Visual sensitivity, probed through perceptual detectability of very brief visual stimuli, is strongly impaired around the time of rapid eye movements. This robust perceptual phenomenon, called saccadic suppression, is frequently attributed to active suppressive signals that are directly derived from eye movement commands. Here we show instead that visual-only mechanisms, activated by saccade-induced image shifts, can account for all perceptual properties of saccadic suppression that we have investigated. Such mechanisms start at, but are not necessarily exclusive to, the very first stage of visual processing in the brain, the retina. Critically, neural suppression originating in the retina outlasts perceptual suppression around the time of saccades, suggesting that extra-retinal movement-related signals, rather than causing suppression, may instead act to shorten it. Our results demonstrate a far-reaching contribution of visual processing mechanisms to perceptual saccadic suppression, starting in the retina, without the need to invoke explicit motor-based suppression commands. Saccadic suppression is frequently attributed to active suppressive signals derived from eye movement commands. Here, the authors show that visual-only mechanisms starting in the retina can account for perceptual saccadic suppression properties without the need for motor-based suppression commands.

/pdf/perceptual-saccadic-suppression-starts-in-the-retina-43caksuaih.pdf

Perceptual saccadic suppression starts in the retina.

The Foveal Visual Representation of the Primate Superior Colliculus.

Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior. Microsaccades are small-amplitude, fixational eye movements that are largely thought to be involuntary. Here, the authors demonstrate that monkeys (and humans) can be easily trained to respond to a remembered target location with a volitional microsaccade, and that a population of superior colliculus neurons is selectively associated with them.

Memory-guided microsaccades.

Parallel Channels for Motion Feature Extraction in the Pretectum and Tectum of Larval Zebrafish.

Visual sensitivity, probed through perceptual detectability of very brief visual stimuli, is strongly impaired around the time of rapid eye movements. This robust perceptual phenomenon, called saccadic suppression, is frequently attributed to active suppressive signals that are directly derived from eye movement commands. Here we show instead that visual-only mechanisms, activated by saccade-induced image shifts, can account for all perceptual properties of saccadic suppression that we have investigated. Such mechanisms start at, but are not necessarily exclusive to, the very first stage of visual processing in the brain, the retina. Critically, neural suppression originating in the retina outlasts perceptual suppression around the time of saccades, suggesting that extra-retinal movement-related signals, rather than causing suppression, may instead act to shorten it. Our results demonstrate a far-reaching contribution of visual processing mechanisms to perceptual saccadic suppression, starting in the retina, without the need to invoke explicit motor-based suppression commands.

/pdf/perceptual-saccadic-suppression-starts-in-the-retina-4vnbapyp96.pdf

Perceptual saccadic suppression starts in the retina

Brief visual stimuli are robustly mislocalized around the time of saccades. Such mislocalization is thought to arise because oculomotor and visual neural maps distort space through foveal magnifica...

/pdf/perisaccadic-perceptual-mislocalization-is-different-for-3m03th5vjf.pdf

Perisaccadic perceptual mislocalization is different for upward saccades.

Brain orexin (hypocretin) neurons are implicated in sleep-wake switching and reward-seeking but their roles in rapid arousal dynamics and reward perception are unclear. Here, cell-specific stimulation, deletion and in vivo recordings revealed strong correlative and causal links between pupil dilation-a quantitative arousal marker-and orexin cell activity. Coding of arousal and reward was distributed across orexin cells, indicating that they specialize in rapid, multiplexed communication of momentary arousal and reward states. 

/pdf/control-and-coding-of-pupil-size-by-hypothalamic-orexin-2z4a6i11.pdf

Control and coding of pupil size by hypothalamic orexin neurons

Saccadic eye movements, which dramatically alter retinal images, are associated with robust peri-movement perceptual alterations. Such alterations, thought to reflect brain mechanisms for maintaining perceptual stability in the face of saccade-induced retinal-image disruptions, are often studied by asking subjects to localize brief stimuli presented around the time of horizontal saccades. However, other saccade directions are not usually explored. Motivated by recently discovered asymmetries in upper and lower visual field representations in the superior colliculus, a structure important for both saccade generation and visual analysis, here we observed significant differences in peri-saccadic perceptual alterations for upward saccades relative to other saccade directions. We also found that, even for purely horizontal saccades, perceptual alterations differ for upper versus lower retinotopic stimulus locations. Our results, coupled with conceptual modeling, suggest that peri-saccadic perceptual alterations might critically depend on neural circuits, like superior colliculus, that asymmetrically represent the upper and lower visual fields.

https://www.biorxiv.org/content/biorxiv/early/2018/05/29/333112.full.pdf

Peri-saccadic perceptual mislocalization is different for upward saccades

Appropriate arousal in our brains critically relies on hypothalamic hypocretin/orexin neurons (HONs). HON activity regulation has been a subject of intense research, uncovering slow responses to nutrients and hormones, and fast responses to external sensory inputs. However, it remains unclear whether HONs also respond to statistical patterns in the environment. Among these, reward probability and uncertainty are fundamental measures of information that enable evaluation of predictions, and guide diverse aspects of cognition such as learning and motivation. Using different cues to denote reward likelihood across the full probability range (0-1), we found that HON population responses to the reward-predicting cues co-vary with reward uncertainty. Single-cell analyses additionally revealed HON subsets specializing in monotonic representations of probability, as well as cells sharply tuned to uncertainty. Furthermore, simultaneous recordings of HONs and midbrain dopamine neurons (DANs) indicated that HONs and DANs diverge in their coding of reward probability, both in responses to reward-predicting cues and to rewards. These results demonstrate previously unseen coding of reward expectation in genetically-defined hypothalamic cells central to clinical conditions and neurobehavioral physiology, and suggest a possible role for HONs in converting reward statistics into arousal-based allocation of cognitive and autonomic resources.

/pdf/coding-of-reward-uncertainty-and-probability-by-orexin-1cnnex09.pdf

Coding of reward uncertainty and probability by orexin neurons

Activation of hypothalamic hypocretin/orexin neurons (HONs) is a neural substrate of arousal. HONs activate during sensory stimuli, and are thus thought to regulate arousal according to sensory input. Here, we measured body movements occurring during sound cues or associated reward outcomes, and used an encoding model to ask whether HONs indeed specialize in tracking certain features, or multiplex diverse types of features. Although some single HONs multiplexed feature combinations, during the cue period the overall HON signal primarily tracked body movements. This persisted across cues signaling different reward probabilities, and substantially diverged from reward-probability tracking in concurrently-recorded VTA dopamine neurons. In contrast, during reward outcome, HONs predominantly signaled the presence or absence of reward, and not body movements, nor surprise or reward prediction error. These results describe an unexpectedly specialized and flexible logic of HON activation, suggesting a role for HONs in tracking actions and subsequent reinforcements.

/pdf/do-orexin-hypocretin-neurons-track-sensory-cognitive-or-2ahd2oxs.pdf

Nikola Grujic

Papers

Perisaccadic perceptual mislocalization is different for upward saccades.

Control and coding of pupil size by hypothalamic orexin neurons

Peri-saccadic perceptual mislocalization is different for upward saccades

Coding of reward uncertainty and probability by orexin neurons

Do orexin/hypocretin neurons track sensory, cognitive, or motor information?