Changes in primary visual and auditory cortex of blind and sighted adults following 10 weeks of click-based echolocation training.

Recent work suggests that the adult human brain is very adaptable when it comes to sensory processing. In this context, it has also been suggested that structural "blueprints" may fundamentally constrain neuroplastic change, e.g. in response to sensory deprivation. Here, we trained 12 blind participants and 14 sighted participants in echolocation over a 10-week period, and used MRI in a pre-post design to measure functional and structural brain changes. We found that blind participants and sighted participants together showed a training-induced increase in activation in left and right V1 in response to echoes, a finding difficult to reconcile with the view that sensory cortex is strictly organized by modality. Further, blind participants and sighted participants showed a training induced increase in activation in right A1 in response to sounds per se (i.e. not echo-specific), and this was accompanied by an increase in gray matter density in right A1 in blind participants and in adjacent acoustic areas in sighted participants. The similarity in functional results between sighted participants and blind participants is consistent with the idea that reorganization may be governed by similar principles in the two groups, yet our structural analyses also showed differences between the groups suggesting that a more nuanced view may be required.

The Occipital Place Area Is Recruited for Echo-Acoustically Guided Navigation in Blind Human Echolocators.

In the investigation of the brain areas involved in human spatial navigation, the traditional focus has been on visually guided navigation in sighted people. Consequently, it is unclear whether the involved areas also support navigational abilities in other modalities. We explored this possibility by testing whether the occipital place area (OPA), a region associated with visual boundary-based navigation in sighted people, has a similar role in echo-acoustically guided navigation in blind human echolocators. We used fMRI to measure brain activity in 6 blind echolocation experts (EEs; five males, one female), 12 blind controls (BCs; six males, six females), and 14 sighted controls (SCs; eight males, six females) as they listened to prerecorded echolocation sounds that conveyed either a route taken through one of three maze environments, a scrambled (i.e., spatiotemporally incoherent) control sound, or a no-echo control sound. We found significantly greater activity in the OPA of EEs, but not the control groups, when they listened to the coherent route sounds relative to the scrambled sounds. This provides evidence that the OPA of the human navigation brain network is not strictly tied to the visual modality but can be recruited for nonvisual navigation. We also found that EEs, but not BCs or SCs, recruited early visual cortex for processing of echo acoustic information. This is consistent with the recent notion that the human brain is organized flexibly by task rather than by specific modalities.SIGNIFICANCE STATEMENT There has been much research on the brain areas involved in visually guided navigation, but we do not know whether the same or different brain regions are involved when blind people use a sense other than vision to navigate. In this study, we show that one part of the brain (occipital place area) known to play a specific role in visually guided navigation is also active in blind human echolocators when they use reflected sound to navigate their environment. This finding opens up new ways of understanding how people navigate, and informs our ability to provide rehabilitative support to people with vision loss.

No effect of 10-week training in click-based echolocation on auditory localization in people who are blind.

What factors are important in the calibration of mental representations of auditory space? A substantial body of research investigating the audiospatial abilities of people who are blind has shown that visual experience might be an important factor for accurate performance in some audiospatial tasks. Yet, it has also been shown that long-term experience using click-based echolocation might play a similar role, with blind expert echolocators demonstrating auditory localization abilities that are superior to those of people who are blind and who do not use click-based echolocation by Vercillo et al. (Neuropsychologia 67: 35-40, 2015). Based on this hypothesis we might predict that training in click-based echolocation may lead to improvement in performance in auditory localization tasks in people who are blind. Here we investigated this hypothesis in a sample of 12 adult people who have been blind from birth. We did not find evidence for an improvement in performance in auditory localization after 10 weeks of training despite significant improvement in echolocation ability. It is possible that longer-term experience with click-based echolocation is required for effects to develop, or that other factors can explain the association between echolocation expertise and superior auditory localization. Considering the practical relevance of click-based echolocation for people who are visually impaired, future research should address these questions.

Human click-based echolocation: Effects of blindness and age, and real-life implications in a 10-week training program.

Understanding the factors that determine if a person can successfully learn a novel sensory skill is essential for understanding how the brain adapts to change, and for providing rehabilitative support for people with sensory loss. We report a training study investigating the effects of blindness and age on the learning of a complex auditory skill: click-based echolocation. Blind and sighted participants of various ages (21-79 yrs; median blind: 45 yrs; median sighted: 26 yrs) trained in 20 sessions over the course of 10 weeks in various practical and virtual navigation tasks. Blind participants also took part in a 3-month follow up survey assessing the effects of the training on their daily life. We found that both sighted and blind people improved considerably on all measures, and in some cases performed comparatively to expert echolocators at the end of training. Somewhat surprisingly, sighted people performed better than those who were blind in some cases, although our analyses suggest that this might be better explained by the younger age (or superior binaural hearing) of the sighted group. Importantly, however, neither age nor blindness was a limiting factor in participants' rate of learning (i.e. their difference in performance from the first to the final session) or in their ability to apply their echolocation skills to novel, untrained tasks. Furthermore, in the follow up survey, all participants who were blind reported improved mobility, and 83% reported better independence and wellbeing. Overall, our results suggest that the ability to learn click-based echolocation is not strongly limited by age or level of vision. This has positive implications for the rehabilitation of people with vision loss or in the early stages of progressive vision loss.

Perceptual constancy with a novel sensory skill.

Making sense of the world requires perceptual constancy-the stable perception of an object across changes in one's sensation of it. To investigate whether constancy is intrinsic to perception, we tested whether humans can learn a form of constancy that is unique to a novel sensory skill (here, the perception of objects through click-based echolocation). Participants judged whether two echoes were different either because: (a) the clicks were different, or (b) the objects were different. For differences carried through spectral changes (but not level changes), blind expert echolocators spontaneously showed a high constancy ability (mean d' = 1.91) compared to sighted and blind people new to echolocation (mean d' = 0.69). Crucially, sighted controls improved rapidly in this ability through training, suggesting that constancy emerges in a domain with which the perceiver has no prior experience. This provides strong evidence that constancy is intrinsic to human perception. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Stimulus uncertainty affects perception in human echolocation: Timing, level, and spectrum.

The human brain may use recent sensory experience to create sensory templates that are then compared to incoming sensory input, that is, "knowing what to listen for." This can lead to greater perceptual sensitivity, as long as the relevant properties of the target stimulus can be reliably estimated from past sensory experiences. Echolocation is an auditory skill probably best understood in bats, but humans can also echolocate. Here we investigated for the first time whether echolocation in humans involves the use of sensory templates derived from recent sensory experiences. Our results showed that when there was certainty in the acoustic properties of the echo relative to the emission, either in temporal onset, spectral content or level, people detected the echo more accurately than when there was uncertainty. In addition, we found that people were more accurate when the emission's spectral content was certain but, surprisingly, not when either its level or temporal onset was certain. Importantly, the lack of an effect of temporal onset of the emission is counter to that found previously for tasks using nonecholocation sounds, suggesting that the underlying mechanisms might be different for echolocation and nonecholocation sounds. Importantly, the effects of stimulus certainty were no different for people with and without experience in echolocation, suggesting that stimulus-specific sensory templates can be used in a skill that people have never used before. From an applied perspective our results suggest that echolocation instruction should encourage users to make clicks that are similar to one another in their spectral content. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Retinotopic-like maps of spatial sound in primary 'visual' cortex of blind human echolocators.

The functional specializations of cortical sensory areas were traditionally viewed as being tied to specific modalities. A radically different emerging view is that the brain is organized by task rather than sensory modality, but it has not yet been shown that this applies to primary sensory cortices. Here, we report such evidence by showing that primary 'visual' cortex can be adapted to map spatial locations of sound in blind humans who regularly perceive space through sound echoes. Specifically, we objectively quantify the similarity between measured stimulus maps for sound eccentricity and predicted stimulus maps for visual eccentricity in primary 'visual' cortex (using a probabilistic atlas based on cortical anatomy) to find that stimulus maps for sound in expert echolocators are directly comparable to those for vision in sighted people. Furthermore, the degree of this similarity is positively related with echolocation ability. We also rule out explanations based on top-down modulation of brain activity-e.g. through imagery. This result is clear evidence that task-specific organization can extend even to primary sensory cortices, and in this way is pivotal in our reinterpretation of the functional organization of the human brain.

Incidental context information increases recollection.

The current study describes a receiver-operating characteristic (ROC) task for human participants based on the spontaneous recognition memory paradigms typically used with rodents. Recollection was significantly higher when an object was in the same location and background as at encoding, a combination used to assess episodic-like memory in animals, but not when only one of these task-irrelevant cues was present. The results show that incidentally encoded cue information can determine the degree of recollection, and opens up the possibility of assessing recollection across species in a single experimental paradigm, allowing better understanding of the cognitive and biological mechanisms at play.

Direct encoding of orientation variance in the visual system.

Our perception of regional irregularity, an example of which is orientation variance, seems effortless when we view two patches of texture that differ in this attribute. Little is understood, however, of how the visual system encodes a regional statistic like orientation variance, but there is some evidence to suggest that it is directly encoded by populations of neurons tuned broadly to high or low levels. The present study shows that selective adaptation to low or high levels of variance results in a perceptual aftereffect that shifts the perceived level of variance of a subsequently viewed texture in the direction away from that of the adapting stimulus (Experiments 1 and 2). Importantly, the effect is durable across changes in mean orientation, suggesting that the encoding of orientation variance is independent of global first moment orientation statistics (i.e., mean orientation). In Experiment 3 it was shown that the variance-specific aftereffect did not show signs of being encoded in a spatiotopic reference frame, similar to the equivalent aftereffect of adaptation to the first moment orientation statistic (the tilt aftereffect), which is represented in the primary visual cortex and exists only in retinotopic coordinates. Experiment 4 shows that a neuropsychological patient with damage to ventral areas of the cortex but spared intact early areas retains sensitivity to orientation variance. Together these results suggest that orientation variance is encoded directly by the visual system and possibly at an early cortical stage.

Exogenous attention to unseen objects?

Attention and awareness are closely related phenomena, but recent evidence has shown that not all attended stimuli give rise to awareness. Controversy still remains over whether, and the extent to which, a dissociation between attention and awareness encompasses all forms of attention. For example, it has been suggested that attention without awareness is more readily demonstrated for voluntary, endogenous attention than its reflexive, exogenous counterpart. Here we examine whether exogenous attentional cueing can have selective behavioural effects on stimuli that nevertheless remain unseen. Using a task in which object-based attention has been shown in the absence of awareness, we remove all possible contingencies between cues and target stimuli to ensure that any cueing effects must be under purely exogenous control, and find evidence of exogenous object-based attention without awareness. In a second experiment we address whether this dissociation crucially depends on the method used to establish that the objects indeed remain unseen. Specifically, to confirm that objects are unseen we adopt appropriate signal detection task procedures, including those that retain parity with the primary attentional task (by requiring participants to discriminate the two types of trial that are used to measure an effect of attention). We show a significant object-based attention effect is apparent under conditions where the selected object indeed remains undetectable.

Color constancy for an unseen surface.

The illumination of a scene strongly affects our perception of objects in that scene, e.g., the pages of a book illuminated by candlelight will appear quite yellow relative to other types of artificial illuminants. Yet at the same time, the reader still judges the pages as white, their surface color unaffected by the interplay of paper and illuminant. It has been shown empirically that we can indeed report two quite different interpretations of "color": one is dependent on the constant surface spectral reflectance of an object (surface color) and the other on the power of light of different wavelengths reflected from that object (reflected color). How then are these two representations related? The common view, dating from Aristotle, is that our experience of surface color is derived from reflected color or, in more familiar terms, that color perception follows from color sensation. By definition, color constancy requires that vision "discounts the illuminant"; thus, it seems reasonable that vision begins with the color of objects as they naively appear and that we infer from their appearances their surface color. Here, we question this classic view. We use metacontrast-masked priming and, by presenting the unseen prime and the visible mask under different illuminants, dissociate two ways in which the prime matched the mask: in surface color or in reflected color. We find that priming of the mask occurs when it matches the prime in surface color, not reflected color. It follows that color perception can arise without prior color sensation.

Spatial attention does not modulate holistic face processing, even when multiple faces are present.

The perception of faces is often considered to be unique in comparison with that of other objects in the world. The fact that faces are processed not by their constituent components but by the spatial configuration between those components (holistic face processing--HFP) is often used to support this. Despite two decades of research, however, there is no consensus as to whether or not HFP is a process that is subject to attentional modulation. Here, in two experiments, we used a method to direct spatial attention not previously used in studies of HFP--an exogenous spatial cue--as it offers a robust, rapid, and involuntary method of directing attention. In one experiment we demonstrate that the degree of HFP afforded to a face is not reduced when attention is directed away from that face. In a second experiment we replicate this finding even when the face is simultaneously flanked by other faces--a condition under which a face-specific processing module would, hypothetically, be more sensitive to attentional guidance. These results add to the argument that HFP is carried out independently of attention.

Object-based attention without awareness.

Attention and awareness are often considered to be related. Some forms of attention can, however, facilitate the processing of stimuli that remain unseen. It is unclear whether this dissociation extends beyond selection on the basis of primitive properties, such as spatial location, to situations in which there are more complex bases for attentional selection. The experiment described here shows that attentional selection at the level of objects can take place without giving rise to awareness of those objects. Pairs of objects were continually masked, which rendered them invisible to participants performing a cued-target-discrimination task. When the cue and target appeared within the same object, discrimination was faster than when they appeared in different objects at the same spatial separation. Participants reported no awareness of the objects and were unable to detect them in a signal-detection task. Object-based attention, therefore, is not sufficient for object awareness.