Signal Multiplexing in Neural Circuits – The Superior Colliculus Deserves a New Look

The primate superior colliculus (SC) is a key component of the system controlling voluntary movements of the eyes and head. A longstanding view is that the SC maintains a retinotopic representation of visual space, and issues commands specifying movements referenced to the fovea. While an accurate representation of target position relative to the fovea is crucial to gaze shifts, information about the position of the eyes in their orbits is important to a number of potential SC functions that include determining the relative contributions of eye and head movements to generate gaze movements, integrating multimodal sensory input, and generating sequences of multiple movements. Nevertheless, the existence and potential role for eye position signals in the SC remains controversial. Adding to a growing body of evidence for an eye position role in SC function, a recent paper by Groh (2011) makes clever use of microstimulation to demonstrate an effect of orbital position of the eyes on the magnitude of saccades evoked from the monkey SC. Although earlier reports revealed an eye position dependency for electrically evoked saccades in both cats and monkeys (Roucoux et al., 1980; Segraves and Goldberg, 1992; Cowie and Robinson, 1994; Freedman et al., 1996; MartinezTrujillo et al., 2003), whether the effects of stimulation implied the presence of an eye position signal in the SC remained unclear. Groh’s report is significant because it compares the effects of two different stimulation frequencies, yielding greater insight into possible mechanisms, and provides a theoretical framework to help explain the presence and purpose of an eye position signal in the SC. Groh’s results suggest that an eye position signal modulates the readout of saccade commands issued from the SC. The effect of the eye position signal was greatest when low frequency stimulation was delivered, and weaker, though still present at slightly higher stimulation frequencies. Some early reports utilized still higher stimulation frequencies, such as 500 Hz (Robinson, 1972; Schiller and Stryker, 1972). Consistent with the trend observed by Groh, at these higher frequencies the effect of eye position is weaker still or entirely absent. While stimulation effects are notoriously difficult to interpret, Groh argues that these results confirm the existence of an eye position signal in the SC, and she further argues that the eye position signals should be incorporated into an accurate model of saccade generation. Two variations of a revised saccade generation model are proposed. Both acknowledge the existence of an eye position signal within the SC, but they differ in three ways: (1) how the putative eye position signal relates to well-characterized saccade vector signals in the same area, (2) whether that signal is enhanced or diminished by electrical stimulation, and finally (3) how and where that eye position signal is utilized downstream. In the first model (shown in Figure 10 of Groh), the direction of eye movement sensitivity is anti-correlated with the direction of saccade vector tuning in the same area. The electrical stimulation enhances the eye position signal. This signal is then subtracted from (or ignored by) the subsequent stage of eye movement processing in a “normalization” step, and then added back at a later stage. Because of the anti-correlation, the result is a shorter than expected saccade. In the second model (Figure 11), the eye movement sensitivity is positively correlated with saccade vector tuning in the same area. Electrical stimulation serves to “clamp” or block the existing eye movement signal. Downstream areas then attempt to decode a signal that is lacking the expected eye position component. Because of the positive correlation, the end result is again a shorter saccade. Seemingly conflicting physiological reports provide evidence in support of both of these models. Pare and Munoz (2001) found that eye position sensitivity was anti-correlated with the directional selectivity of co-present saccade vector signals in support of the first model. In support of the second model, Van Opstal et al. (1995) and Campos et al. (2006) found that eye position sensitivity was positively correlated with saccade vector tuning. However, as discussed in Groh (2011), these studies utilized different tasks. The analysis intervals used may have also contributed to the conflicting findings. Importantly, Pare and Munoz (2001) analyzed buildup activity that occurred close to the beginning of a saccade, in a task in which the monkeys were expected to have a strong recentering bias. By continuously measuring the strength of saccade vector and eye position tuning, Campos et al. (2006) found that eye position sensitivity was strongest at times far removed from the saccade, and that the eye position signal strength decreased as the saccade onset approached. The natural scanning paradigm in the latter study may also have diminished the strength of a re-centering bias. Future physiological studies will be needed to characterize the strength of eye position signals in various task conditions. Just as the physiological literature does not definitively resolve differences between the models offered by Groh, neither does the current understanding of the effect of electrical stimulation. If stimulation serves to enhance an already present eye position signal, the model shown in Figure 10 is supported. If stimulation, instead, serves to suppress the normally present eye movement signal, then the model shown in Figure 11 is supported. There is a growing body of evidence that electrical stimulation can either facilitate or suppress activity depending on the location of the stimulation,