Michael J. Proulx

The role of visual experience for the neural basis of spatial cognition

Blindness often results in the adaptive neural reorganization of the remaining modalities, producing sharper auditory and haptic behavioral performance. Yet, non-visual modalities might not be able to fully compensate for the lack of visual experience as in the case of congenital blindness. For example, developmental visual experience seems to be necessary for the maturation of multisensory neurons for spatial tasks. Additionally, the ability of vision to convey information in parallel might be taken into account as the main attribute that cannot be fully compensated by the spared modalities. Therefore, the lack of visual experience might impair all spatial tasks that require the integration of inputs from different modalities, such as having to represent a set of objects on the basis of the spatial relationships among the objects, rather than the spatial relationship that each object has with oneself. Here we integrate behavioral and neural evidence to conclude that visual experience is necessary for the neural development of normal spatial cognition.

Seeing ‘Where’ through the Ears: Effects of Learning-by-Doing and Long-Term Sensory Deprivation on Localization Based on Image-to-Sound Substitution

Background Sensory substitution devices for the blind translate inaccessible visual information into a format that intact sensory pathways can process. We here tested image-to-sound conversion-based localization of visual stimuli (LEDs and objects) in 13 blindfolded participants. Methods and Findings Subjects were assigned to different roles as a function of two variables: visual deprivation (blindfolded continuously (Bc) for 24 hours per day for 21 days; blindfolded for the tests only (Bt)) and system use (system not used (Sn); system used for tests only (St); system used continuously for 21 days (Sc)). The effect of learning-by-doing was assessed by comparing the performance of eight subjects (BtSt) who only used the mobile substitution device for the tests, to that of three subjects who, in addition, practiced with it for four hours daily in their normal life (BtSc and BcSc); two subjects who did not use the device at all (BtSn and BcSn) allowed assessment of its use in the tasks we employed. The impact of long-term sensory deprivation was investigated by blindfolding three of those participants throughout the three week-long experiment (BcSn, BcSn/c, and BcSc); the other ten subjects were only blindfolded during the tests (BtSn, BtSc, and the eight BtSt subjects). Expectedly, the two subjects who never used the substitution device, while fast in finding the targets, had chance accuracy, whereas subjects who used the device were markedly slower, but showed much better accuracy which improved significantly across our four testing sessions. The three subjects who freely used the device daily as well as during tests were faster and more accurate than those who used it during tests only; however, long-term blindfolding did not notably influence performance. Conclusions Together, the results demonstrate that the device allowed blindfolded subjects to increasingly know where something was by listening, and indicate that practice in naturalistic conditions effectively improved “visual” localization performance.

Target-nontarget similarity modulates stimulus-driven control in visual search

The literature contains conflicting results concerning whether an irrelevant featural singleton (an item unique with respect to a feature such as color or brightness) can control attention in a stimulus-driven manner. The present study explores whether target-nontarget similarity influences stimulus-driven shifts of attention to a distractor. An experiment evaluated whether manipulating target-nontarget similarity by varying orientation would modulate distraction by an irrelevant feature (a bright singleton). We found that increasing target-nontarget similarity resulted in a decreased impact of a uniquely bright object on visual search. This method of manipulating the target-nontarget similarity independent of the salience of a distracting feature suggests that the extent to which visual attention is stimulus-driven depends on the target-nontarget similarity.

Size Matters: Large Objects Capture Attention in Visual Search

Can objects or events ever capture ones attention in a purely stimulus-driven manner? A recent review of the literature set out the criteria required to find stimulus-driven attentional capture independent of goal-directed influences, and concluded that no published study has satisfied that criteria. Here visual search experiments assessed whether an irrelevantly large object can capture attention. Capture of attention by this static visual feature was found. The results suggest that a large object can indeed capture attention in a stimulus-driven manner and independent of displaywide features of the task that might encourage a goal-directed bias for large items. It is concluded that these results are either consistent with the stimulus-driven criteria published previously or alternatively consistent with a flexible, goal-directed mechanism of saliency detection.

Congenital blindness improves semantic and episodic memory.

Previous studies reported that congenitally blind people possess superior verb-generation skills. Here we tested the impact of blindness on capacity and the fidelity of semantic memory by using a false memory paradigm. In the Deese-Roediger-McDermott paradigm, participants study lists of words that are all semantically related to a lure that is not presented. Subsequently, participants frequently recall the missing lure. We found that congenitally blind participants have enhanced memory performance for recalling the presented words and reduced false memories for the lure. The dissociation of memory capacity and fidelity provides further evidence for enhanced verbal ability in the blind, supported by their broader structural and functional brain reorganisation.

Bottom-Up Guidance in Visual Search for Conjunctions.

Understanding the relative role of top-down and bottom-up guidance is crucial for models of visual search. Previous studies have addressed the role of top-down and bottom-up processes in search for a conjunction of features but with inconsistent results. Here, the author used an attentional capture method to address the role of top-down and bottom-up processes in conjunction search. The role of bottom-up processing was assayed by inclusion of an irrelevant-size singleton in a search for a conjunction of color and orientation. One object was uniquely larger on each trial, with chance probability of coinciding with the target; thus, the irrelevant feature of size was not predictive of the targets location. Participants searched more efficiently for the target when it was also the size singleton, and they searched less efficiently for the target when a nontarget was the size singleton. Although a conjunction target cannot be detected on the basis of bottom-up processing alone, participants used search strategies that relied significantly on bottom-up guidance in finding the target, resulting in interference from the irrelevant-size singleton.

Synthetic synaesthesia and sensory substitution

Visual information can be provided to blind users through sensory substitution devices that convert images into sound. Through extensive use to develop expertise, some blind users have reported visual experiences when using such a device. These blind expert users have also reported visual phenomenology to other sounds even when not using the device. The blind users acquired synthetic synaesthesia, with visual experience evoked by sounds only after gaining such expertise. Sensorimotor learning may facilitate and perhaps even be required to develop expertise in the use of multimodal information. Furthermore, other areas where expertise is acquired in dividing attention amongst cross-modal information or integrating such information might also give rise to synthetic synaesthesia.

Can bees simultaneously engage in adaptive foraging behaviour and attend to cryptic predators

Bees foraging for nectar often have to discriminate between flowers with similar appearance but different nectar rewards. At the same time, they must be vigilant for ambush predators, such as crab spiders, which can camouflage themselves on flowers. We investigated whether bees, Bombus terrestris, can efficiently discriminate similar flower colours while exposed to predation threat from cryptic predators. Bees were individually tested in tightly controlled laboratory experiments using artificial flowers whose nectar supply was administered with precision pumps. Predation risk was simulated by automated crab spider ‘robots’ that captured bees for a limited duration without injuring them. Bees’ behaviour was monitored by a 3D video tracking system. We experimented with both cryptic and conspicuous spiders, finding that bees had no difficulty avoiding conspicuous spiders while still foraging adaptively. Conversely, they prioritized predator avoidance at the expense of maximizing energy intake when faced with detecting cryptic predators and a difficult colour discrimination task. This difference in behaviour was not due to cognitive limitations: bees were able to discriminate between similar flower types under predation risk from cryptic spiders when choosing the safe flower type incurred a gustatory punishment in the form of bitter quinine solution. However, this resulted in bees incurring substantially higher costs in terms of floral inspection times. We conclude that bees have the capacity to attend to difficult foraging tasks while simultaneously avoiding cryptic predators, but only do so when avoidance of gustatory punishment justifies the increased costs.

Multisensory integration, sensory substitution and visual rehabilitation.

Sensory substitution has advanced remarkably over the past 35 years since first introduced to the scientific literature by Paul Bach-y-Rita. In this issue dedicated to his memory, we describe a collection of reviews that assess the current state of neuroscience research on sensory substitution, visual rehabilitation, and multisensory processes.

Additional-singleton interference in efficient visual search: A common salience route for detection and compound tasks

In efficient search for feature singleton targets, additional singletons (ASs) defined in a nontarget dimension are frequently found to interfere with performance. All search tasks that are processed via a spatial saliency map of the display would be predicted to be subject to such AS interference. In contrast, dual-route models, such as feature integration theory, assume that singletons are detected not via a saliency map, but via a nonspatial route that is immune to interference from cross-dimensional ASs. Consistent with this, a number of studies have reported absent interference effects in detection tasks. However, recent work suggests that the failure to find such effects may be due to the particular frequencies at which ASs were presented, as well as to their relative saliency. These two factors were examined in the present study. In contrast to previous reports, cross-dimensional ASs were found to slow detection (target-present and target-absent) responses, modulated by both their frequency of occurrence and saliency (relative to the target). These findings challenge dual-route models and support single-route models, such as dimension weighting and guided search.