Sensory and decision-making processes underlying perceptual adaptation.

Perceptual systems adapt to their inputs. As a result, prolonged exposure to particular stimuli alters judgments about subsequent stimuli. This phenomenon is commonly assumed to be sensory in origin. Changes in the decision-making process, however, may also be a component of adaptation. Here, we quantify sensory and decision-making contributions to adaptation in a facial expression paradigm. As expected, exposure to happy or sad expressions shifts the psychometric function toward the adaptor. More surprisingly, response times show both an overall decline and an asymmetry, with faster responses opposite the adapting category, implicating a substantial change in the decision-making process. Specifically, we infer that sensory changes from adaptation are accompanied by changes in how much sensory information is accumulated for the two choices. We speculate that adaptation influences implicit expectations about the stimuli one will encounter, causing modifications in the decision-making process as part of a normative response to a change in context.

Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation.

The parahippocampal place area (PPA) is a widely studied high-level visual region in the human brain involved in place and scene processing. The goal of the present study was to identify the most probable location of place-selective voxels in medial ventral temporal cortex. To achieve this goal, we first used cortex-based alignment (CBA) to create a probabilistic place-selective region of interest (ROI) from one group of 12 participants. We then tested how well this ROI could predict place selectivity in each hemisphere within a new group of 12 participants. Our results reveal that a probabilistic ROI (pROI) generated from one group of 12 participants accurately predicts the location and functional selectivity in individual brains from a new group of 12 participants, despite between subject variability in the exact location of place-selective voxels relative to the folding of parahippocampal cortex. Additionally, the prediction accuracy of our pROI is significantly higher than that achieved by volume-based Talairach alignment. Comparing the location of the pROI of the PPA relative to published data from over 500 participants, including data from the Human Connectome Project, shows a striking convergence of the predicted location of the PPA and the cortical location of voxels exhibiting the highest place selectivity across studies using various methods and stimuli. Specifically, the most predictive anatomical location of voxels exhibiting the highest place selectivity in medial ventral temporal cortex is the junction of the collateral and anterior lingual sulci. Methodologically, we make this pROI freely available (vpnl.stanford.edu/PlaceSelectivity), which provides a means to accurately identify a functional region from anatomical MRI data when fMRI data are not available (for example, in patient populations). Theoretically, we consider different anatomical and functional factors that may contribute to the consistent anatomical location of place selectivity relative to the folding of high-level visual cortex.

Identification of the ventral occipital visual field maps in the human brain.

The location and topography of the first three visual field maps in the human brain, V1-V3, are well agreed upon and routinely measured across most laboratories. The position of 4 th visual field map, 'hV4', is identified with less consistency in the neuroimaging literature.  Using magnetic resonance imaging data, we describe landmarks to help identify the position and borders of 'hV4'. The data consist of anatomical images, visualized as cortical meshes to highlight the sulcal and gyral patterns, and functional data obtained from retinotopic mapping experiments, visualized as eccentricity and angle maps on the cortical surface. Several features of the functional and anatomical data can be found across nearly all subjects and are helpful for identifying the location and extent of the hV4 map. The medial border of hV4 is shared with the posterior, ventral portion of V3, and is marked by a retinotopic representation of the upper vertical meridian. The anterior border of hV4 is shared with the VO-1 map, and falls on a retinotopic representation of the peripheral visual field, usually coincident with the posterior transverse collateral sulcus. The ventro-lateral edge of the map typically falls on the inferior occipital gyrus, where functional MRI artifacts often obscure the retinotopic data. Finally, we demonstrate the continuity of retinotopic parameters between hV4 and its neighbors; hV4 and V3v contain iso-eccentricity lines in register, whereas hV4 and VO-1 contain iso-polar angle lines in register. Together, the multiple constraints allow for a consistent identification of the hV4 map across most human subjects.

The field of view available to the ventral occipito-temporal reading circuitry.

Skilled reading requires rapidly recognizing letters and word forms; people learn this skill best for words presented in the central visual field. Measurements over the last decade have shown that when children learn to read, responses within ventral occipito-temporal cortex (VOT) become increasingly selective to word forms. We call these regions the VOT reading circuitry (VOTRC). The portion of the visual field that evokes a response in the VOTRC is called the field of view (FOV). We measured the FOV of the VOTRC and found that it is a small subset of the entire field of view available to the human visual system. For the typical subject, the FOV of the VOTRC in each hemisphere is contralaterally and foveally biased. The FOV of the left VOTRC extends ∼9° into the right visual field and ∼4° into the left visual field along the horizontal meridian. The FOV of the right VOTRC is roughly mirror symmetric to that of the left VOTRC. The size and shape of the FOV covers the region of the visual field that contains relevant information for reading English. It may be that the size and shape of the FOV, which varies between subjects, will prove useful in predicting behavioral aspects of reading.

Corresponding ECoG and fMRI category-selective signals in human ventral temporal cortex.

Functional magnetic resonance imaging (fMRI) and electrocorticography (ECoG) research have been influential in revealing the functional characteristics of category-selective responses in human ventral temporal cortex (VTC). One important, but unanswered, question is how these two types of measurements might be related with respect to the VTC. Here we examined which components of the ECoG signal correspond to the fMRI response by using a rare opportunity to measure both fMRI and ECoG responses from the same individuals to images of exemplars of various categories including faces, limbs, cars and houses. Our data reveal three key findings. First, we discovered that the coupling between fMRI and ECoG responses is frequency and time dependent. The strongest and most sustained correlation is observed between fMRI and high frequency broadband (HFB) ECoG responses (30-160 hz). In contrast, the correlation between fMRI and ECoG signals in lower frequency bands is temporally transient, where the correlation is initially positive, but then tapers off or becomes negative. Second, we find that the strong and positive correlation between fMRI and ECoG signals in all frequency bands emerges rapidly around 100 ms after stimulus onset, together with the onset of the first stimulus-driven neural signals in VTC. Third, we find that the spatial topology and representational structure of category-selectivity in VTC reflected in ECoG HFB responses mirrors the topology and structure observed with fMRI. These findings of a strong and rapid coupling between fMRI and HFB responses validate fMRI measurements of functional selectivity with recordings of direct neural activity and suggest that fMRI category-selective signals in VTC are associated with feed-forward neural processing.

Human V4 and ventral occipital retinotopic maps.

The ventral surface of the human occipital lobe contains multiple retinotopic maps. The most posterior of these maps is considered a potential homolog of macaque V4, and referred to as human V4 ("hV4"). The location of the hV4 map, its retinotopic organization, its role in visual encoding, and the cortical areas it borders have been the subject of considerable investigation and debate over the last 25 years. We review the history of this map and adjacent maps in ventral occipital cortex, and consider the different hypotheses for how these ventral occipital maps are organized. Advances in neuroimaging, computational modeling, and characterization of the nearby anatomical landmarks and functional brain areas have improved our understanding of where human V4 is and what kind of visual representations it contains.

The physiology of perception in human temporal lobe is specialized for contextual novelty.

The human ventral temporal cortex has regions that are known to selectively process certain categories of visual inputs; they are specialized for the content ("faces," "places," "tools") and not the form ("line," "patch") of the image being seen. In our study, human patients with implanted electrocorticography (ECoG) electrode arrays were shown sequences of simple face and house pictures. We quantified neuronal population activity, finding robust face-selective sites on the fusiform gyrus and house-selective sites on the lingual/parahippocampal gyri. The magnitude and timing of single trials were compared between novel ("house-face") and repeated ("face-face") stimulus-type responses. More than half of the category-selective sites showed significantly greater total activity for novel stimulus class. Approximately half of the face-selective sites (and none of the house-selective sites) showed significantly faster latency to peak (∼ 50 ms) for novel stimulus class. This establishes subregions within category-selective areas that are differentially tuned to novelty in sequential context, where novel stimuli are processed faster in some regions, and with increased activity in others.

Prevalence of learned grapheme-color pairings in a large online sample of synesthetes.

In this paper we estimate the minimum prevalence of grapheme-color synesthetes with letter-color matches learned from an external stimulus, by analyzing a large sample of English-speaking grapheme-color synesthetes. We find that at least 6% (400/6588 participants) of the total sample learned many of their matches from a widely available colored letter toy. Among those born in the decade after the toy began to be manufactured, the proportion of synesthetes with learned letter-color pairings approaches 15% for some 5-year periods. Among those born 5 years or more before it was manufactured, none have colors learned from the toy. Analysis of the letter-color matching data suggests the only difference between synesthetes with matches to the toy and those without is exposure to the stimulus. These data indicate learning of letter-color pairings from external contingencies can occur in a substantial fraction of synesthetes, and are consistent with the hypothesis that grapheme-color synesthesia is a kind of conditioned mental imagery.

Functionally defined white matter reveals segregated pathways in human ventral temporal cortex associated with category-specific processing.

It is unknown if the white-matter properties associated with specific visual networks selectively affect category-specific processing. In a novel protocol we combined measurements of white-matter structure, functional selectivity, and behavior in the same subjects. We find two parallel white-matter pathways along the ventral temporal lobe connecting to either face-selective or place-selective regions. Diffusion properties of portions of these tracts adjacent to face- and place-selective regions of ventral temporal cortex correlate with behavioral performance for face or place processing, respectively. Strikingly, adults with developmental prosopagnosia (face blindness) express an atypical structure-behavior relationship near face-selective cortex, suggesting that white-matter atypicalities in this region may have behavioral consequences. These data suggest that examining the interplay between cortical function, anatomical connectivity, and visual behavior is integral to understanding functional networks and their role in producing visual abilities and deficits.

Cultural differences in perceptual reorganization in US and Pirahã adults.

Visual illusions and other perceptual phenomena can be used as tools to uncover the otherwise hidden constructive processes that give rise to perception. Although many perceptual processes are assumed to be universal, variable susceptibility to certain illusions and perceptual effects across populations suggests a role for factors that vary culturally. One striking phenomenon is seen with two-tone images-photos reduced to two tones: black and white. Deficient recognition is observed in young children under conditions that trigger automatic recognition in adults. Here we show a similar lack of cue-triggered perceptual reorganization in the Pirahã, a hunter-gatherer tribe with limited exposure to modern visual media, suggesting such recognition is experience- and culture-specific.

Where is human V4? Predicting the location of hV4 and VO1 from cortical folding.

A strong relationship between cortical folding and the location of primary sensory areas in the human brain is well established. However, it is unknown if coupling between functional responses and gross anatomy is found at higher stages of sensory processing. We examined the relationship between cortical folding and the location of the retinotopic maps hV4 and VO1, which are intermediate stages in the human ventral visual processing stream. Our data show a consistent arrangement of the eccentricity maps within hV4 and VO1 with respect to anatomy, with the consequence that the hV4/VO1 boundary is found consistently in the posterior transverse collateral sulcus (ptCoS) despite individual variability in map size and cortical folding. Understanding this relationship allowed us to predict the location of visual areas hV4 and VO1 in a separate set of individuals, using only their anatomies, with >85% accuracy. These findings have important implications for understanding the relation between cortical folding and functional maps as well as for defining visual areas from anatomical landmarks alone.

Global similarity and pattern separation in the human medial temporal lobe predict subsequent memory.

Intense debate surrounds the role of medial temporal lobe (MTL) structures in recognition memory. Using high-resolution fMRI and analyses of pattern similarity in humans, we examined the encoding computations subserved by MTL subregions. Specifically, we tested the theory that MTL cortex supports memory by encoding overlapping representations, whereas hippocampus supports memory by encoding pattern-separated representations. Consistent with this view, the relationship between encoding pattern similarity and subsequent memory dissociated MTL cortex and hippocampus: later memory was predicted by greater across-item pattern similarity in perirhinal cortex and in parahippocampal cortex, but greater pattern distinctiveness in hippocampus. Additionally, by comparing neural patterns elicited by individual stimuli regardless of subsequent memory, we found that perirhinal cortex and parahippocampal cortex exhibited differential content sensitivity for multiple stimulus categories, whereas hippocampus failed to demonstrate content sensitivity. These data provide novel evidence that complementary MTL encoding computations subserve declarative memory.

Learning, memory, and synesthesia.

People with color-grapheme synesthesia experience color when viewing written letters or numerals, usually with a particular color evoked by each grapheme. Here, we report on data from 11 color-grapheme synesthetes who had startlingly similar color-grapheme pairings traceable to childhood toys containing colored letters. These are the first and only data to show learned synesthesia of this kind in more than a single individual. Whereas some researchers have focused on genetic and perceptual aspects of synesthesia, our results indicate that a complete explanation of synesthesia must also incorporate a central role for learning and memory. We argue that these two positions can be reconciled by thinking of synesthesia as the automatic retrieval of highly specific mnemonic associations, in which perceptual contents are brought to mind in a manner akin to mental imagery or the perceptual-reinstatement effects found in memory studies.

Electrical stimulation of human fusiform face-selective regions distorts face perception.

Face-selective neural responses in the human fusiform gyrus have been widely examined. However, their causal role in human face perception is largely unknown. Here, we used a multimodal approach of electrocorticography (ECoG), high-resolution functional magnetic resonance imaging (fMRI), and electrical brain stimulation (EBS) to directly investigate the causal role of face-selective neural responses of the fusiform gyrus (FG) in face perception in a patient implanted with subdural electrodes in the right inferior temporal lobe. High-resolution fMRI identified two distinct FG face-selective regions [mFus-faces and pFus-faces (mid and posterior fusiform, respectively)]. ECoG revealed a striking anatomical and functional correspondence with fMRI data where a pair of face-selective electrodes, positioned 1 cm apart, overlapped mFus-faces and pFus-faces, respectively. Moreover, electrical charge delivered to this pair of electrodes induced a profound face-specific perceptual distortion during viewing of real faces. Specifically, the subject reported a "metamorphosed" appearance of faces of people in the room. Several controls illustrate the specificity of the effect to the perception of faces. EBS of mFus-faces and pFus-faces neither produced a significant deficit in naming pictures of famous faces on the computer, nor did it affect the appearance of nonface objects. Further, the appearance of faces remained unaffected during both sham stimulation and stimulation of a pair of nearby electrodes that were not face-selective. Overall, our findings reveal a striking convergence of fMRI, ECoG, and EBS, which together offer a rare causal link between functional subsets of the human FG network and face perception.

Illusions of visual motion elicited by electrical stimulation of human MT complex.

Human cortical area MT(+) (hMT(+)) is known to respond to visual motion stimuli, but its causal role in the conscious experience of motion remains largely unexplored. Studies in non-human primates demonstrate that altering activity in area MT can influence motion perception judgments, but animal studies are inherently limited in assessing subjective conscious experience. In the current study, we use functional magnetic resonance imaging (fMRI), intracranial electrocorticography (ECoG), and electrical brain stimulation (EBS) in three patients implanted with intracranial electrodes to address the role of area hMT(+) in conscious visual motion perception. We show that in conscious human subjects, reproducible illusory motion can be elicited by electrical stimulation of hMT(+). These visual motion percepts only occurred when the site of stimulation overlapped directly with the region of the brain that had increased fMRI and electrophysiological activity during moving compared to static visual stimuli in the same individual subjects. Electrical stimulation in neighboring regions failed to produce illusory motion. Our study provides evidence for the sufficient causal link between the hMT(+) network and the human conscious experience of visual motion. It also suggests a clear spatial relationship between fMRI signal and ECoG activity in the human brain.

Deos the bairn not raed ervey lteter by istlef, but the wrod as a wlohe?

In this issue of Neuron, Glezer et al. find higher sensitivity to changes in real words than pseudowords in the left visual word form area (VWFA). Here we discuss the implications of their findings and the constraints they impose on neural coding in the lVWFA.

Russian blues reveal effects of language on color discrimination.

English and Russian color terms divide the color spectrum differently. Unlike English, Russian makes an obligatory distinction between lighter blues ("goluboy") and darker blues ("siniy"). We investigated whether this linguistic difference leads to differences in color discrimination. We tested English and Russian speakers in a speeded color discrimination task using blue stimuli that spanned the siniy/goluboy border. We found that Russian speakers were faster to discriminate two colors when they fell into different linguistic categories in Russian (one siniy and the other goluboy) than when they were from the same linguistic category (both siniy or both goluboy). Moreover, this category advantage was eliminated by a verbal, but not a spatial, dual task. These effects were stronger for difficult discriminations (i.e., when the colors were perceptually close) than for easy discriminations (i.e., when the colors were further apart). English speakers tested on the identical stimuli did not show a category advantage in any of the conditions. These results demonstrate that (i) categories in language affect performance on simple perceptual color tasks and (ii) the effect of language is online (and can be disrupted by verbal interference).

Synesthetic colors determined by having colored refrigerator magnets in childhood.

Synesthesia is a condition in which percepts in one modality reliably elicit secondary perceptions in the same or a different modality that are not in the stimulus. In a common manifestation, synesthetes see colors in response to spoken or written letters, words and numbers. In this paper we demonstrate that the particular colors seen by a grapheme-color synesthete AED were learned from a set of refrigerator magnets and that the synesthesia later transferred to Cyrillic in a systematic way, with the colors induced by the Cyrillic letters determined by their visual or phonetic similarity to English letters. Closer examination of the data reveals that letters of either language that are more visually similar to the English capitals in the magnet set are also more saturated. In order to differentiate AED's synesthesia from ordinary memory, we use a novel psychophysical method to show that AED's synesthetic colors are subject to ordinary lightness constancy mechanisms. This suggests that the level of representation at which her synesthesia arises is early in the stream of visual processing.