Motor functions of the superior colliculus

Abstract

The mammalian superior colliculus (SC) and its nonmammalian homolog, the optic tectum, constitute a major node in processing sensory information, incorporating cognitive factors, and issuing motor commands. The resulting action-to orient toward or away from a stimulus-can be accomplished as an integrated movement across oculomotor, cephalomotor, and skeletomotor effectors. The SC also participates in preserving fixation during intersaccadic intervals. This review highlights the repertoire of movements attributed to SC function and analyzes the significance of results obtained from causality-based experiments (microstimulation and inactivation). The mechanisms potentially used to decode the population activity in the SC into an appropriate movement command are also discussed.

Figure 1

Fundamental properties of the superior colliculus (SC) for the generation of saccades. (a) A schematic of the topographic organization of contralateral saccade vectors (left) is encoded in retinotopic coordinates. Isoradial and isodirectional bands are shown as solid and dashed lines, respectively. The radial and directions bands are identified in green and blue numbers, respectively. Each band is represented in a different color. The mapping of these bands in the contralateral hemifield is shown in the right panel. A disproportionately large amount of SC space is used to produce small amplitude saccades relative to the caudal SC areas that produce larger vectors. (b) Neurons in the deep SC layers discharge for a range of saccade amplitudes and directions. Its location on the SC map dictates the optimal vector for which the cell emits its maximal burst. Burst profiles are shown for different amplitude saccades in the optimal direction (left) and for several optimal amplitude saccades in various directions (right). Adapted from Sparks & Gandhi (2003). (c) Population response for the generation of a saccade can be envisioned as a mound of activity across a large portion of the deep SC layers. The amplitude and direction of the executed saccade typically matches with the vector encoded at the locus of maximal activity. Neurons that are active but are located away from the center exhibit a suboptimal burst. Adapted from Sparks & Gandhi (2003).

Figure 2

Activity of superior colliculus (SC) neurons during coordinated eye-head movements (gaze shifts) and head-only movements. (a) Several examples of gaze shifts (left) and head-only movements (right) are plotted as a function of time. For gaze shifts (left), the change in line of sight (equivalently, gaze or eye-in-space) (green traces) is produced initially by rapidly moving the eyes within the orbits (eye-in-head) (blue traces). The head movement (orange traces) typically lags gaze onset, but it can continue for several hundred milliseconds after the termination of the gaze shift, during which the eyes counter-rotate in the orbits. During head-only movements (right), gaze remains stable as the eyes counter-rotate in the orbits. (b) Average spike density waveform of a SC neuron that resembles a classical gaze-related burst neuron. This cell produced a high-frequency burst for optimal size gaze shifts (left), while its activity was negligible for all head-only movements (right). (c) Average spike density waveform of another SC neuron that responds during head-only movements (right). It also discharges for gaze shifts (left), but the duration of activity outlasts the duration of the gaze shift and is better correlated with head duration. Note that the firing rate is too low to be a high-frequency burst even when optimal-amplitude head-only movements and gaze shifts were produced. The traces illustrated in the top row are not the specific movements generated during the neural recordings shown in the bottom two rows. Adapted from Walton et al. (2007), with permission.

Figure 3

Movement field characterization for head-only movements of four superior colliculus (SC) neurons. Average firing rate during the head-only movement (legend key) is plotted as a function of its horizontal and vertical components. The filled contour plots were constructed from individual trial data points. Adapted from Walton et al. (2007), with permission.

Figure 4

Effects of reversible inactivation with lidocaine on head-unrestrained gaze shifts. (a) Position and (b) velocity waveforms of several ∼40° gaze shifts are plotted before (blue) and after (red) a microinjection in the caudal superior colliculus. The onsets of both gaze and head components are delayed, but the head movement initiates sooner. Thus, the eyes counter-rotate in the orbits before gaze onset (arrows). Peak gaze velocity is also reduced after the inactivation. In contrast, the peak head velocity sometimes increases a modest amount. Adapted from Walton et al. (2008), with permission.

Figure 5

Schematic of distribution of activity in deep superior colliculus (SC) layers during fixation. (a) Population activity across the two colliculi is balanced during fixation of a visual target. (b) An inactivation of a small region in the rostral SC (blue circle inside right SC) induces a compensatory shift in activity in the intact side (left SC). Ensemble activity on the lesion side is also redistributed due to inter- and intracollicular interactions. The net activity across the two SC, however, remains balanced to preserve continued fixation on or near the foveal target. Illustration generated based on results by Hafed et al. (2009).

Figure 6

Frameworks of contemporary models for decoding superior colliculus (SC) activity to generate saccadic eye movements. (a) Static averaging decoding model that defines desired saccade metrics by using a vector averaging computation (r_n is the mean firing rate of cell n and R⃗_n is the optimal vector encoded by that cell). (b) Static summation decoding model uses vector summation to define saccade metrics (m⃗_n is the vector contribution of cell n and α is a fixed scaling constant). For both static averaging and summation models, the trajectory and kinematics are controlled downstream by nonlinear local feedback. (c) Dual-coding hypothesis model shares some of the framework of the static vector-averaging model. In addition, the firing rate of the SC across time can modulate the gain of the burst generator. In this manner, SC output now contributes to both metrics and kinematics. (d) Dynamic summation model integrates across time the spikes from an active population. The accumulating activity specifies the intended movement trajectory. Each spike from an SC cell adds a fixed, site-specific “mini” vector contribution to the movement command. In contrast to the other frameworks, the movement is controlled downstream by linear feedback. The projections from the SC are weighted (thickness of lines and size of arrows) according to its origin site along the rostral-caudal dimension. Model parameters: ΔE, desired eye displacement; Δe(t), current eye displacement; me(t), dynamic motor error; ė(t), current eye velocity;∫ dt, temporal integration; “burst,” brainstem burst generator. Adapted from Goossens & Van Opstal (2006).