Retinal input integration in excitatory and inhibitory neurons in the mouse superior colliculus in vivo
Vision for perception versus vision for action: dissociable contributions of visual sensory drives from primary visual cortex and superior colliculus neurons to orienting behaviors
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.
A neural mechanism for terminating decisions
The brain makes decisions by accumulating evidence until there is enough to stop and choose. Neural mechanisms of evidence accumulation are well established in association cortex, but the site and mechanism of termination is unknown. Here, we elucidate a mechanism for termination by neurons in the primate superior colliculus. We recorded simultaneously from neurons in lateral intraparietal cortex (LIP) and the superior colliculus (SC) while monkeys made perceptual decisions, reported by eye-movements. Single-trial analyses revealed distinct dynamics: LIP tracked the accumulation of evidence on each decision, and SC generated one burst at the end of the decision, occasionally preceded by smaller bursts. We hypothesized that the bursts manifest a threshold mechanism applied to LIP activity to terminate the decision. Focal inactivation of SC produced behavioral effects diagnostic of an impaired threshold sensor, requiring a stronger LIP signal to terminate a decision. The results reveal the transformation from deliberation to commitment.
Mechanisms of visual circuit development: aligning topographic maps of space
Multisensory Integration: Development, Plasticity, and Translational Applications
Visual Processing in the Superior Colliculus
Deciding to stop deciding: A cortical-subcortical circuit for forming and terminating a decision
The neurobiology of decision-making is informed by neurons capable of representing information over time scales of seconds. Such neurons were initially characterized in studies of spatial working memory, motor planning (e.g., Richard Andersen lab) and spatial attention. For decision-making, such neurons emit graded spike rates, that represent the accumulated evidence for or against a choice. They establish the conduit between the formation of the decision and its completion, usually in the form of a commitment to an action, even if provisional. Indeed, many decisions appear to arise through an accumulation of noisy samples of evidence to a terminating threshold, or bound. Previous studies show that single neurons in the lateral intraparietal area (LIP) represent the accumulation of evidence when monkeys make decisions about the direction of random dot motion (RDM) and express their decision with a saccade to the neuron’s preferred target. The mechanism of termination (the bound) is elusive. LIP is interconnected with other brain regions that also display decision-related activity. Whether these areas play roles in the decision process that are similar to or fundamentally different from that of LIP is unclear. I will present new unpublished experiments that begin to resolve these issues by recording from populations of neurons simultaneously in LIP and one of its primary targets, the superior colliculus (SC), while monkeys make difficult perceptual decisions.
Arousal modulates retinal output
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