Representational geometry of perceptual decisions in the monkey parietal cortex.

Lateral intraparietal (LIP) neurons represent formation of perceptual decisions involving eye movements. In circuit models for these decisions, neural ensembles that encode actions compete to form decisions. Consequently, representation and readout of the decision variables (DVs) are implemented similarly for decisions with identical competing actions, irrespective of input and task context differences. Further, DVs are encoded as partially potentiated action plans through balance of activity of action-selective ensembles. Here, we test those core principles. We show that in a novel face-discrimination task, LIP firing rates decrease with supporting evidence, contrary to conventional motion-discrimination tasks. These opposite response patterns arise from similar mechanisms in which decisions form along curved population-response manifolds misaligned with action representations. These manifolds rotate in state space based on context, indicating distinct optimal readouts for different tasks. We show similar manifolds in lateral and medial prefrontal cortices, suggesting similar representational geometry across decision-making circuits.

Development of Concurrent Retinotopic Maps in the Fly Motion Detection Circuit.

Understanding how complex brain wiring is produced during development is a daunting challenge. In Drosophila, information from 800 retinal ommatidia is processed in distinct brain neuropiles, each subdivided into 800 matching retinotopic columns. The lobula plate comprises four T4 and four T5 neuronal subtypes. T4 neurons respond to bright edge motion, whereas T5 neurons respond to dark edge motion. Each is tuned to motion in one of the four cardinal directions, effectively establishing eight concurrent retinotopic maps to support wide-field motion. We discovered a mode of neurogenesis where two sequential Notch-dependent divisions of either a horizontal or a vertical progenitor produce matching sets of two T4 and two T5 neurons retinotopically coincident with pairwise opposite direction selectivity. We show that retinotopy is an emergent characteristic of this neurogenic program and derives directly from neuronal birth order. Our work illustrates how simple developmental rules can implement complex neural organization.

Cortical Integration of Vestibular and Visual Cues for Navigation, Visual Processing, and Perception.

Despite increasing evidence of its involvement in several key functions of the cerebral cortex, the vestibular sense rarely enters our consciousness. Indeed, the extent to which these internal signals are incorporated within cortical sensory representation and how they might be relied upon for sensory-driven decision-making, during, for example, spatial navigation, is yet to be understood. Recent novel experimental approaches in rodents have probed both the physiological and behavioral significance of vestibular signals and indicate that their widespread integration with vision improves both the cortical representation and perceptual accuracy of self-motion and orientation. Here, we summarize these recent findings with a focus on cortical circuits involved in visual perception and spatial navigation and highlight the major remaining knowledge gaps. We suggest that vestibulo-visual integration reflects a process of constant updating regarding the status of self-motion, and access to such information by the cortex is used for sensory perception and predictions that may be implemented for rapid, navigation-related decision-making.

How Flies See Motion.

How neurons detect the direction of motion is a prime example of neural computation: Motion vision is found in the visual systems of virtually all sighted animals, it is important for survival, and it requires interesting computations with well-defined linear and nonlinear processing steps-yet the whole process is of moderate complexity. The genetic methods available in the fruit fly Drosophila and the charting of a connectome of its visual system have led to rapid progress and unprecedented detail in our understanding of how neurons compute the direction of motion in this organism. The picture that emerged incorporates not only the identity, morphology, and synaptic connectivity of each neuron involved but also its neurotransmitters, its receptors, and their subcellular localization. Together with the neurons' membrane potential responses to visual stimulation, this information provides the basis for a biophysically realistic model of the circuit that computes the direction of visual motion.

Motion detection: neuronal circuit meets theory.

Motion detection in fly vision has been investigated experimentally and theoretically for half of a century, yet mechanistic insights into the neuronal computation have only started to emerge. In a recent issue of Nature, two studies provide major insights into how motion direction is extracted from the image flow projected onto the retina.

Odour motion sensing enhances navigation of complex plumes.

Odour plumes in the wild are spatially complex and rapidly fluctuating structures carried by turbulent airflows1-4. To successfully navigate plumes in search of food and mates, insects must extract and integrate multiple features of the odour signal, including odour identity5, intensity6 and timing6-12. Effective navigation requires balancing these multiple streams of olfactory information and integrating them with other sensory inputs, including mechanosensory and visual cues9,12,13. Studies dating back a century have indicated that, of these many sensory inputs, the wind provides the main directional cue in turbulent plumes, leading to the longstanding model of insect odour navigation as odour-elicited upwind motion6,8-12,14,15. Here we show that Drosophila melanogaster shape their navigational decisions using an additional directional cue-the direction of motion of odours-which they detect using temporal correlations in the odour signal between their two antennae. Using a high-resolution virtual-reality paradigm to deliver spatiotemporally complex fictive odours to freely walking flies, we demonstrate that such odour-direction sensing involves algorithms analogous to those in visual-direction sensing16. Combining simulations, theory and experiments, we show that odour motion contains valuable directional information that is absent from the airflow alone, and that both Drosophila and virtual agents are aided by that information in navigating naturalistic plumes. The generality of our findings suggests that odour-direction sensing may exist throughout the animal kingdom and could improve olfactory robot navigation in uncertain environments.

Human subcortical pathways automatically detect collision trajectory without attention and awareness.

Detecting imminent collisions is essential for survival. Here, we used high-resolution fMRI at 7 Tesla to investigate the role of attention and consciousness for detecting collision trajectory in human subcortical pathways. Healthy participants can precisely discriminate collision from near-miss trajectory of an approaching object, with pupil size change reflecting collision sensitivity. Subcortical pathways from the superior colliculus (SC) to the ventromedial pulvinar (vmPul) and ventral tegmental area (VTA) exhibited collision-sensitive responses even when participants were not paying attention to the looming stimuli. For hemianopic patients with unilateral lesions of the geniculostriate pathway, the ipsilesional SC and VTA showed significant activation to collision stimuli in their scotoma. Furthermore, stronger SC responses predicted better behavioral performance in collision detection even in the absence of awareness. Therefore, human tectofugal pathways could automatically detect collision trajectories without the observers' attention to and awareness of looming stimuli, supporting "blindsight" detection of impending visual threats.

Integrated Perceptual Decisions Rely on Parallel Evidence Accumulation.

The ability to make accurate and timely decisions, such as judging when it is safe to cross the road, is the foundation of adaptive behavior. While the computational and neural processes supporting simple decisions on isolated stimuli have been well characterized, decision-making in the real world often requires integration of discrete sensory events over time and space. Most previous experimental work on perceptual decision-making has focused on tasks that involve only a single, task-relevant source of sensory input. It remains unclear, therefore, how such integrative decisions are regulated computationally. Here we used psychophysics, electroencephalography, and computational modeling to understand how the human brain combines visual motion signals across space in the service of a single, integrated decision. To that purpose, we presented two random-dot kinematograms in the left and the right visual hemifields. Coherent motion signals were shown briefly and concurrently in each location, and healthy adult human participants of both sexes reported the average of the two motion signals. We directly tested competing predictions arising from influential serial and parallel accounts of visual processing. Using a biologically plausible model of motion filtering, we found evidence in favor of parallel integration as the fundamental computational mechanism regulating integrated perceptual decisions.

Distinct Cortical Correlates of Perception and Motor Function in Balance Control.

Fluctuations in brain activity alter how we perceive our body and generate movements but have not been investigated in functional whole-body behaviors. During reactive balance, we recently showed that evoked brain activity is associated with the balance ability in young individuals. Furthermore, in PD, impaired whole-body motion perception in reactive balance is associated with impaired balance. Here, we investigated the brain activity during the whole-body motion perception in reactive balance in young adults (9 female, 10 male). We hypothesized that both ongoing and evoked cortical activity influences the efficiency of information processing for successful perception and movement during whole-body behaviors. We characterized two cortical signals using electroencephalography localized to the SMA: (1) the "N1," a perturbation-evoked potential that decreases in amplitude with expectancy and is larger in individuals with lower balance function, and (2) preperturbation ß power, a transient rhythm that favors maintenance of the current sensorimotor state and is inversely associated with tactile perception. In a two-alternative forced choice task, participants judged whether pairs of backward support surface perturbations during standing were in the "same" or "different" direction. As expected, lower whole-body perception was associated with lower balance ability. Within a perturbation pair, N1 attenuation was larger on correctly perceived trials and associated with better balance, but not perception. In contrast, preperturbation ß power was higher on incorrectly perceived trials and associated with poorer perception, but not balance. Together, ongoing and evoked cortical activity have unique roles in information processing that give rise to distinct associations with perceptual and balance ability.

Transformation of Motion Pattern Selectivity from Retina to Superior Colliculus.

The superior colliculus (SC) is a prominent and conserved visual center in all vertebrates. In mice, the most superficial lamina of the SC is enriched with neurons that are selective for the moving direction of visual stimuli. Here, we study how these direction selective neurons respond to complex motion patterns known as plaids, using two-photon calcium imaging in awake male and female mice. The plaid pattern consists of two superimposed sinusoidal gratings moving in different directions, giving an apparent pattern direction that lies between the directions of the two component gratings. Most direction selective neurons in the mouse SC respond robustly to the plaids and show a high selectivity for the moving direction of the plaid pattern but not of its components. Pattern motion selectivity is seen in both excitatory and inhibitory SC neurons and is especially prevalent in response to plaids with large cross angles between the two component gratings. However, retinal inputs to the SC are ambiguous in their selectivity to pattern versus component motion. Modeling suggests that pattern motion selectivity in the SC can arise from a nonlinear transformation of converging retinal inputs. In contrast, the prevalence of pattern motion selective neurons is not seen in the primary visual cortex (V1). These results demonstrate an interesting difference between the SC and V1 in motion processing and reveal the SC as an important site for encoding pattern motion.

Differential Expression Analysis Identifies Candidate Synaptogenic Molecules for Wiring Direction-Selective Circuits in the Retina.

An organizational feature of neural circuits is the specificity of synaptic connections. A striking example is the direction-selective (DS) circuit of the retina. There are multiple subtypes of DS retinal ganglion cells (DSGCs) that prefer motion along one of four preferred directions. This computation is mediated by selective wiring of a single inhibitory interneuron, the starburst amacrine cell (SAC), with each DSGC subtype preferentially receiving input from a subset of SAC processes. We hypothesize that the molecular basis of this wiring is mediated in part by unique expression profiles of DSGC subtypes. To test this, we first performed paired recordings from isolated mouse retinas of both sexes to determine that postnatal day 10 (P10) represents the age at which asymmetric synapses form. Second, we performed RNA sequencing and differential expression analysis on isolated P10 ON-OFF DSGCs tuned for either nasal or ventral motion and identified candidates which may promote direction-specific wiring. We then used a conditional knock-out strategy to test the role of one candidate, the secreted synaptic organizer cerebellin-4 (Cbln4), in the development of DS tuning. Using two-photon calcium imaging, we observed a small deficit in directional tuning among ventral-preferring DSGCs lacking Cbln4, though whole-cell voltage-clamp recordings did not identify a significant change in inhibitory inputs. This suggests that Cbln4 does not function primarily via a cell-autonomous mechanism to instruct wiring of DS circuits. Nevertheless, our transcriptomic analysis identified unique candidate factors for gaining insights into the molecular mechanisms that instruct wiring specificity in the DS circuit.

Visual Circuits for Direction Selectivity.

Images projected onto the retina of an animal eye are rarely still. Instead, they usually contain motion signals originating either from moving objects or from retinal slip caused by self-motion. Accordingly, motion signals tell the animal in which direction a predator, prey, or the animal itself is moving. At the neural level, visual motion detection has been proposed to extract directional information by a delay-and-compare mechanism, representing a classic example of neural computation. Neurons responding selectively to motion in one but not in the other direction have been identified in many systems, most prominently in the mammalian retina and the fly optic lobe. Technological advances have now allowed researchers to characterize these neurons' upstream circuits in exquisite detail. Focusing on these upstream circuits, we review and compare recent progress in understanding the mechanisms that generate direction selectivity in the early visual system of mammals and flies.

The Role of the Lateral Intraparietal Area in (the Study of) Decision Making.

Over the past two decades, neurophysiological responses in the lateral intraparietal area (LIP) have received extensive study for insight into decision making. In a parallel manner, inferred cognitive processes have enriched interpretations of LIP activity. Because of this bidirectional interplay between physiology and cognition, LIP has served as fertile ground for developing quantitative models that link neural activity with decision making. These models stand as some of the most important frameworks for linking brain and mind, and they are now mature enough to be evaluated in finer detail and integrated with other lines of investigation of LIP function. Here, we focus on the relationship between LIP responses and known sensory and motor events in perceptual decision-making tasks, as assessed by correlative and causal methods. The resulting sensorimotor-focused approach offers an account of LIP activity as a multiplexed amalgam of sensory, cognitive, and motor-related activity, with a complex and often indirect relationship to decision processes. Our data-driven focus on multiplexing (and de-multiplexing) of various response components can complement decision-focused models and provides more detailed insight into how neural signals might relate to cognitive processes such as decision making.

Noncortical coding of biological motion in newborn chicks' brain.

Biological motion, the typical movement of vertebrates, is perceptually salient for many animal species. Newly hatched domestic chicks and human newborns show a spontaneous preference for simple biological motion stimuli (point-light displays) at birth prior to any visual learning. Despite evidence of such preference at birth, neural studies performed so far have focused on a specialized neural network involving primarily cortical areas. Here, we presented newly hatched visually naïve domestic chicks to either biological or rigid motion stimuli and measured for the first time their brain activation. Immediate Early Gene (c-Fos) expression revealed selective activation in the preoptic area of the hypothalamus and the nucleus taeniae of the amygdala. These results suggest that subpallial/subcortical regions play a crucial role in biological motion perception at hatching, paving the way for future studies on adult animals, including humans.

Distinct neural markers of evidence accumulation index metacognitive processing before and after simple visual decisions.

Perceptual decision-making is affected by uncertainty arising from the reliability of incoming sensory evidence (perceptual uncertainty) and the categorization of that evidence relative to a choice boundary (categorical uncertainty). Here, we investigated how these factors impact the temporal dynamics of evidence processing during decision-making and subsequent metacognitive judgments. Participants performed a motion discrimination task while electroencephalography was recorded. We manipulated perceptual uncertainty by varying motion coherence, and categorical uncertainty by varying the angular offset of motion signals relative to a criterion. After each trial, participants rated their desire to change their mind. High uncertainty impaired perceptual and metacognitive judgments and reduced the amplitude of the centro-parietal positivity, a neural marker of evidence accumulation. Coherence and offset affected the centro-parietal positivity at different time points, suggesting that perceptual and categorical uncertainty affect decision-making in sequential stages. Moreover, the centro-parietal positivity predicted participants' metacognitive judgments: larger predecisional centro-parietal positivity amplitude was associated with less desire to change one's mind, whereas larger postdecisional centro-parietal positivity amplitude was associated with greater desire to change one's mind, but only following errors. These findings reveal a dissociation between predecisional and postdecisional evidence processing, suggesting that the CPP tracks potentially distinct cognitive processes before and after a decision.

Modality-specific effects of threat on self-motion perception.

BACKGROUND: Threat and individual differences in threat-processing bias perception of stimuli in the environment. Yet, their effect on perception of one's own (body-based) self-motion in space is unknown. Here, we tested the effects of threat on self-motion perception using a multisensory motion simulator with concurrent threatening or neutral auditory stimuli. RESULTS: Strikingly, threat had opposite effects on vestibular and visual self-motion perception, leading to overestimation of vestibular, but underestimation of visual self-motions. Trait anxiety tended to be associated with an enhanced effect of threat on estimates of self-motion for both modalities. CONCLUSIONS: Enhanced vestibular perception under threat might stem from shared neural substrates with emotional processing, whereas diminished visual self-motion perception may indicate that a threatening stimulus diverts attention away from optic flow integration. Thus, threat induces modality-specific biases in everyday experiences of self-motion.

Representation of Motion Direction in Visual Area MT Accounts for High Sensitivity to Centripetal Motion, Aligning with Efficient Coding of Retinal Motion Statistics.

The overrepresentation of centrifugal motion in the middle temporal visual area (area MT) has long been thought to provide an efficient coding strategy for optic flow processing. However, this overrepresentation compromises the detection of approaching objects, which is essential for survival. In the present study, we revisited this long-held notion by reanalyzing motion selectivity in area MT of three macaque monkeys (two males, one female) using random-dot stimuli instead of spot stimuli. We found no differences in the number of neurons tuned to centrifugal versus centripetal motion; however, centrifugally tuned neurons showed stronger tuning than centripetally tuned neurons. This was attributed to the heightened suppression of responses in centrifugal neurons to centripetal motion compared with that of centripetal neurons to centrifugal motion. Our modeling implies that this intensified suppression accounts for superior detection performance for weak centripetal motion stimuli. Moreover, through Fisher information analysis, we establish that the population sensitivity to motion direction in peripheral vision corresponds well with retinal motion statistics during forward locomotion. While these results challenge established concepts, considering the interplay of logarithmic Gaussian receptive fields and spot stimuli can shed light on the previously documented overrepresentation of centrifugal motion. Significantly, our findings reconcile a previously found discrepancy between MT activity and human behavior, highlighting the proficiency of peripheral MT neurons in encoding motion direction efficiently.SIGNIFICANCE STATEMENT The efficient coding hypothesis states that sensory neurons are tuned to specific, frequently experienced stimuli. Whereas previous work has found that neurons in the middle temporal (MT) area favor centrifugal motion, which results from forward locomotion, we show here that there is no such bias. Moreover, we found that the response of centrifugal neurons for centripetal motion was more suppressed than that of centripetal neurons for centrifugal motion. Combined with modeling, this provides a solution to a previously known discrepancy between reported centrifugal bias in MT and better detection of centripetal motion by human observers. Additionally, we show that population sensitivity in peripheral MT neurons conforms to an efficient code of retinal motion statistics during forward locomotion.

Neurons in Primate Area MSTd Signal Eye Movement Direction Inferred from Dynamic Perspective Cues in Optic Flow.

Smooth eye movements are common during natural viewing; we frequently rotate our eyes to track moving objects or to maintain fixation on an object during self-movement. Reliable information about smooth eye movements is crucial to various neural computations, such as estimating heading from optic flow or judging depth from motion parallax. While it is well established that extraretinal signals (e.g., efference copies of motor commands) carry critical information about eye velocity, the rotational optic flow field produced by eye rotations also carries valuable information. Although previous work has shown that dynamic perspective cues in optic flow can be used in computations that require estimates of eye velocity, it has remained unclear where and how the brain processes these visual cues and how they are integrated with extraretinal signals regarding eye rotation. We examined how neurons in the dorsal region of the medial superior temporal area (MSTd) of two male rhesus monkeys represent the direction of smooth pursuit eye movements based on both visual cues (dynamic perspective) and extraretinal signals. We find that most MSTd neurons have matched preferences for the direction of eye rotation based on visual and extraretinal signals. Moreover, neural responses to combinations of these signals are well predicted by a weighted linear summation model. These findings demonstrate a neural substrate for representing the velocity of smooth eye movements based on rotational optic flow and establish area MSTd as a key node for integrating visual and extraretinal signals into a more generalized representation of smooth eye movements.SIGNIFICANCE STATEMENT We frequently rotate our eyes to smoothly track objects of interest during self-motion. Information about eye velocity is crucial for a variety of computations performed by the brain, including depth perception and heading perception. Traditionally, information about eye rotation has been thought to arise mainly from extraretinal signals, such as efference copies of motor commands. Previous work shows that eye velocity can also be inferred from rotational optic flow that accompanies smooth eye movements, but the neural origins of these visual signals about eye rotation have remained unknown. We demonstrate that macaque neurons signal the direction of smooth eye rotation based on visual signals, and that they integrate both visual and extraretinal signals regarding eye rotation in a congruent fashion.

Effect of a False Inertial Cue in the Velocity-Storage Circuit on Head Posture and Inertia Perception.

The velocity-storage circuit participates in the vestibulopostural reflex, but its role in the postural reflex requires further elucidation. The velocity-storage circuit differentiates gravitoinertial information into gravitational and inertial cues using rotational cues. This implies that a false rotational cue can cause an erroneous estimation of gravity and inertial cues. We hypothesized the velocity-storage circuit is a common gateway for all vestibular reflex pathways and tested that hypothesis by measuring the postural and perceptual responses from a false inertial cue estimated in the velocity-storage circuit. Twenty healthy human participants (40.5 ± 8.2 years old, 6 men) underwent two different sessions of earth-vertical axis rotations at 120°/s for 60 s. During each session, the participants were rotated clockwise and then counterclockwise with two different starting head positions (head-down and head-up). During the first (control) session, the participants kept a steady head position at the end of rotation. During the second (test) session, the participants changed their head position at the end of rotation, from head-down to head-up or vice versa. The head position and inertial motion perception at the end of rotation were aligned with the inertia direction anticipated by the velocity-storage model. The participants showed a significant correlation between postural and perceptual responses. The velocity-storage circuit appears to be a shared neural integrator for the vestibulopostural reflex and vestibular perception. Because the postural responses depended on the inertial direction, the postural instability in vestibular disorders may be the consequence of the vestibulopostural reflex responding to centrally estimated false vestibular cues.SIGNIFICANCE STATEMENT The velocity-storage circuit appears to participate in the vestibulopostural reflex, which stabilizes the head and body position in space. However, it is still unclear whether the velocity-storage circuit for the postural reflex is in common with that involved in eye movement and perception. We evaluated the postural and perceptual responses to a false inertial cue estimated by the velocity-storage circuit. The postural and perceptual responses were consistent with the inertia direction predicted in the velocity-storage model and were correlated closely with each other. These results show that the velocity-storage circuit is a shared neural integrator for vestibular-driven responses and suggest that the vestibulopostural response to a false vestibular cue is the pathomechanism of postural instability clinically observed in vestibular disorders.

A Visual Pathway into Central Complex for High-Frequency Motion-Defined Bars in Drosophila.

Relative motion breaks a camouflaged target from a same-textured background, thus eliciting discrimination of a motion-defined object. Ring (R) neurons are critical components in the Drosophila central complex, which has been implicated in multiple visually guided behaviors. Using two-photon calcium imaging with female flies, we demonstrated that a specific population of R neurons that innervate the superior domain of bulb neuropil, termed superior R neurons, encoded a motion-defined bar with high spatial frequency contents. Upstream superior tuberculo-bulbar (TuBu) neurons transmitted visual signals by releasing acetylcholine within synapses connected with superior R neurons. Blocking TuBu or R neurons impaired tracking performance of the bar, which reveals their importance in motion-defined feature encoding. Additionally, the presentation of a low spatial frequency luminance-defined bar evoked consistent excitation in R neurons of the superior bulb, whereas either excited or inhibited responses were evoked in the inferior bulb. The distinct properties of the responses to the two bar stimuli indicate there is a functional division between the bulb subdomains. Moreover, physiological and behavioral tests with restricted lines suggest that R4d neurons play a vital role in tracking motion-defined bars. We conclude that the central complex receives the motion-defined features via a visual pathway from superior TuBu to R neurons and might encode different visual features via distinct response patterns at the population level, thereby driving visually guided behaviors.SIGNIFICANCE STATEMENT Animals could discriminate a motion-defined object that is indistinguishable with a same-textured background until it moves, but little is known about the underlying neural mechanisms. In this study, we identified that R neurons and their upstream partners, TuBu neurons, innervating the superior bulb of Drosophila central brain are involved in the discrimination of high-frequency motion-defined bars. Our study provides new evidence that R neurons receive multiple visual inputs from distinct upstream neurons, indicating a population coding mechanism for the fly central brain to discriminate diverse visual features. These results build progress in unraveling neural substrates for visually guided behaviors.