studies reviewed herein indicate that following the retinotopic coding of spatial location in the retina and tectum, spatial location information appears to enter a different coordinate system at tegmental levels in which spatial aspects of orienting movement are coded in terms of their discrete horizontal and vertical components. This Cartesian coordinate system is an example of an abstract neural coordinate system, in that it is a simple, low-dimensional representation of spatial location which differs greatly from both sensory and motor representations. Also, this Cartesian representation may be common to many orienting movements, yet it appears to differ from the coordinate systems controlling other movement types such as stabilization or phasic movements. This suggests an hypothesis in which coordinate systems, especially at intermediate levels of processing, may be organized according to behavioral task as opposed to being determined by the particular sensory or motor system involved in the behavior. Understanding the evolutionary heritage and computational function of abstract neural coordinate systems, and the relation between different coordinate systems and behavioral tasks may be useful in understanding general aspects of sensory information processing and motor control.

Tectotectal connectivity in goldfish

“…These latter findings are in accord with recently reported data showing differences in the tectal connectivity with downstream brainstem structures depending on the injected sites and on their functional properties (Grantyn et al, 1997); hence, they disagree with those proposals (Masino, 1992) indicating that the different functional properties of each tectal region were not supported by particular connectivities with each downstream premotor center in the brainstem. The results presented here, in goldfish, showing the symmetrical point-to-point tectotectal arrangement, could suggest that the functional properties of each tectal site would be supported, at least in part, in a topographic wiring by the descending and medial tracts.…”

What insects can tell us about the origins of consciousness

“…Within a species, the sensory topographic maps in different layers of the SC are superposed, meaning specific regions of space are represented by similar points in each overlaid sensory map (39). This arrangement allows a point of convergence for processed spatially structured information, in turn allowing an integrated sense of space that includes the position, state, and movement of the body (9,(40)(41)(42).…”

The efference cascade, consciousness, and its self: naturalizing the first person pivot of action control

“…Rotation-based coordinate transformations accordingly are central operations in their coordination and control (Crawford et al, 2011). That control is implemented by highly conserved and complex sensorimotor circuitry of the brainstem (Simpson et al, 1988; Büttner-Ennever et al, 1989; Grantyn et al, 1992; Masino, 1992; Isa and Sasaki, 2002), ultimately anchored to the vestibular system (Cohen, 1988). All higher control of orienting behavior must in one way or another access that control circuitry.…”