Unlocking the symmetric transfer of irrelevant information: gene-environment interplay and enhanced interhemispheric cross-talk.

Hemispheric specialization influences stimulus processing and behavioural control, affecting responses to relevant stimuli. However, most sensory input is irrelevant and must be filtered out to prevent interference with task-relevant behaviour, a process known as habituation. Despite habituation's vital role, little is known about hemispheric specialization for this brain function. We conducted an experiment with domestic chicks, an elite animal model to study lateralization. They were exposed to distracting visual stimuli while feeding when using binocular or monocular vision. Switching the viewing eye after habituation, we examined if habituation was confined to the stimulated hemisphere or shared across hemispheres. We found that both hemispheres learned equally to ignore distracting stimuli. However, embryonic light stimulation, influencing hemispheric specialization, revealed an asymmetry in interhemispheric transfer of the irrelevant information discarded via habituation. Unstimulated chicks exhibited a directional bias, with the right hemisphere failing to transfer distracting stimulus information to the left hemisphere, while transfer from left to right was possible. Nevertheless, embryonic light stimulation counteracted this asymmetry, enhancing communication from the right to the left hemisphere and reducing the pre-existing imbalance. This sharing extends beyond hemisphere-specific functions and encompasses a broader representation of irrelevant events.

Habituation (of attentional capture) is not what you think it is.

Habituation represents a well-established form of learning in various neuroscience domains. However, cognitive psychologists working in the field of visual attention have largely overlooked this phenomenon. In this regard, I would like to argue that the reduction in attentional capture observed with repetitive salient distractors, and specifically abrupt visual onsets, could be attributed to habituation. Three classic models of habituation, independently devised by Sokolov, Wagner, and by Thompson, will be presented and discussed in relation to the capture of attention. Of particular interest is the fact that Sokolov's model is governed by a prediction-error minimization principle, where a stimulus attracts attention to the extent that it violates the expected sensory input, which is anticipated on the basis of the previous history of stimulation. Hence, at least in humans, habituation is governed by high-order cognitive processes, and should not be confounded with peripheral sensory adaptation or fatigue. Furthermore, the cognitive nature of habituation is also attested by the fact that visual distractor filtering is context-specific. In conclusion, as already suggested by others, I believe that researchers working in the field of attention should give more consideration to the notion of habituation, especially with regard to the control of stimulus-driven capture. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Habituation to visual onsets is affected by local and global distractors rate.

Recent findings demonstrate that habituation of capture is stronger where onset distractors are frequent and weaker where they are rare, thus showing that habituation to onsets has a spatial selective nature. However, a debated question is whether habituation at a specific location is exclusively determined by the distractors' local rate, or whether instead local habituation is also affected by the global rate of the distractors, which may occur also at other locations. Here, we report the results from a between-participants experiment involving three groups of participants exposed to visual onsets during a visual search task. In two groups, onsets appeared at a single location with a high 60% rate or a low 15% rate, respectively, whereas in a third group, distractors could appear in four distinct locations with the same 15% local rate, leading to a 60% global rate. Our results confirmed that locally, habituation of capture was stronger the higher the distractors rate. However, the key finding was that we found a clear and robust modulation of the global distractors rate on the local habituation level. Taken together, our results unambiguously show that habituation has both a spatially selective and a spatially nonselective nature.

Ignoring visual distractors: Habituation to onsets is driven by time-based expectation.

An increasing bulk of evidence shows that through different mechanisms, experienced-based or voluntary, reactive or proactive, human beings can attenuate the distracting impact of salient visual, albeit irrelevant, stimuli. Current mechanisms assume that this is achieved by suppressing the salient distractor's features or location at the priority map level, or at lower dimension-based maps levels. However, this functional architecture has so far ignored the role of time in distractors filtering, a key question that we have addressed in the present study. We found that during a visual discrimination task, a "standard" onset distractor, always appearing at the same interval from the beginning of the trial, was subject to habituation. Crucially, however, when the onset distractor was unfrequently presented with an unexpected 1-second delay, it reboosted capture at full strength, while the "standard" distractor continued to remain overall habituated. As predicted by Sokolov's (1963, Annual Review of Physiology, 25[1], 545-580) theory, our results show that habituation mechanisms filter the irrelevant distracting sensory input also on the basis of its temporal parameters. We conclude that habituation to onsets is controlled also by time-based expectation mechanisms and suggest that more recently proposed theories of distractors filtering should also incorporate the temporal parameter among the factors that allow an efficient handling of visual distraction.

Habituation to onsets is controlled by spatially selective distractor expectation.

Habituation to onset distractors has been shown to be stronger the higher the distractor probability. However, since in previous studies distractor probability covaried with distractor numerosity, it was unclear whether habituation was controlled by a mechanism that relies on distractor expectation (Sokolov, 1963), or by a mechanism that is merely driven by the number of stimulations delivered to the nervous system (Groves & Thompson, 1970). To address this issue, we manipulated the probability of distractor occurrence at a fixed location, without varying the number of distractors being presented. The results of Experiment 1 clearly favored the Sokolov model of habituation, showing that habituation of capture is controlled by the level of distractor expectation for the same distractors number. Experiment 2 excluded that the pattern of habituation was determined by the difference in the temporal frequency of the distractor between higher and lower distractor rates. Furthermore, the results of Experiment 3 suggested that the amount of habituation of capture is mainly controlled by the local rather than by the global rate of the onset distractor occurrence, thus indicating that habituation of capture is largely spatially specific. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Habituation to abrupt-onset distractors with different spatial occurrence probability.

Previous studies have shown that abrupt onsets randomly appearing at different locations can be ignored with practice, a result that was interpreted as an instance of habituation. Here we addressed whether habituation of capture can be spatially selective and determined by the rate of onset occurrence at different locations, and whether habituation is achieved via spatial suppression applied at the distractor location. In agreement with the habituation hypothesis, we found that capture attenuation was larger where the onset distractor occurred more frequently, similarly to what has been documented for feature-singleton distractors (the "distractor-location effect"), and that onset interference decreased across trials at both the high- and low-probability distractor locations. By contrast, evidence was inconclusive as to whether distractor filtering was also accompanied by a larger impairment in target processing when it appeared at the more likely distractor location (the "target-location effect"), as instead previously reported for feature-singleton distractors. Finally, here we discuss how and to what extent distractor rejection based on statistical learning and habituation of capture are different, and conclude that the two notions are intimately related, as the Sokolov model of habituation operates by comparing the upcoming sensory input with expectation based on the statistics of previous stimulation.

Testing reward-cue attentional salience: Attainment and dynamic changes.

A great wealth of studies has investigated the capacity of motivationally relevant stimuli to bias attention, suggesting that reward predicting cues are prioritized even when reward is no longer delivered and when attending to such stimuli is detrimental to reward achievement. Despite multiple procedures have been adopted to unveil the mechanisms whereby reward cues gain attentional salience, some open questions remain. Indeed, mechanisms different from motivation can be responsible for the capture of attention triggered by the reward cue. In addition, we note that at present only a few studies have sought to address whether the cue attractiveness dynamically follows changes in the associated reward value. Investigating how and to what extent the salience of the reward cue is updated when motivation changes, could help shedding light on how reward-cues attain and maintain their capacity to attract attention, and therefore on apparent irrational attentive behaviors.

Impaired selection of a previously ignored singleton: Evidence for salience map plastic changes.

Spatial suppression of a salient colour distractor is achievable via statistical learning. Distractor suppression attenuates unwanted capture, but at the same time target selection at the most likely distractor location is impaired. This result corroborates the idea that the distractor salience is attenuated via inhibitory signals applied to the corresponding location in the priority map. What is less clear, however, is whether lingering impairment in target selection when the distractor is removed are due to the proactive strategic maintenance of the suppressive signal at the previous most likely distractor location or result from the fact that suppression has induced plastic changes in the priority map, probably changing input weights. Here, we provide evidence that supports the latter possibility, as we found that impairment in target selection persisted even when the singleton distractor in the training phase became the target of search in a subsequent test phase. This manipulation rules out the possibility that the observed impairments at the previous most likely distractor location were caused by a signal suppression maintained at this location. Rather, the results reveal that the inhibitory signals cause long-lasting changes in the priority map, which affect future computation of the target salience at the same location, and therefore the efficiency of attentional selection.

Context-Specific Habituation: A Review.

Habituation consists of the progressive response decrement to a repeated stimulation, a response decline that is not accounted for by sensory or motor fatigue. Together with sensitization, habituation has been traditionally considered to be a prototypical example of non-associative learning, being affected only by the features of the stimulation, as for instance its intensity or frequency. However, despite this widespread belief, evidence exists showing that habituation can be specific to the context of the stimulation, thus suggesting that habituation can have an associative nature. Such an unexpected characteristic of habituation was in fact predicted by a theoretical model of associative learning proposed by Wagner in a series of works that appeared in the late 1970s. Here, we critically review the experimental data that since then have been accumulated in support of this hypothesis. What emerges from the literature is that context-specific habituation is common to several animal species and that the ability to form an association between the habituating stimulus and its context is independent of the complexity of the animal's nervous system. Finally, context-specific habituation is observed for a variety of organism's responses, ranging from visceral to motor and mental activities.

Distractor filtering is affected by local and global distractor probability, emerges very rapidly but is resistant to extinction.

Effects of statistical learning (SL) of distractor location have been shown to persist when the probabilities of distractor occurrence are equalized across different locations in a so-called extinction phase. Here, we asked whether lingering effects of SL are still observed when a true extinction phase, during which the distractor is completely omitted, is implemented. The results showed that, once established, the effects of SL of distractor location do survive the true extinction phase, indicating that the pattern of suppression in the saliency map is encoded in a form of long-lasting memory. Quite unexpectedly, we also found that the amount of filtering implemented at a given location is not only dictated by the specific rate of distractor occurrence at that location, as previously found, but also by the global distractor probability. We therefore suggest that the visual attention system could be more or less (implicitly) prone to suppression as a function of how often the distractor is encountered overall, and that this suppressive bias affects the degree of suppression at the specific distractor-probability location. Finally, our results showed that the effects of SL of distractor location can appear much more rapidly than has been previously documented, requiring a few trials to become manifest. Hence, SL of distractor location appears to have an asymmetrical rate of learning during acquisition and extinction, while the amount of suppression exerted at a specific distractor location is modulated by distractor contextual probabilistic information.

On the resilience of reward cues attentional salience to reward devaluation, time, incentive learning, and contingency remapping.

Previous evidence has shown that after conditioning reward cues may continue to grab attention even when the paired reward is devalued, thus triggering an irrational attentional capture. Here, we investigated whether such persistent cue attentional salience, once established, can be abolished. In Experiment 1, we first confirmed that the cue attentional salience outlasted reward devaluation, and then we found that such persistent capture did not change after an incentive-learning procedure with a devalued reward. In Experiment 2, we showed that the reward cue salience remained unaltered after reward devaluation for at least 1 week. In Experiment 3, we finally succeeded in modifying the cue attentional salience when a new contingency between the cue and the reward was learned, and the reward was not devalued, such that the organism was in a high motivational state. The pattern of results emerging from our study reveals a complex interaction between attention, learning, and motivation, and may help shedding light on the learning mechanisms underlying addiction. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Microsaccades inhibition triggered by a repetitive visual distractor is not subject to habituation: Implications for the programming of reflexive saccades.

The oculomotor capture triggered by a peripheral onset is subject to habituation, a basic form of learning consisting in a response decrement toward a repeatedly presented stimulus. However, it is unclear whether habituation of reflexive saccades takes place at the saccadic programming or execution stage (or both). To address this issue, we exploited the fact that during fixation the programming of a reflexive saccade exerts a robust but short-lasting phasic inhibition in the absolute microsaccadic frequency. Hence, if habituation of reflexive saccades occurs at the programming stage, then this should also affect the microsaccadic frequency, with a progressive reduction of the inhibitory phase. Conversely, if habituation occurs only at the later stage of saccade execution, the no change in the microsaccadic pattern is expected. Participants were repeatedly exposed to a peripheral onset distractor, and when eye movements were allowed, we replicated the oculomotor capture habituation. Crucially, however, when fixation was maintained the microsaccadic response did not change as exposure to the onset progressed, suggesting that habituation of reflexive saccades does not take place at the programming stage in the superior colliculus (SC), but at the later stage of saccade execution in the brainstem, where the competition between different saccades might be resolved. This scenario challenges one of the main assumptions of the competitive integration model for oculomotor control, which assumes that competition between exogenous and endogenous saccade programs occurs in the (SC). Our results and interpretation are instead in agreement with neurophysiological studies in non-human primates showing that saccadic adaption, another form of oculomotor plasticity, takes place downstream from the SC.

Context learning before birth: evidence from the chick embryo.

Learning contextual information to form associative memories with stimuli of interest is an important brain function in both human and non-human animals. Intuitively, one would expect that such a sophisticated cognitive skill develops postnatally, as the organism starts exploring the surrounding environment to search for significant contingencies among stimuli. Here we show, instead, that even before hatching, domestic chicks are capable of forming associative memories between discrete alerting sounds and the surrounding context, as attested by the fact that habituation of the freezing response to the sounds is affected by the context of stimulation. This finding indicates that, while in the egg, chicks recognize and learn the context in which they are stimulated. Hence, context learning in chicks is an innate brain function already active before birth, which can provide an immediate survival advantage to the newborns of this precocial avian species.

Getting rid of visual distractors: the why, when, how, and where.

Distractor suppression, or the ability to disregard salient distractors while dealing with task-relevant information, is a key component of selective attention. Recent research has shown that distractor suppression can take place in different circumstances and present itself in different guises, which is presumably paralleled by a multiplicity of underlying neural mechanisms. In this review article, we discuss a number of central themes concerning distractor suppression and the underlying neural mechanisms, and also highlight several unresolved issues that will have to be addressed in future investigations.

Multiple reward-cue contingencies favor expectancy over uncertainty in shaping the reward-cue attentional salience.

Reward-predicting cues attract attention because of their motivational value. A debated question regards the conditions under which the cue's attentional salience is governed more by reward expectancy rather than by reward uncertainty. To help shedding light on this relevant issue, here, we manipulated expectancy and uncertainty using three levels of reward-cue contingency, so that, for example, a high level of reward expectancy (p = .8) was compared with the highest level of reward uncertainty (p = .5). In Experiment 1, the best reward-cue during conditioning was preferentially attended in a subsequent visual search task. This result was replicated in Experiment 2, in which the cues were matched in terms of response history. In Experiment 3, we implemented a hybrid procedure consisting of two phases: an omission contingency procedure during conditioning, followed by a visual search task as in the previous experiments. Crucially, during both phases, the reward-cues were never task relevant. Results confirmed that, when multiple reward-cue contingencies are explored by a human observer, expectancy is the major factor controlling both the attentional and the oculomotor salience of the reward-cue.

Habituation of oculomotor capture by sudden onsets: Stimulus specificity, spontaneous recovery and dishabituation.

Previous studies have confirmed that visual onsets are very powerful in attracting our gaze. The reflexive saccades triggered by sudden onsets have a high adaptive value because they ensure a rapid inspection of potentially appetitive or dangerous events. Here we showed, however, that such exogenously driven saccades are rapidly attenuated as the exposure to the same irrelevant onset progresses. Crucially, we found that such decrement in oculomotor capture conforms to several key features of habituation, an ancestral and widespread form of learning, consisting in a response reduction to a repeated irrelevant stimulation. In addition, we documented both spontaneous recovery and specificity of habituation, the phenomenon of dishabituation, and that habituation of capture was stimulation-frequency dependent. We also found both short-term and long-term habituation of oculomotor capture. Although we cannot exclude the contribution of top-down strategic inhibitory mechanisms to filter the onset distractors, the oculomotor capture reduction that we have documented finds a straightforward explanation in the neural and cognitive mechanisms underlying habituation of the orienting reflex, as originally suggested by Sokolov. Our study lends support to the idea that habituation plays a key filtering role in regulating the exogenous saccadic response triggered by peripheral onset distractors. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Short-term memory in habituation and dishabituation of newborn chicks' freezing response.

Cognitive models of habituation and dishabituation postulate that the latter is attributable to the perturbation of the model of the repeated stimulation stored in short-term memory (STM) by the occurrence of a new stimulus, called dishabituator. However, although both behavioral phenomena depend on STM, previous studies in Aplysia have found that dishabituation seems to require further steps of development of the STM system to emerge. Here, we addressed whether this is a universal condition for the appearance of the 2 forms of learning, namely whether dishabituation must necessarily follow habituation. To this aim, we studied habituation and dishabituation of the freezing response to a sudden acoustic stimulation in newly hatched chicks (1 day old vs. 3 days old). The results showed that in chicks, dishabituation was fully present a few hours after hatching, a pattern of results indicating that, in this precocial avian species, habituation and dishabituation share the same developmental trajectory and the underlying STM mechanisms are simultaneously operative soon after birth. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Desensitizing the attention system to distraction while idling: A new latent learning phenomenon in the visual attention domain.

For the good and the bad, the world around us is full of distraction. In particular, onset stimuli that appear abruptly in the scene grab attention, thus disrupting the ongoing task. Different cognitive mechanisms for distractor filtering have been proposed, but prevalent accounts share the idea that filtering is accomplished to shield target processing from interference. Here we provide novel evidence that challenges this view, as passive exposure to a repeating visual onset is sufficient to trigger learning-dependent mechanisms to filter the unwanted stimulation. In other words, our study shows that during passive exposure the cognitive system is capable of learning about the characteristics of the salient yet irrelevant stimulation, and to reduce the responsiveness of the attention system to it, thus significantly decreasing the impact of the distractor upon start of an active task. However, despite passive viewing efficiently attenuates the spatial capture of attention, a short-lived performance cost is found when the distractor is initially encountered within the context of the active task. This cost, which dissipates in a few trials, likely reflects the need to familiarize with the distractor, already seen during passive viewing, in the new context of the active task. Although top-down inhibitory signals can be applied to distractors for the successful completion of goal-directed behavior, our results emphasize the role of more automatic habituation mechanisms for distraction exclusion based on a neural model of the history of the irrelevant stimulation. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Rapid plasticity attenuation soon after birth revealed by habituation in newborn chicks.

Habituation reflects a form of experience-dependent plasticity whereby the organism progressively learns to ignore the irrelevant information repeatedly encountered. Here, we measured the freezing response to a repeated loud noise in three groups of newborn chicks (Gallus gallus) of different ages (1-2 Day old, 2-3 Day old, and 3-4 Day old) to investigate the ontogeny of habituation in this avian species. Habituation was already present 1 Day after hatching, revealing that the neural mechanisms underlying this form of plasticity are immediately active. Unexpectedly, however, we also found that in the second Day of stimulation the amount of learning was significantly attenuated in chicks of 3-4 days of age as compared to the younger animals, thus showing that 24-48 hr of maturation were sufficient to reduce plasticity. While previous findings in other animal species have proved the existence of a precocious critical period of plasticity in early cortical areas by means of sensory deprivation, our results demonstrate that during the initial development of an intact avian brain also the degree of plasticity underlying a learning process like habituation is maximal soon after birth, and then is subject to a rapid attenuation.