Human navigation strategies and their errors result from dynamic interactions of spatial uncertainties.

Goal-directed navigation requires continuously integrating uncertain self-motion and landmark cues into an internal sense of location and direction, concurrently planning future paths, and sequentially executing motor actions. Here, we provide a unified account of these processes with a computational model of probabilistic path planning in the framework of optimal feedback control under uncertainty. This model gives rise to diverse human navigational strategies previously believed to be distinct behaviors and predicts quantitatively both the errors and the variability of navigation across numerous experiments. This furthermore explains how sequential egocentric landmark observations form an uncertain allocentric cognitive map, how this internal map is used both in route planning and during execution of movements, and reconciles seemingly contradictory results about cue-integration behavior in navigation. Taken together, the present work provides a parsimonious explanation of how patterns of human goal-directed navigation behavior arise from the continuous and dynamic interactions of spatial uncertainties in perception, cognition, and action.

Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation.

Reorientation, the process of regaining one's bearings after becoming lost, requires identification of a spatial context (context recognition) and recovery of facing direction within that context (heading retrieval). We previously showed that these processes rely on the use of features and geometry, respectively. Here, we examine reorientation behavior in a task that creates contextual ambiguity over a long timescale to demonstrate that male mice learn to combine both featural and geometric cues to recover heading. At the neural level, most CA1 neurons persistently align to geometry, and this alignment predicts heading behavior. However, a small subset of cells remaps coherently in a context-sensitive manner, which serves to predict context. Efficient heading retrieval and context recognition correlate with rate changes reflecting integration of featural and geometric information in the active ensemble. These data illustrate how context recognition and heading retrieval are coded in CA1 and how these processes change with experience.

How does V1 population activity inform perceptual certainty?

Neural population activity in sensory cortex informs our perceptual interpretation of the environment. Oftentimes, this population activity will support multiple alternative interpretations. The larger the spread of probability over different alternatives, the more uncertain the selected perceptual interpretation. We test the hypothesis that the reliability of perceptual interpretations can be revealed through simple transformations of sensory population activity. We recorded V1 population activity in fixating macaques while presenting oriented stimuli under different levels of nuisance variability and signal strength. We developed a decoding procedure to infer from V1 activity the most likely stimulus orientation as well as the certainty of this estimate. Our analysis shows that response magnitude, response dispersion, and variability in response gain all offer useful proxies for orientation certainty. Of these three metrics, the last one has the strongest association with the decoder's uncertainty estimates. These results clarify that the nature of neural population activity in sensory cortex provides downstream circuits with multiple options to assess the reliability of perceptual interpretations.

Do microsaccades vary with discriminability around the visual field?

Microsaccades-tiny fixational eye movements-improve discriminability in high-acuity tasks in the foveola. To investigate whether they help compensate for low discriminability at the perifovea, we examined microsaccade characteristics relative to the adult visual performance field, which is characterized by two perceptual asymmetries: horizontal-vertical anisotropy (better discrimination along the horizontal than vertical meridian) and vertical meridian asymmetry (better discrimination along the lower than upper vertical meridian). We investigated whether and to what extent microsaccade directionality varies when stimuli are at isoeccentric locations along the cardinals under conditions of heterogeneous discriminability (Experiment 1) and homogeneous discriminability, equated by adjusting stimulus contrast (Experiment 2). Participants performed a two-alternative forced-choice orientation discrimination task. In both experiments, performance was better on trials without microsaccades between ready signal onset and stimulus offset than on trials with microsaccades. Across the trial sequence, the microsaccade rate and directional pattern were similar across locations. Our results indicate that microsaccades were similar regardless of stimulus discriminability and target location, except during the response period-once the stimuli were no longer present and target location no longer uncertain-when microsaccades were biased toward the target location. Thus, this study reveals that microsaccades do not flexibly adapt as a function of varying discriminability in a basic visual task around the visual field.

Development and organization of the retinal orientation selectivity map.

Orientation or axial selectivity, the property of neurons in the visual system to respond preferentially to certain angles of visual stimuli, plays a pivotal role in our understanding of visual perception and information processing. This computation is performed as early as the retina, and although much work has established the cellular mechanisms of retinal orientation selectivity, how this computation is organized across the retina is unknown. Using a large dataset collected across the mouse retina, we demonstrate functional organization rules of retinal orientation selectivity. First, we identify three major functional classes of retinal cells that are orientation selective and match previous descriptions. Second, we show that one orientation is predominantly represented in the retina and that this predominant orientation changes as a function of retinal location. Third, we demonstrate that neural activity plays little role on the organization of retinal orientation selectivity. Lastly, we use in silico modeling followed by validation experiments to demonstrate that the overrepresented orientation aligns along concentric axes. These results demonstrate that, similar to direction selectivity, orientation selectivity is organized in a functional map as early as the retina.

Transfer of visual perceptual learning over a task-irrelevant feature through feature-invariant representations: Behavioral experiments and model simulations.

A large body of literature has examined specificity and transfer of perceptual learning, suggesting a complex picture. Here, we distinguish between transfer over variations in a "task-relevant" feature (e.g., transfer of a learned orientation task to a different reference orientation) and transfer over a "task-irrelevant" feature (e.g., transfer of a learned orientation task to a different retinal location or different spatial frequency), and we focus on the mechanism for the latter. Experimentally, we assessed whether learning a judgment of one feature (such as orientation) using one value of an irrelevant feature (e.g., spatial frequency) transfers to another value of the irrelevant feature. Experiment 1 examined whether learning in eight-alternative orientation identification with one or multiple spatial frequencies transfers to stimuli at five different spatial frequencies. Experiment 2 paralleled Experiment 1, examining whether learning in eight-alternative spatial-frequency identification at one or multiple orientations transfers to stimuli with five different orientations. Training the orientation task with a single spatial frequency transferred widely to all other spatial frequencies, with a tendency to specificity when training with the highest spatial frequency. Training the spatial frequency task fully transferred across all orientations. Computationally, we extended the identification integrated reweighting theory (I-IRT) to account for the transfer data (Dosher, Liu, & Lu, 2023; Liu, Dosher, & Lu, 2023). Just as location-invariant representations in the original IRT explain transfer over retinal locations, incorporating feature-invariant representations effectively accounted for the observed transfer. Taken together, we suggest that feature-invariant representations can account for transfer of learning over a "task-irrelevant" feature.

Magnetic orientation in juvenile Atlantic herring (Clupea harengus) could involve cryptochrome 4 as a potential magnetoreceptor.

The Earth's magnetic field can provide reliable directional information, allowing migrating animals to orient themselves using a magnetic compass or estimate their position relative to a target using map-based orientation. Here we show for the first time that young, inexperienced herring (Clupea harengus, Ch) have a magnetic compass when they migrate hundreds of kilometres to their feeding grounds. In birds, such as the European robin (Erithacus rubecula), radical pair-based magnetoreception involving cryptochrome 4 (ErCRY4) was demonstrated; the molecular basis of magnetoreception in fish is still elusive. We show that cry4 expression in the eye of herring is upregulated during the migratory season, but not before, indicating a possible use for migration. The amino acid structure of herring ChCRY4 shows four tryptophans and a flavin adenine dinucleotide-binding site, a prerequisite for a magnetic receptor. Using homology modelling, we successfully reconstructed ChCRY4 of herring, DrCRY4 of zebrafish (Danio rerio) and StCRY4 of brown trout (Salmo trutta) and showed that ChCRY4, DrCRY4 and ErCRY4a, but not StCRY4, exhibit very comparable dynamic behaviour. The electron transfer could take place in ChCRY4 in a similar way to ErCRY4a. The combined behavioural, transcriptomic and simulation experiments provide evidence that CRY4 could act as a magnetoreceptor in Atlantic herring.

A spatial version of the Stroop task for examining proactive and reactive control independently from non-conflict processes.

Conflict-induced control refers to humans' ability to regulate attention in the processing of target information (e.g., the color of a word in the color-word Stroop task) based on experience with conflict created by distracting information (e.g., an incongruent color word), and to do so either in a proactive (preparatory) or a reactive (stimulus-driven) fashion. Interest in conflict-induced control has grown recently, as has the awareness that effects attributed to those processes might be affected by conflict-unrelated processes (e.g., the learning of stimulus-response associations). This awareness has resulted in the recommendation to move away from traditional interference paradigms with small stimulus/response sets and towards paradigms with larger sets (at least four targets, distractors, and responses), paradigms that allow better control of non-conflict processes. Using larger sets, however, is not always feasible. Doing so in the Stroop task, for example, would require either multiple arbitrary responses that are difficult for participants to learn (e.g., manual responses to colors) or non-arbitrary responses that can be difficult for researchers to collect (e.g., vocal responses in online experiments). Here, we present a spatial version of the Stroop task that solves many of those problems. In this task, participants respond to one of six directions indicated by an arrow, each requiring a specific, non-arbitrary manual response, while ignoring the location where the arrow is displayed. We illustrate the usefulness of this task by showing the results of two experiments in which evidence for proactive and reactive control was obtained while controlling for the impact of non-conflict processes.

Online corrections can occur within movement imagery: An investigation of the motor-cognitive model.

The motor-cognitive model proposes that movement imagery additionally requires conscious monitoring owing to an absence of veridical online sensory feedback. Therefore, it is predicted that there would be a comparatively limited ability for individuals to update or correct movement imagery as they could within execution. To investigate, participants executed and imagined target-directed aiming movements featuring either an unexpected target perturbation (Exp. 1) or removal of visual sensory feedback (Exp. 2). The results of both experiments indicated that the time-course of executed and imagined movements was equally influenced by each of these online visual manipulations. Thus, contrary to some of the tenets of the motor-cognitive model, movement imagery holds the capacity to interpolate online corrections despite the absence of veridical sensory feedback. The further theoretical implications of these findings are discussed.

Collision avoidance behaviours while young adults avoid a virtual pedestrian approaching on a 45° angle under attentionally demanding conditions.

Individuals rely on visual information to determine when to adapt their behaviours (i.e., by changing path and/or speed) to avoid an approaching object or person. After initiating an avoidance behaviour, individuals may control the space (i.e., minimum clearance distance) between themselves and another person or object. The current study aimed to determine the action strategies of young adults while avoiding a virtual pedestrian approaching along a 45° angle in an attentionally demanding task. Twenty-one young adults (22.9 ± 1.9 yrs., 11 males) were immersed in a virtual environment and were instructed to walk along a 7.5 m path towards a goal located along the midline. Two virtual pedestrians (VP) positioned 2.83 m to the left and right of the midline approached participants on a 45° angle. To manipulate the point at which the participants and the VP would intersect during different trials, the VP approached at one of three speeds: 0.8×, 1.0×, or 1.2× each participants' average walking speed. Participants were instructed to walk to a goal without colliding with the VP while performing the attention task; reporting whether a shape changed above the VPs' heads. Results revealed that young adults did not modulate their timing of avoidance to the approach characteristics of the VP, as they consistently avoided the collision 1.67 s after the VP began moving. However, young adults seem to control how they avoid an oncoming collision by maintaining a consistent safety margin after an avoidance behaviour was initiated.

Tactile adaptation to orientation produces a robust tilt aftereffect and exhibits crossmodal transfer when tested in vision.

Orientation processing is one of the most fundamental functions in both visual and somatosensory perception. Converging findings suggest that orientation processing in both modalities is closely linked: somatosensory neurons share a similar orientation organisation as visual neurons, and the visual cortex has been found to be heavily involved in tactile orientation perception. Hence, we hypothesized that somatosensation would exhibit a similar orientation adaptation effect, and this adaptation effect would be transferable between the two modalities, considering the above-mentioned connection. The tilt aftereffect (TAE) is a demonstration of orientation adaptation and is used widely in behavioural experiments to investigate orientation mechanisms in vision. By testing the classic TAE paradigm in both tactile and crossmodal orientation tasks between vision and touch, we were able to show that tactile perception of orientation shows a very robust TAE, similar to its visual counterpart. We further show that orientation adaptation in touch transfers to produce a TAE when tested in vision, but not vice versa. Additionally, when examining the test sequence following adaptation for serial effects, we observed another asymmetry between the two conditions where the visual test sequence displayed a repulsive intramodal serial dependence effect while the tactile test sequence exhibited an attractive serial dependence. These findings provide concrete evidence that vision and touch engage a similar orientation processing mechanism. However, the asymmetry in the crossmodal transfer of TAE and serial dependence points to a non-reciprocal connection between the two modalities, providing further insights into the underlying processing mechanism.

Serial dependence requires visual awareness: Evidence from continuous flash suppression.

The visual system often undergoes a relatively stable perception even in a noisy visual environment. This crucial function was reflected in a visual perception phenomenon-serial dependence, in which recent stimulus history systematically biases current visual decisions. Although serial dependence effects have been revealed in numerous studies, few studies examined whether serial dependence would require visual awareness. By using the continuous flash suppression (CFS) technique to render grating stimuli invisible, we investigated whether serial dependence effects could emerge at the unconscious levels. In an orientation adjustment task, subjects viewed a randomly oriented grating and reported their orientation perception via an adjustment response. Subjects performed a series of three type trial pairs. The first two trial pairs, in which subjects were instructed to make a response or no response toward the first trial of the pairs, respectively, were used to measure serial dependence at the conscious levels; the third trial pair, in which the grating stimulus in the first trial of the pair was masked by a CFS stimulus, was used to measure the serial dependence at the unconscious levels. One-back serial dependence effects for the second trial of the pairs were evaluated. We found significant serial dependence effects at the conscious levels, whether absence (Experiment 1) or presence (Experiment 2) of CFS stimuli, but failed to find the effects at the unconscious levels, corroborating the view that serial dependence requires visual awareness.

Discriminating orientation information with phase consistency in alpha and low-gamma frequency bands: an EEG study.

Recent studies suggest that noninvasive imaging methods (EEG, MEG) in the human brain scalp can decode the content of visual features information (orientation, color, motion, etc.) in Visual-Working Memory (VWM). Previous work demonstrated that with the sustained low-frequency Event-Related Potential (ERP under 6 Hz) of scalp EEG distributions, it is possible to accurately decode the content of orientation information in VWM during the delay interval. In addition, previous studies showed that the raw data captured by a combination of the occi-parietal electrodes could be used to decode the orientation. However, it is unclear whether the orientation information is available in other frequency bands (higher than 6 Hz) or whether this information is feasible with fewer electrodes. Furthermore, the exploration of orientation information in the phase values of the signal has not been well-addressed. In this study, we propose that orientation information is also accessible through the phase consistency of the occipital region in the alpha band frequency. Our results reveal a significant difference between orientations within 200 ms after stimulus offset in early visual sensory processing, with no apparent effect in power and Event-Related Oscillation (ERO) during this period. Additionally, in later periods (420-500 ms after stimulus offset), a noticeable difference is observed in the phase consistency of low gamma-band activity in the occipital area. Importantly, our findings suggest that phase consistency between trials of the orientation feature in the occipital alpha and low gamma-band can serve as a measure to obtain orientation information in VWM. Furthermore, the study demonstrates that phase consistency in the alpha and low gamma band can reflect the distribution of orientation-selective neuron numbers in the four main orientations in the occipital area.

Albatrosses employ orientation and routing strategies similar to yacht racers.

The way goal-oriented birds adjust their travel direction and route in response to wind significantly affects their travel costs. This is expected to be particularly pronounced in pelagic seabirds, which utilize a wind-dependent flight style called dynamic soaring. Dynamic soaring seabirds in situations without a definite goal, e.g. searching for prey, are known to preferentially fly with crosswinds or quartering-tailwinds to increase the speed and search area, and reduce travel costs. However, little is known about their reaction to wind when heading to a definite goal, such as homing. Homing tracks of wandering albatrosses (Diomedea exulans) vary from beelines to zigzags, which are similar to those of sailboats. Here, given that both albatrosses and sailboats travel slower in headwinds and tailwinds, we tested whether the time-minimizing strategies used by yacht racers can be compared to the locomotion patterns of wandering albatrosses. We predicted that when the goal is located upwind or downwind, albatrosses should deviate their travel directions from the goal on the mesoscale and increase the number of turns on the macroscale. Both hypotheses were supported by track data from albatrosses and racing yachts in the Southern Ocean confirming that albatrosses qualitatively employ the same strategy as yacht racers. Nevertheless, albatrosses did not strictly minimize their travel time, likely making their flight robust against wind fluctuations to reduce flight costs. Our study provides empirical evidence of tacking in albatrosses and demonstrates that man-made movement strategies provide a new perspective on the laws underlying wildlife movement.

Visual boundary cues suffice to anchor place and grid cells in virtual reality.

The hippocampal formation contains neurons responsive to an animal's current location and orientation, which together provide the organism with a neural map of space.1,2,3 Spatially tuned neurons rely on external landmark cues and internally generated movement information to estimate position.4,5 An important class of landmark cue are the boundaries delimiting an environment, which can define place cell field position6,7 and stabilize grid cell firing.8 However, the precise nature of the sensory information used to detect boundaries remains unknown. We used 2-dimensional virtual reality (VR)9 to show that visual cues from elevated walls surrounding the environment are both sufficient and necessary to stabilize place and grid cell responses in VR, when only visual and self-motion cues are available. By contrast, flat boundaries formed by the edges of a textured floor did not stabilize place and grid cells, indicating only specific forms of visual boundary stabilize hippocampal spatial firing. Unstable grid cells retain internally coherent, hexagonally arranged firing fields, but these fields "drift" with respect to the virtual environment over periods >5 s. Optic flow from a virtual floor does not slow drift dynamics, emphasizing the importance of boundary-related visual information. Surprisingly, place fields are more stable close to boundaries even with floor and wall cues removed, suggesting invisible boundaries are inferred using the motion of a discrete, separate cue (a beacon signaling reward location). Subsets of place cells show allocentric directional tuning toward the beacon, with strength of tuning correlating with place field stability when boundaries are removed.

Feature variability determines specificity and transfer in multiorientation feature detection learning.

Historically, in many perceptual learning experiments, only a single stimulus is practiced, and learning is often specific to the trained feature. Our prior work has demonstrated that multi-stimulus learning (e.g., training-plus-exposure procedure) has the potential to achieve generalization. Here, we investigated two important characteristics of multi-stimulus learning, namely, roving and feature variability, and their impacts on multi-stimulus learning and generalization. We adopted a feature detection task in which an oddly oriented target bar differed by 16° from the background bars. The stimulus onset asynchrony threshold between the target and the mask was measured with a staircase procedure. Observers were trained with four target orientation search stimuli, either with a 5° deviation (30°-35°-40°-45°) or with a 45° deviation (30°-75°-120°-165°), and the four reference stimuli were presented in a roving manner. The transfer of learning to the swapped target-background orientations was evaluated after training. We found that multi-stimulus training with a 5° deviation resulted in significant learning improvement, but learning failed to transfer to the swapped target-background orientations. In contrast, training with a 45° deviation slowed learning but produced a significant generalization to swapped orientations. Furthermore, a modified training-plus-exposure procedure, in which observers were trained with four orientation search stimuli with a 5° deviation and simultaneously passively exposed to orientations with high feature variability (45° deviation), led to significant orientation learning generalization. Learning transfer also occurred when the four orientation search stimuli with a 5° deviation were presented in separate blocks. These results help us to specify the condition under which multistimuli learning produces generalization, which holds potential for real-world applications of perceptual learning, such as vision rehabilitation and expert training.

When experience with scenes foils attentional orienting: ERP evidence against flexible target-context mapping in visual search.

Visual search is speeded when a target is repeatedly presented in an invariant scene context of nontargets (contextual cueing), demonstrating observers' capability for using statistical long-term memory (LTM) to make predictions about upcoming sensory events, thus improving attentional orienting. In the current study, we investigated whether expectations arising from individual, learned environmental structures can encompass multiple target locations. We recorded event-related potentials (ERPs) while participants performed a contextual cueing search task with repeated and non-repeated spatial item configurations. Notably, a given search display could be associated with either a single target location (standard contextual cueing) or two possible target locations. Our result showed that LTM-guided attention was always limited to only one target position in single- but also in the dual-target displays, as evidenced by expedited reaction times (RTs) and enhanced N1pc and N2pc deflections contralateral to one ("dominant") target of up to two repeating target locations. This contrasts with the processing of non-learned ("minor") target positions (in dual-target displays), which revealed slowed RTs alongside an initial N1pc "misguidance" signal that then vanished in the subsequent N2pc. This RT slowing was accompanied by enhanced N200 and N400 waveforms over fronto-central electrodes, suggesting that control mechanisms regulate the competition between dominant and minor targets. Our study thus reveals a dissociation in processing dominant versus minor targets: While LTM templates guide attention to dominant targets, minor targets necessitate control processes to overcome the automatic bias towards previously learned, dominant target locations.

Orienting role of the putative human posterior infero-temporal area in visual attention.

The dorsal attention network (DAN) is a network of brain regions essential for attentional orienting, which includes the lateral intraparietal area (LIP) and frontal eye field (FEF). Recently, the putative human dorsal posterior infero-temporal area (phPITd) has been identified as a new node of the DAN. However, its functional relationship with other areas of the DAN and its specific role in visual attention remained unclear. In this study, we analyzed a large publicly available neuroimaging dataset to investigate the intrinsic functional connectivities (FCs) of the phPITd with other brain areas. The results showed that the intrinsic FCs of the phPITd with the areas of the visual network and the DAN were significantly stronger than those with the ventral attention network (VAN) areas and areas of other networks. We further conducted individual difference analyses with a sample size of 295 participants and a series of attentional tasks to investigate which attentional components each phPITd-based DAN edge predicts. Our findings revealed that the intrinsic FC of the left phPITd with the LIPv could predict individual ability in attentional orienting, but not in alerting, executive control, and distractor suppression. Our results not only provide direct evidence of the phPITd's functional relationship with the LIPv, but also offer a comprehensive understanding of its specific role in visual attention.

Visuospatial cueing differences as a function of autistic traits.

Atypical orienting of visuospatial attention in autistic individuals or individuals with a high level of autistic-like traits (ALTs) has been well documented and viewed as a core feature underlying the development of autism. However, there has been limited testing of three alternative theoretical positions advanced to explain atypical orienting - difficulty in disengagement, cue indifference, and delay in orienting. Moreover, research commonly has not separated facilitation (reaction time difference between neutral and valid cues) and cost effects (reaction time difference between invalid and neutral cues) in orienting tasks. We addressed these limitations in two experiments that compared groups selected for Low- and High-ALT levels on exogenous and endogenous versions of the Posner cueing paradigm. Experiment 1 showed that High-ALT participants exhibited a significantly reduced cost effect compared to Low-ALT participants in the endogenous cueing task, although the overall orienting effect remained small. In Experiment 2, we increased task difficulty of the endogenous task to augment cueing effects. Results were comparable to Experiment 1 regarding the finding of a reduced cost effect for High-ALT participants on the endogenous cueing task and additionally demonstrated a reduced facilitation effect in High-ALT participants on the same task. No ALT group differences were observed on an exogenous cueing task included in Experiment 2. These findings suggest atypical orienting in High-ALT individuals may be attributable to general cue indifference, which implicates differences in top-down attentional processes between Low- and High-ALT individuals. We discuss how indifference to endogenous cues may contribute to social cognitive differences in autism.

Top-down suppression of negative features applies flexibly contingent on visual search goals.

Visually searching for a frequently changing target is assumed to be guided by flexible working memory representations of specific features necessary to discriminate targets from distractors. Here, we tested if these representations allow selective suppression or always facilitate perception based on search goals. Participants searched for a target (i.e., a horizontal bar) defined by one of two different negative features (e.g., not red vs. not blue; Experiment 1) or a positive (e.g., blue) versus a negative feature (Experiments 2 and 3). A prompt informed participants about the target identity, and search tasks alternated or repeated randomly. We used different peripheral singleton cues presented at the same (valid condition) or a different (invalid condition) position as the target to examine if negative features were suppressed depending on current instructions. In all experiments, cues with negative features elicited slower search times in valid than invalid trials, indicating suppression. Additionally, suppression of negative color cues tended to be selective when participants searched for the target by different negative features but generalized to negative and non-matching cue colors when switching between positive and negative search criteria was required. Nevertheless, when the same color - red - was used in positive and negative search tasks, red cues captured attention or were suppressed depending on whether red was positive or negative (Experiment 3). Our results suggest that working memory representations flexibly trigger suppression or attentional capture contingent on a task-relevant feature's functional meaning during visual search, but top-down suppression operates at different levels of specificity depending on current task demands.