The primary visual cortex (V1) directly projects to the superior colliculus (SC) and is believed to provide sensory drive for eye movements. Consistent with this, a majority of saccade-related SC neurons also exhibit short-latency, stimulus-driven visual responses, which are additionally feature-tuned. However, direct neurophysiological comparisons of the visual response properties of the two anatomically-connected brain areas are surprisingly lacking, especially with respect to active looking behaviors. I will describe a series of experiments characterizing visual response properties in primate V1 and SC neurons, exploring feature dimensions like visual field location, spatial frequency, orientation, contrast, and luminance polarity. The results suggest a substantial, qualitative reformatting of SC visual responses when compared to V1. For example, SC visual response latencies are actively delayed, independent of individual neuron tuning preferences, as a function of increasing spatial frequency, and this phenomenon is directly correlated with saccadic reaction times. Such “coarse-to-fine” rank ordering of SC visual response latencies as a function of spatial frequency is much weaker in V1, suggesting a dissociation of V1 responses from saccade timing. Consistent with this, when we next explored trial-by-trial correlations of individual neurons’ visual response strengths and visual response latencies with saccadic reaction times, we found that most SC neurons exhibited, on a trial-by-trial basis, stronger and earlier visual responses for faster saccadic reaction times. Moreover, these correlations were substantially higher for visual-motor neurons in the intermediate and deep layers than for more superficial visual-only neurons. No such correlations existed systematically in V1. Thus, visual responses in SC and V1 serve fundamentally different roles in active vision: V1 jumpstarts sensing and image analysis, but SC jumpstarts moving. I will finish by demonstrating, using V1 reversible inactivation, that, despite reformatting of signals from V1 to the brainstem, V1 is still a necessary gateway for visually-driven oculomotor responses to occur, even for the most reflexive of eye movement phenomena. This is a fundamental difference from rodent studies demonstrating clear V1-independent processing in afferent visual pathways bypassing the geniculostriate one, and it demonstrates the importance of multi-species comparisons in the study of oculomotor control.

In this lecture, I will present our recent progress on three aspects of population responses in the primary visual cortex: encoding local stimulus attributes, electrical microstimulation and higher visual function. In the first part I will focus on population encoding and reconstruction of contour shapes in V1 and the comparison between monkey and mouse visual responses. In the second part of the talk I will present the effects of microstimulation on neural population in V1 and the relation to evoked saccades. In the final part of the talk I will discuss top-down influences in V1 and their relation to higher visual functions.

Team work makes sensory streams work: our senses work together, learn from each other, and stand in for one another, the result of which is perception and understanding. Learned associations between stimuli in different sensory modalities can shape the way we perceive these stimuli (Mcgurk and Macdonald, 1976). During audio-visual associative learning, auditory cortex is thought to underlie multi-modal plasticity in visual cortex (McIntosh et al., 1998; Mishra et al., 2007; Zangenehpour and Zatorre, 2010). However, it is not well understood how processing in visual cortex is altered by an auditory stimulus that is predictive of a visual stimulus and what the mechanisms are that mediate such experience-dependent, audio-visual associations in sensory cortex. Here we describe a neural mechanism by which an auditory input can shape visual representations of behaviorally relevant stimuli through direct interactions between auditory and visual cortices. We show that the association of an auditory stimulus with a visual stimulus in a behaviorally relevant context leads to an experience-dependent suppression of visual responses in primary visual cortex (V1). Auditory cortex axons carry a mixture of auditory and retinotopically-matched visual input to V1, and optogenetic stimulation of these axons selectively suppresses V1 neurons responsive to the associated visual stimulus after, but not before, learning. Our results suggest that cross-modal associations can be stored in long-range cortical connections and that with learning these cross-modal connections function to suppress the responses to predictable input.

Neural responses in the visual system are usually not purely visual but depend on behavioural and internal states such as arousal. This dependence is seen both in primary visual cortex (V1) and in subcortical brain structures receiving direct retinal input. In this talk, I will show that modulation by behavioural state arises as early as in the output of the retina.To measure retinal activity in the awake, intact brain, we imaged the synaptic boutons of retinal axons in the superficial superior colliculus (sSC) of mice. The activity of about half of the boutons depended not only on vision but also on running speed and pupil size, regardless of retinal illumination. Arousal typically reduced the boutons’ visual responses to preferred direction and their selectivity for direction and orientation.Arousal may affect activity in retinal boutons by presynaptic neuromodulation. To test whether the effects of arousal occur already in the retina, we recorded from retinal axons in the optic tract. We found that, in darkness, more than one third of the recorded axons was significantly correlated with running speed. Arousal had similar effects postsynaptically, in sSC neurons, independent of activity in V1, the other main source of visual inputs to colliculus. Optogenetic inactivation of V1 generally decreased activity in collicular neurons but did not diminish the effects of arousal. These results indicate that arousal modulates activity at every stage of the visual system. In the future, we will study the purpose and the underlying mechanisms of behavioural modulation in the early visual system