Neurocognitive mechanisms of synesthesia

Synesthesia is a condition in which stimulation of one sensory modality causes unusual experiences in a second, unstimulated modality. Although long treated as a curiosity, recent research with a combination of phenomenological, behavioral, and neuroimaging methods has begun to identify the cognitive and neural basis of synesthesia. Here, we review this literature with an emphasis on grapheme-color synesthesia, in which viewing letters and numbers induces the perception of colors. We discuss both the substantial progress that has been made in the past fifteen years and some open questions. In particular, we focus on debates in the field relating to the neural basis of synesthesia, including the relationship between synesthesia and attention and the role of meaning in synesthetic colors. We propose that some, but probably not all, of these differences can be accounted for by differences in the synesthetes studied and discuss some methodological implications of these individual differences.     

Survival of the Synesthesia Gene: Why Do People Hear Colors and Taste Words?

Synesthesia is a perceptual experience in which stimuli presented through one modality will spontaneously evoke sensations in an unrelated modality. The condition occurs from increased communication between sensory regions and is involuntary, automatic, and stable over time. While synesthesia can occur in response to drugs, sensory deprivation, or brain damage, research has largely focused on heritable variants comprising roughly 4% of the general population. Genetic research on synesthesia suggests the phenomenon is heterogeneous and polygenetic, yet it remains unclear whether synesthesia ever provided a selective advantage or is merely a byproduct of some other useful selected trait. Progress in uncovering the genetic basis of synesthesia will help us understand why synesthesia has been conserved in the population.     

Enhanced cortical excitability in grapheme-color synesthesia and its modulation

Synesthesia is an unusual condition characterized by the over-binding of two or more features and the concomitant automatic and conscious experience of atypical, ancillary images or perceptions. Previous research suggests that synesthetes display enhanced modality-specific perceptual processing, but it remains unclear whether enhanced processing contributes to conscious awareness of color photisms. In three experiments, we investigated whether grapheme-color synesthesia is characterized by enhanced cortical excitability in primary visual cortex and the role played by this hyperexcitability in the expression of synesthesia. Using transcranial magnetic stimulation, we show that synesthetes display 3-fold lower phosphene thresholds than controls during stimulation of the primary visual cortex. We next used transcranial direct current stimulation to discriminate between two competing hypotheses of the role of hyperexcitability in the expression of synesthesia. We demonstrate that synesthesia can be selectively augmented with cathodal stimulation and attenuated with anodal stimulation of primary visual cortex. A control task revealed that the effect of the brain stimulation was specific to the experience of synesthesia. These results indicate that hyperexcitability acts as a source of noise in visual cortex that influences the availability of the neuronal signals underlying conscious awareness of synesthetic photisms.     

Training Synesthetic Letter-color Associations by Reading in Color

Synesthesia is a rare condition in which a stimulus from one modality automatically and consistently triggers unusual sensations in the same and/or other modalities. A relatively common and well-studied type is grapheme-color synesthesia, defined as the consistent experience of color when viewing, hearing and thinking about letters, words and numbers. We describe our method for investigating to what extent synesthetic associations between letters and colors can be learned by reading in color in nonsynesthetes. Reading in color is a special method for training associations in the sense that the associations are learned implicitly while the reader reads text as he or she normally would and it does not require explicit computer-directed training methods. In this protocol, participants are given specially prepared books to read in which four high-frequency letters are paired with four high-frequency colors. Participants receive unique sets of letter-color pairs based on their pre-existing preferences for colored letters. A modified Stroop task is administered before and after reading in order to test for learned letter-color associations and changes in brain activation. In addition to objective testing, a reading experience questionnaire is administered that is designed to probe for differences in subjective experience. A subset of questions may predict how well an individual learned the associations from reading in color. Importantly, we are not claiming that this method will cause each individual to develop grapheme-color synesthesia, only that it is possible for certain individuals to form letter-color associations by reading in color and these associations are similar in some aspects to those seen in developmental grapheme-color synesthetes. The method is quite flexible and can be used to investigate different aspects and outcomes of training synesthetic associations, including learning-induced changes in brain function and structure.     

A Whole-Genome Scan and Fine-Mapping Linkage Study of Auditory-Visual Synesthesia Reveals Evidence of Linkage to Chromosomes 2q24, 5q33, 6p12, and 12p12

Synesthesia, a neurological condition affecting between 0.05%–1% of the population, is characterized by anomalous sensory perception and associated alterations in cognitive function due to interference from synesthetic percepts. A stimulus in one sensory modality triggers an automatic, consistent response in either another modality or a different aspect of the same modality. Familiality studies show evidence of a strong genetic predisposition; whereas initial pedigree analyses supported a single-gene X-linked dominant mode of inheritance with a skewed F:M ratio and a notable absence of male-to-male transmission, subsequent analyses in larger samples indicated that the mode of inheritance was likely to be more complex. Here, we report the results of a whole-genome linkage scan for auditory-visual synesthesia with 410 microsatellite markers at 9.05 cM density in 43 multiplex families (n = 196) with potential candidate regions fine-mapped at 5 cM density. Using NPL and HLOD analysis, we identified four candidate regions. Significant linkage at the genome-wide level was detected to chromosome 2q24 (HLOD = 3.025, empirical genome-wide p = 0.047). Suggestive linkage was found to chromosomes 5q33, 6p12, and 12p12. No support was found for linkage to the X chromosome; furthermore, we have identified two confirmed cases of male-to-male transmission of synesthesia. Our results demonstrate that auditory-visual synesthesia is likely to be an oligogenic disorder subject to multiple modes of inheritance and locus heterogeneity. This study comprises a significant step toward identifying the genetic substrates underlying synesthesia, with important implications for our understanding of the role of genes in human cognition and perception.     

Sensory Perception: Lessons from Synesthesia: Using Synesthesia to Inform the Understanding of Sensory Perception

Synesthesia, the conscious, idiosyncratic, repeatable, and involuntary sensation of one sensory modality in response to another, is a condition that has puzzled both researchers and philosophers for centuries. Much time has been spent proving the condition’s existence as well as investigating its etiology, but what can be learned from synesthesia remains a poorly discussed topic. Here, synaesthesia is presented as a possible answer rather than a question to the current gaps in our understanding of sensory perception. By first appreciating the similarities between normal sensory perception and synesthesia, one can use what is known about synaesthesia, from behavioral and imaging studies, to inform our understanding of “normal” sensory perception. In particular, in considering synesthesia, one can better understand how and where the different sensory modalities interact in the brain, how different sensory modalities can interact without confusion ― the binding problem ― as well as how sensory perception develops.     

Twice-Born, Once Conceived: Meaning Construction and Cultural Cognition

Cultural cognition is the product of two different sorts of meaning: (a) the (objective) semiotic organization of cultural texts or models, and (b) the (subjective) processes of meaning construction through which cultural symbols become available to consciousness as "experience." This article proposes a way to bridge these two kinds of meaning by considering how cultural knowledge is grounded in sensory experience. Several cognitive processes (schematization, synesthesia, secondary intersubjectivity) are proposed for linking the objectively available schemata found in cultural practices and the processes of meaning construction by which individuals appropriate symbols to consciousness. The nature of the relation between public symbols and individual experience is discussed in relation to a number of current issues in post-structuralist culture theory.     

Assessment of the Hemispheric Lateralization of Grapheme-Color Synesthesia with Stroop-Type Tests

Grapheme-color synesthesia, the idiosyncratic, arbitrary association of colors to letters or numbers, develops in childhood once reading is mastered. Because language processing is strongly left-lateralized in most individuals, we hypothesized that grapheme-color synesthesia could be left-lateralized as well. We used synesthetic versions of the Stroop test with colored letters and numbers presented either in the right or the left visual field of thirty-four synesthetes. Interference by synesthetic colors was stronger for stimuli in the right hemifield (first experiment, color naming task). Synesthetes were also faster in the right hemifield when naming the synesthetic color of graphemes (second experiment). Overall, the lateralization effect was 7 ms (the 95% confidence interval was [1.5 12] ms), a delay compatible with an additional callosal transfer for stimuli presented in the left hemifield. Though weak, this effect suggests that the association of synesthetic colors to graphemes may be preferentially processed in the left hemisphere. We speculate that this left-lateralization could be a landmark of synesthetic grapheme-color associations, if not found for color associations learnt by non-synesthete adults.     

Components of Attention in Grapheme-Color Synesthesia: A Modeling Approach

Grapheme-color synesthesia is a condition where the perception of graphemes consistently and automatically evokes an experience of non-physical color. Many have studied how synesthesia affects the processing of achromatic graphemes, but less is known about the synesthetic processing of physically colored graphemes. Here, we investigated how the visual processing of colored letters is affected by the congruence or incongruence of synesthetic grapheme-color associations. We briefly presented graphemes (10–150 ms) to 9 grapheme-color synesthetes and to 9 control observers. Their task was to report as many letters (targets) as possible, while ignoring digit (distractors). Graphemes were either congruently or incongruently colored with the synesthetes’ reported grapheme-color association. A mathematical model, based on Bundesen’s (1990) Theory of Visual Attention (TVA), was fitted to each observer’s data, allowing us to estimate discrete components of visual attention. The models suggested that the synesthetes processed congruent letters faster than incongruent ones, and that they were able to retain more congruent letters in visual short-term memory, while the control group’s model parameters were not significantly affected by congruence. The increase in processing speed, when synesthetes process congruent letters, suggests that synesthesia affects the processing of letters at a perceptual level. To account for the benefit in processing speed, we propose that synesthetic associations become integrated into the categories of graphemes, and that letter colors are considered as evidence for making certain perceptual categorizations in the visual system. We also propose that enhanced visual short-term memory capacity for congruently colored graphemes can be explained by the synesthetes’ expertise regarding their specific grapheme-color associations.     

Salivary testosterone measurements among women: relative magnitude of circadian and menstrual cycles.

Measures of testosterone among women are potentially useful in behavioral research, but information is needed on how much error is introduced by variability across the menstrual cycle. Morning and evening salivary testosterone concentrations were measured at weekly intervals across one menstrual cycle in each of 22 women, using the luteinizing hormone surge to mark midcycle. Menstrual cycles were statistically significant but smaller than daily cycles or individual differences. Menstrual cycle effects can be ignored in most research relating psychological and behavioral variables to individual differences in testosterone.     

Genetic and environmental influences on human psychological differences

Psychological researchers typically distinguish five major domains of individual differences in human behavior: cognitive abilities, personality, social attitudes, psychological interests, and psychopathology (Lubinski, 2000). In this article we: discuss a number of methodological errors commonly found in research on human individual differences; introduce a broad framework for interpreting findings from contemporary behavioral genetic studies; briefly outline the basic quantitative methods used in human behavioral genetic research; review the major criticisms of behavior genetic designs, with particular emphasis on the twin and adoption methods; describe the major or dominant theoretical scheme in each domain; and review behavioral genetic findings in all five domains. We conclude that there is now strong evidence that virtually all individual psychological differences, when reliably measured, are moderately to substantially heritable.     

An ontogenetic perspective on individual differences

Phenotypic differences among individuals can arise during any stage of life. Although several distinct processes underlying individual differences have been defined and studied (e.g. parental effects, senescence), we lack an explicit, unified perspective for understanding how these processes contribute separately and synergistically to observed variation in functional traits. We propose a conceptual framework based on a developmental view of life-history variation, linking each ontogenetic stage with the types of individual differences originating during that period. In our view, the salient differences among these types are encapsulated by three key criteria: timing of onset, when fitness consequences are realized, and potential for reversibility. To fill a critical gap in this framework, we formulate a new term to refer to individual differences generated during adulthood—reversible state effects. We define these as ‘reversible changes in a functional trait resulting from life-history trade-offs during adulthood that affect fitness’, highlighting how the adult phenotype can be repeatedly altered in response to environmental variation. Defining individual differences in terms of trade-offs allows explicit predictions regarding when and where fitness consequences should be expected. Moreover, viewing individual differences in a developmental context highlights how different processes can work in concert to shape phenotype and fitness, and lays a foundation for research linking individual differences to ecological and evolutionary theory.     

Research on fish ecology in Japan: a brief history and selected review

Fish play an important role in the culture of Japan, supplying the primary source of food protein. Research on fish ecology in Japan began developing about 1955, and paralleled that in North America and Europe, but has a number of unique differences. Two main research foci, stream fish ecology and ecology of Lake Biwa, were founded by H. Kawanabe and his colleagues while graduate students in D. Miyadi's laboratory at Kyoto University in the 1950s. The focus on studies of individual differences in ecology, life history, and behavior by direct observation that were developed in this laboratory had a pervasive influence on research that has continued to the present. In the 1980s, Kawanabe, who had succeeded Miyadi as laboratory head, also co-organized a major research project on the complex communities of cichlid fishes in Lake Tanganyika, which has involved nearly every major Japanese investigator in fish ecology since. A review of research conducted by Japanese investigators in stream fish ecology, ecology of fishes in lakes Biwa and Tanganyika, and marine reef fish ecology revealed a wealth of literature of which most English-speaking fish ecologists are unaware. The most striking difference between Western and Japanese research is the focus on detailed observations and experiments in natural habitats of individual differences in behavior, life history, and ecology, and how these ultimately affect processes at the population and community level, as amply demonstrated by Kawanabe's early work on ayu, Plecoglossus altivelis. This approach predated by 20–30 years the current interest in individual differences and individual-based models in North America and Europe.     

Personality influences the neural responses to viewing facial expressions of emotion

Cognitive research has long been aware of the relationship between individual differences in personality and performance on behavioural tasks. However, within the field of cognitive neuroscience, the way in which such differences manifest at a neural level has received relatively little attention. We review recent research addressing the relationship between personality traits and the neural response to viewing facial signals of emotion. In one section, we discuss work demonstrating the relationship between anxiety and the amygdala response to facial signals of threat. A second section considers research showing that individual differences in reward drive (behavioural activation system), a trait linked to aggression, influence the neural responsivity and connectivity between brain regions implicated in aggression when viewing facial signals of anger. Finally, we address recent criticisms of the correlational approach to fMRI analyses and conclude that when used appropriately, analyses examining the relationship between personality and brain activity provide a useful tool for understanding the neural basis of facial expression processing and emotion processing in general.     

Understanding the unexplained: The magnitude and correlates of individual differences in residual variance

Behavioral and physiological ecologists have long been interested in explaining the causes and consequences of trait variation, with a focus on individual differences in mean values. However, the majority of phenotypic variation typically occurs within individuals, rather than among individuals (as indicated by average repeatability being less than 0.5). Recent studies have further shown that individuals can also differ in the magnitude of variation that is unexplained by individual variation or environmental factors (i.e., residual variation). The significance of residual variation, or why individuals differ, is largely unexplained, but is important from evolutionary, methodological, and statistical perspectives. Here, we broadly reviewed literature on individual variation in behavior and physiology, and located 39 datasets with sufficient repeated measures to evaluate individual differences in residual variance. We then analyzed these datasets using methods that permit direct comparisons of parameters across studies. This revealed substantial and widespread individual differences in residual variance. The magnitude of individual variation appeared larger in behavioral traits than in physiological traits, and heterogeneity was greater in more controlled situations. We discuss potential ecological and evolutionary implications of individual differences in residual variance and suggest productive future research directions.     

Dominance status and certain operants in a communal colony of rhesus macaques

This study was designed to test the hypothesis that in some species of primates individual differences in responsiveness to certain situations is related to dominance status. During the first phase of the study, the existence of a linear dominance hierarchy was confirmed by ratings of agonistic interactions. In the second phase, bar-pressing behavior was recorded on a cumulative recorder while the experimenter simultaneously rated, at 30-second intervals, all animals present in the research setting. Results indicated that dominance status was systematically related both to rate of bar-pressing and to duration of response blocks, with the more dominant animals bar-pressing at slower rates for longer blocks of time. The finding that individual differences in rate did not vary with social context suggests that dominance-related differences in responsiveness may be quite stable. Certain dominancerelated trends in the variation of social context in the research setting were also noted.     

Individual differences in behavioural plasticities

Interest in individual differences in animal behavioural plasticities has surged in recent years, but research in this area has been hampered by semantic confusion as different investigators use the same terms (e.g. plasticity, flexibility, responsiveness) to refer to different phenomena. The first goal of this review is to suggest a framework for categorizing the many different types of behavioural plasticities, describe examples of each, and indicate why using reversibility as a criterion for categorizing behavioural plasticities is problematic. This framework is then used to address a number of timely questions about individual differences in behavioural plasticities. One set of questions concerns the experimental designs that can be used to study individual differences in various types of behavioural plasticities. Although within‐individual designs are the default option for empirical studies of many types of behavioural plasticities, in some situations (e.g. when experience at an early age affects the behaviour expressed at subsequent ages), ‘replicate individual’ designs can provide useful insights into individual differences in behavioural plasticities. To date, researchers using within‐individual and replicate individual designs have documented individual differences in all of the major categories of behavioural plasticities described herein. Another important question is whether and how different types of behavioural plasticities are related to one another. Currently there is empirical evidence that many behavioural plasticities [e.g. contextual plasticity, learning rates, IIV (intra‐individual variability), endogenous plasticities, ontogenetic plasticities) can themselves vary as a function of experiences earlier in life, that is, many types of behavioural plasticity are themselves developmentally plastic. These findings support the assumption that differences among individuals in prior experiences may contribute to individual differences in behavioural plasticities observed at a given age. Several authors have predicted correlations across individuals between different types of behavioural plasticities, i.e. that some individuals will be generally more plastic than others. However, empirical support for most of these predictions, including indirect evidence from studies of relationships between personality traits and plasticities, is currently sparse and equivocal. The final section of this review suggests how an appreciation of the similarities and differences between different types of behavioural plasticities may help theoreticians formulate testable models to explain the evolution of individual differences in behavioural plasticities and the evolutionary and ecological consequences of individual differences in behavioural plasticities.     

Designing theoretically-informed implementation interventions

Background

A better theoretical base for understanding professional behaviour change is needed to support evidence-based changes in medical practice. Traditionally strategies to encourage changes in clinical practices have been guided empirically, without explicit consideration of underlying theoretical rationales for such strategies. This paper considers a theoretical framework for reasoning from within psychology for identifying individual differences in cognitive processing between doctors that could moderate the decision to incorporate new evidence into their clinical decision-making.

Discussion

Parallel dual processing models of reasoning posit two cognitive modes of information processing that are in constant operation as humans reason. One mode has been described as experiential, fast and heuristic; the other as rational, conscious and rule based. Within such models, the uptake of new research evidence can be represented by the latter mode; it is reflective, explicit and intentional. On the other hand, well practiced clinical judgments can be positioned in the experiential mode, being automatic, reflexive and swift. Research suggests that individual differences between people in both cognitive capacity (e.g., intelligence) and cognitive processing (e.g., thinking styles) influence how both reasoning modes interact. This being so, it is proposed that these same differences between doctors may moderate the uptake of new research evidence. Such dispositional characteristics have largely been ignored in research investigating effective strategies in implementing research evidence. Whilst medical decision-making occurs in a complex social environment with multiple influences and decision makers, it remains true that an individual doctor's judgment still retains a key position in terms of diagnostic and treatment decisions for individual patients. This paper argues therefore, that individual differences between doctors in terms of reasoning are important considerations in any discussion relating to changing clinical practice.

Summary

It is imperative that change strategies in healthcare consider relevant theoretical frameworks from other disciplines such as psychology. Generic dual processing models of reasoning are proposed as potentially useful in identifying factors within doctors that may moderate their individual uptake of evidence into clinical decision-making. Such factors can then inform strategies to change practice.     

Individual differences and metacognitive knowledge of visual search strategy

A crucial ability for an organism is to orient toward important objects and to ignore temporarily irrelevant objects. Attention provides the perceptual selectivity necessary to filter an overwhelming input of sensory information to allow for efficient object detection. Although much research has examined visual search and the 'template' of attentional set that allows for target detection, the behavior of individual subjects often reveals the limits of experimental control of attention. Few studies have examined important aspects such as individual differences and metacognitive strategies. The present study analyzes the data from two visual search experiments for a conjunctively defined target (Proulx, 2007). The data revealed attentional capture blindness, individual differences in search strategies, and a significant rate of metacognitive errors for the assessment of the strategies employed. These results highlight a challenge for visual attention studies to account for individual differences in search behavior and distractibility, and participants that do not (or are unable to) follow instructions.     

Solving the puzzle of collective action through inter-individual differences

Models of collective action infrequently account for differences across individuals beyond a limited set of strategies, ignoring variation in endowment (e.g. physical condition, wealth, knowledge, personality, support), individual costs of effort, or expected gains from cooperation. However, behavioural research indicates these inter-individual differences can have significant effects on the dynamics of collective action. The papers contributed to this theme issue evaluate how individual differences affect the propensity to cooperate, and how they can catalyse others’ likelihood of cooperation (e.g. via leadership). Many of the papers emphasize the relationship between individual decisions and socio-ecological context, particularly the effect of group size. All together, the papers in this theme issue provide a more complete picture of collective action, by embracing the reality of inter-individual variation and its multiple roles in the success or failure of collective action.