Representation Of Stimuli Research Articles

The influence of visual experience and cognitive goals on the spatial representations of nociceptive stimuli.

Localizing pain is crucial because it allows for detecting which part of the body is being hurt and identifying in its surrounding which stimulus is producing the damage. Nociceptive inputs should therefore be mapped according to somatotopic ("which limb is stimulated?") and spatiotopic representations ("where is the stimulated limb?"). Because the body posture constantly changes, the brain has to realign the different spatial representations, for instance when the arms are crossed with the left hand in the right space and vice versa, to adequately guide actions towards the threatening object. Such ability is thought to be dependent on past sensory experience and contextual factors. We compared performances of early blind and normally sighted participants during temporal order judgement tasks. Two nociceptive stimuli were applied, one on each hand, with the hands either uncrossed or crossed. Participants reported which stimulus they perceived as first presented, according to either its location on the body or the position of the stimulated hand, respectively, prioritizing anatomy or external space as task-relevant reference frame. Relative to the uncrossed posture, sighted participants' performances were decreased when the hands were crossed, whatever the instruction be. Early blind participants' performances were affected by crossing the hands during spatial instruction, but not during anatomical instruction. These results indicate that nociceptive stimuli are automatically coded according to both somatotopic and spatiotopic representations, but the integration of the different spatial reference frames depends on early visual experience and ongoing cognitive goals, illustrating the plasticity and the flexibility of the nociceptive system.

Aberrant reward prediction error during Pavlovian appetitive learning in alexithymia.

Extensive literature shows that alexithymia, a subclinical trait defined by difficulties in identifying and describing feelings, is characterized by multifaceted impairments in processing emotional stimuli. Nevertheless, its underlying mechanisms remain elusive. Here, we hypothesize that alexithymia may be characterized by an alteration in learning the emotional value of encountered stimuli and test this by assessing differences between individuals with low (LA) and high (HA) levels of alexithymia in the computation of reward prediction errors (RPEs) during Pavlovian appetitive conditioning. As a marker of RPE, the amplitude of the feedback-related negativity (FRN) event-related potential was assessed while participants were presented with two conditioned stimuli (CS) associated with expected or unexpected feedback, indicating delivery of reward or no-reward. No-reward (vs reward) feedback elicited the FRN both in LA and HA. However, unexpected (vs expected) feedback enhanced the FRN in LA but not in HA, indicating impaired computation of RPE in HA. Thus, although HA show preserved sensitivity to rewards, they cannot use this response to update the value of CS that predict them. This impairment may hinder the construction of internal representations of emotional stimuli, leaving individuals with alexithymia unable to effectively recognize, respond and regulate their response to emotional stimuli.

Transfer learning of deep neural network representations for fMRI decoding

BackgroundDeep neural networks have revolutionised machine learning, with unparalleled performance in object classification. However, in brain imaging (e.g., fMRI), the direct application of Convolutional Neural Networks (CNN) to decoding subject states or perception from imaging data seems impractical given the scarcity of available data. New methodIn this work we propose a robust method to transfer information from deep learning (DL) features to brain fMRI data with the goal of decoding. By adopting Reduced Rank Regression with Ridge Regularisation we establish a multivariate link between imaging data and the fully connected layer (fc7) of a CNN. We exploit the reconstructed fc7 features by performing an object image classification task on two datasets: one of the largest fMRI databases, taken from different scanners from more than two hundred subjects watching different movie clips, and another with fMRI data taken while watching static images. ResultsThe fc7 features could be significantly reconstructed from the imaging data, and led to significant decoding performance. Comparison with existing methodsThe decoding based on reconstructed fc7 outperformed the decoding based on imaging data alone. ConclusionIn this work we show how to improve fMRI-based decoding benefiting from the mapping between functional data and CNN features. The potential advantage of the proposed method is twofold: the extraction of stimuli representations by means of an automatic procedure (unsupervised) and the embedding of high-dimensional neuroimaging data onto a space designed for visual object discrimination, leading to a more manageable space from dimensionality point of view.

Diversity of Ocular Dominance Patterns in Visual Cortex Originates from Variations in Local Cortical Retinotopy.

The primary visual cortex contains a detailed map of retinal stimulus position (retinotopic map) and eye input (ocular dominance map) that results from the precise arrangement of thalamic afferents during cortical development. For reasons that remain unclear, the patterns of ocular dominance are very diverse across species and can take the shape of highly organized stripes, convoluted beads, or no pattern at all. Here, we use a new image-processing algorithm to measure ocular dominance patterns more accurately than in the past. We use these measurements to demonstrate that ocular dominance maps follow a common organizing principle that makes the cortical axis with the slowest retinotopic gradient orthogonal to the ocular dominance stripes. We demonstrate this relation in multiple regions of the primary visual cortex from individual animals, and different species. Moreover, consistent with the increase in the retinotopic gradient with visual eccentricity, we demonstrate a strong correlation between eccentricity and ocular dominance stripe width. We also show that an eye/polarity grid emerges within the visual cortical map when the representation of light and dark stimuli segregates along an axis orthogonal to the ocular dominance stripes, as recently demonstrated in cats. Based on these results, we propose a developmental model of visual cortical topography that sorts thalamic afferents by eye input and stimulus polarity, and then maximizes the binocular retinotopic match needed for depth perception and the light-dark retinotopic mismatch needed to process stimulus orientation. In this model, the different ocular dominance patterns simply emerge from differences in local retinotopic cortical topography.SIGNIFICANCE STATEMENT Thalamocortical afferents segregate in primary visual cortex by eye input and light-dark polarity. This afferent segregation forms cortical patterns that vary greatly across species for reasons that remain unknown. Here we show that the formation of ocular dominance patterns follows a common organizing principle across species that aligns the cortical axis of ocular dominance segregation with the axis of slowest retinotopic gradient. Based on our results, we propose a model of visual cortical topography that sorts thalamic afferents by eye input and stimulus polarity along orthogonal axes with the slowest and fastest retinotopic gradients, respectively. This organization maximizes the binocular retinotopic match needed for depth perception and the light-dark retinotopic mismatch needed to process stimulus orientation in carnivores and primates.

Population adaptation in efficient balanced networks.

Adaptation is a key component of efficient coding in sensory neurons. However, it remains unclear how neurons can provide a stable representation of external stimuli given their history-dependent responses. Here we show that a stable representation is maintained if efficiency is optimized by a population of neurons rather than by neurons individually. We show that spike-frequency adaptation and E/I balanced recurrent connectivity emerge as solutions to a global cost-accuracy tradeoff. The network will redistribute sensory responses from highly excitable neurons to less excitable neurons as the cost of neural activity increases. This does not change the representation at the population level despite causing dynamic changes in individual neurons. By applying this framework to an orientation coding network, we reconcile neural and behavioral findings. Our approach underscores the common mechanisms behind the diversity of neural adaptation and its role in producing a reliable representation of the stimulus while minimizing metabolic cost.

Activity in human visual areas reflects the precision of motion perception

Any neural representation of a visual stimulus is necessarily uncertain, due to sensory noise and ambiguity in the inputs. Recent advances in fMRI decoding provide a principled approach for estimating the amount of uncertainty in cortical stimulus representations (van Bergen, Ma, Pratte & Jehee, 2015, Nature Neuroscience). However, these previous findings were limited to orientation perception. We here demonstrate that a similar decoding approach can be used to characterize the degree of uncertainty in cortical representations of motion. Participants viewed stimuli consisting of dots that moved coherently into a random direction, while their brain activity was measured with fMRI. Shortly after the dots disappeared from the screen, observers reported the direction of motion. Using a probabilistic analysis approach, we decoded the posterior probability distribution of motion direction from activity in visual areas V1–V4, and hMT+. We found that the decoded posterior distributions were generally bimodal, with two distinct peaks separated by roughly 180 degrees. One peak was reliably larger than the other, and centered on the true direction of stimulus motion. This bimodality suggests that the decoded distributions reflected not only motion, but also orientation information in the patterns of cortical activity. To assess the degree to which the decoded distributions reflected perceptual uncertainty, we computed the entropy of the decoded distributions. We compared this measure of uncertainty with behavioral variability, reasoning that a more precise representation in cortex should result in less variable (more precise) behavior. We found that uncertainty decoded from visual cortex was linked to participant behavior. Specifically, the entropy of the decoded distributions reliably predicted the variability in the observers’ estimates of motion direction. This suggests that the precision of motion perception can be reliably extracted from activity in human visual cortex.

Characterizing the influence of spatial attention on stimulus-evoked cortical representations

Past work suggests that covert attention shifts spatial receptive fields (RFs) towards attended locations, increasing the neuronal resources devoted to representing the attended location (Anton-Erxleben & Carrasco, 2013). If such shifts of spatial RFs occur on a large scale, the size of the cortical representation of visual stimuli should expand because attended stimuli will fall within the RFs of a broader range of neurons. Past work with fMRI, however, has found increases in the amplitude of the stimulus representations, but no substantial change in their size (Sprague & Serences, 2013; Võ et al., 2017), a finding that is hard to reconcile with the hypothesis that attention shifts spatial RFs towards attended locations. Two factors motivate further examination of this question. First, prior studies have shown that increases in BOLD activity at attended locations are additive (i.e., independent) of stimulus contrast, suggesting that this measure may not tap into modulations of stimulus-evoked responses (Murray, 2008). Second, direct comparisons of fMRI and EEG activity have revealed qualitatively distinct modulations by attention (Itthipuripat et al., 2018). Thus, we re-examined this question with a focus on stimulus-evoked EEG activity. We measured the response evoked by attended and unattended stimuli. Using an IEM, we reconstructed spatial channel-tuning functions (CTFs) from the broadband EEG response evoked by the stimuli. This analysis revealed that both the amplitude and the size of the stimulus-evoked CTF was larger for attended than for unattended stimuli. The change in the size of the spatial CTFs cannot be explained by sensory gain alone, which can only change the amplitude of CTFs. Thus, our results suggest that covert spatial attention shifts RFs towards the attended location, expanding the cortical representation evoked by stimuli in that location.

Simultaneous multi-area recordings suggest that attention improves performance by reshaping stimulus representations.

Visual attention dramatically improves subjects’ ability to see and also modulates the responses of neurons in every known visual and oculomotor area, but whether those modulations can account for perceptual improvements remains unclear. We measured the relationship between populations of visual neurons, oculomotor neurons, and behavior during detection and discrimination tasks. We found that neither of the two prominent hypothesized neuronal mechanisms underlying attention (which concern changes in information coding and the way sensory information is read out) provide a satisfying account of the observed behavioral improvements. Instead, our results are more consistent with the novel hypothesis that attention reshapes the representation of attended stimuli to more effectively influence behavior. Our results suggest a path toward understanding the neural underpinnings of perception and cognition in health and disease by analyzing neuronal responses in ways that are constrained by behavior and interactions between brain areas.

Experience enhances the representations of salient stimuli in the dentate gyrus

Experience enhances the representations of salient stimuli in the dentate gyrus

Why Does George Clooney Make Coffee Sexy? The Case for Attribute Conditioning

When a celebrity (e.g., George Clooney) endorses a brand (e.g., a coffee type), people’s assessment of this brand typically changes. We suggest that the mere repeated pairing of celebrities with brands imbues brands with the celebrities’ attributes. We call this effect attribute conditioning, which is, more generally, the phenomenon that people assess a stimulus’s attributes differently as a results of its pairing with another stimulus possessing that attribute. We review evidence showing that this effect goes beyond evaluative-conditioning effects, that it is not a demand effect, and that it is easily shown with many attributes (e.g., sexy, athletic, healthy) and many different stimuli (e.g., faces, shapes, brand logos). In addition, we review process evidence supporting the hypothesis that the effect is based on a memory structure that links the mental representations of the paired stimuli. We conclude with a brief outline of possible applied (e.g., marketing) and theoretical avenues for further research.

Laminar specificity of oscillatory coherence in the auditory cortex.

Empirical evidence suggests that, in the auditory cortex (AC), the phase relationship between spikes and local-field potentials (LFPs) plays an important role in the processing of auditory stimuli. Nevertheless, unlike the case of other sensory systems, it remains largely unexplored in the auditory modality whether the properties of the cortical columnar microcircuit shape the dynamics of spike-LFP coherence in a layer-specific manner. In this study, we directly tackle this issue by addressing whether spike-LFP and LFP-stimulus phase synchronization are spatially distributed in the AC during sensory processing, by performing laminar recordings in the cortex of awake short-tailed bats (Carollia perspicillata) while animals listened to conspecific distress vocalizations. We show that, in the AC, spike-LFP and LFP-stimulus synchrony depend significantly on cortical depth, and that sensory stimulation alters the spatial and spectral patterns of spike-LFP phase-locking. We argue that such laminar distribution of coherence could have functional implications for the representation of naturalistic auditory stimuli at a cortical level.

The intrinsic attractor manifold and population dynamics of a canonical cognitive circuit across waking and sleep.

Neural circuits construct distributed representations of key variables-external stimuli or internal constructs of quantities relevant for survival, such as an estimate of one's location in the world-as vectors of population activity. Although population activity vectors may have thousands of entries (dimensions), we consider that they trace out a low-dimensional manifold whose dimension and topology match the represented variable. This manifold perspective enables blind discovery and decoding of the represented variable using only neural population activity (without knowledge of the input, output, behavior or topography). We characterize and directly visualize manifold structure in the mammalian head direction circuit, revealing that the states form a topologically nontrivial one-dimensional ring. The ring exhibits isometry and is invariant across waking and rapid eye movement sleep. This result directly demonstrates that there are continuous attractor dynamics and enables powerful inference about mechanism. Finally, external rather than internal noise limits memory fidelity, and the manifold approach reveals new dynamical trajectories during sleep.

Ventral midbrain stimulation induces perceptual learning and cortical plasticity in primates

Practice improves perception and enhances neural representations of trained visual stimuli, a phenomenon known as visual perceptual learning (VPL). While attention to task-relevant stimuli plays an important role in such learning, Pavlovian stimulus-reinforcer associations are sufficient to drive VPL, even subconsciously. It has been proposed that reinforcement facilitates perceptual learning through the activation of neuromodulatory centers, but this has not been directly confirmed in primates. Here, we paired task-irrelevant visual stimuli with microstimulation of a dopaminergic center, the ventral tegmental area (VTA), in macaques. Pairing VTA microstimulation with a task-irrelevant visual stimulus increased fMRI activity and improved classification of fMRI activity patterns selectively for the microstimulation-paired stimulus. Moreover, pairing VTA microstimulation with a task-irrelevant visual stimulus improved the subject’s capacity to discriminate that stimulus. This is the first causal demonstration of the role of neuromodulatory centers in VPL in primates.

No effects of attention or visual perceptual load on cochlear function, as measured with stimulus-frequency otoacoustic emissions.

The effects of selectively attending to a target stimulus in a background containing distractors can be observed in cortical representations of sound as an attenuation of the representation of distractor stimuli. The locus in the auditory system at which attentional modulations first arise is unknown, but anatomical evidence suggests that cortically driven modulation of neural activity could extend as peripherally as the cochlea itself. Previous studies of selective attention have used otoacoustic emissions to probe cochlear function under varying conditions of attention with mixed results. In the current study, two experiments combined visual and auditory tasks to maximize sustained attention, perceptual load, and cochlear dynamic range in an attempt to improve the likelihood of observing selective attention effects on cochlear responses. Across a total of 45 listeners in the two experiments, no systematic effects of attention or perceptual load were observed on stimulus-frequency otoacoustic emissions. The results revealed significant between-subject variability in the otoacoustic-emission measure of cochlear function that does not depend on listener performance in the behavioral tasks and is not related to movement-generated noise. The findings suggest that attentional modulation of auditory information in humans arises at stages of processing beyond the cochlea.

Neural evidence for age-related differences in representational quality and strategic retrieval processes

Mounting behavioral evidence suggests that declines in both representational quality and controlled retrieval processes contribute to episodic memory decline with age. The present study sought neural evidence for age-related change in these factors by measuring neural differentiation during encoding of paired associates and changes in regional blood oxygenation level–dependent activity and functional connectivity during retrieval conditions that placed low (intact pairs) and high (recombined pairs) demands on controlled retrieval processes. Pattern similarity analysis revealed age-related declines in the differentiation of stimulus representations at encoding, manifesting as both reduced pattern similarity between closely related events and increased pattern similarity between distinct events. During retrieval, both groups increased recruitment of areas within the core recollection network when endorsing studied pairs, including the hippocampus and angular gyrus. In contrast, only younger adults increased recruitment of, and hippocampal connectivity with, lateral prefrontal regions during correct rejections of recombined pairs. These results provide evidence for age-related changes in representational quality and in the neural mechanisms supporting memory retrieval under conditions of high, but not low, control demand.

Occipitotemporal representations reflect individual differences in conceptual knowledge.

Through selective attention, decision-makers can learn to ignore behaviorally irrelevant stimulus dimensions. This can improve learning and increase the perceptual discriminability of relevant stimulus information. Across cognitive models of categorization, this is typically accomplished through the inclusion of attentional parameters, which provide information about the importance assigned to each stimulus dimension by each participant. The effect of these parameters on psychological representation is often described geometrically, such that perceptual differences over relevant psychological dimensions are accentuated (or stretched), and differences over irrelevant dimensions are down-weighted (or compressed). In sensory and association cortex, representations of stimulus features are known to covary with their behavioral relevance. Although this implies that neural representational space might closely resemble that hypothesized by formal categorization theory, to date, attentional effects in the brain have been demonstrated through powerful experimental manipulations (e.g., contrasts between relevant and irrelevant features). This approach sidesteps the role of idiosyncratic conceptual knowledge in guiding attention to useful information sources. To bridge this divide, we used formal categorization models, which were fit to behavioral data, to make inferences about the concepts and strategies used by individual participants during decision-making. We found that when greater attentional weight was devoted to a particular visual feature (e.g., “color”), its value (e.g., “red”) was more accurately decoded from occipitotemporal cortex. We also found that this effect was sufficiently sensitive to reflect individual differences in conceptual knowledge, indicating that occipitotemporal stimulus representations are embedded within a space closely resembling that formalized by classic categorization theory.

A Critique of Olfactory Objects.

Does the sense of smell involve the perception of odor objects? General discussion of perceptual objecthood centers on three criteria: stimulus representation, perceptual constancy, and figure-ground segregation. These criteria, derived from theories of vision, have been applied to olfaction in recent philosophical debates about psychology. An inherent problem with such framing of olfactory objecthood is that philosophers explicitly ignore the constitutive factors of the sensory systems that underpin the implementation of these criteria. The biological basis of odor coding is fundamentally different from the coding principles of the visual system. This article analyzes the three measures of perceptual objecthood against the biological background of the olfactory system. It contrasts the coding principles in olfaction with the visual system to show why these criteria of objecthood fail to be instantiated in odor perception. The argument demonstrates that olfaction affords perceptual categorization without the need to form odor objects.

Search for the Missing Dimensions: Building a Feature-Space Representation for a Natural-Science Category Domain

An important goal in cognitive and mathematical psychology is to scale up the application of computational models of human classification learning to real-world, naturalistic domains. Application of the models, however, requires the derivation of the complex, multidimensional “feature spaces” in which the to-be-classified objects are embedded and to which the formal models make reference. In recent work, using rock classification in the geologic sciences as an example target domain, we used multidimensional scaling (MDS) of similarity-judgment data as an approach to deriving the feature space (Nosofsky et al., Behavior Research Methods 50:530–556, 2018c). However, subsequent work involving the modeling of independent sets of classification-learning data led us to the hypothesis that the MDS solution had many “missing dimensions” that were crucial to categorization performance (Nosofsky et al., Psychonomic Bulletin & Review 26:48–76, 2019). In the present work, we conduct a “search for the missing dimensions” in an effort to develop a more comprehensive feature-space representation for the rock stimuli. By supplementing the original MDS solution with the missing dimensions, we achieve dramatically improved accounts of varied sets of classification-learning data in this domain. We outline future steps for continuing and expanding the work to meet the goal of achieving meaningful computational modeling of human classification in naturalistic object domains.

Evoked Response Strength in Primary Auditory Cortex Predicts Performance in a Spectro-Spatial Discrimination Task in Rats.

The extent to which the primary auditory cortex (A1) participates in instructing animal behavior remains debated. Although multiple studies have shown A1 activity to correlate with animals' perceptual judgments (Jaramillo and Zador, 2011; Bizley et al., 2013; Rodgers and DeWeese, 2014), others have found no relationship between A1 responses and reported auditory percepts (Lemus et al., 2009; Dong et al., 2011). To address this ambiguity, we performed chronic recordings of evoked local field potentials (eLFPs) in A1 of head-fixed female rats performing a two-alternative forced-choice auditory discrimination task. Rats were presented with two interleaved sequences of pure tones from opposite sides and had to indicate the side from which the higher-frequency target stimulus was played. Animal performance closely correlated (rrm = 0.68) with the difference between the target and distractor eLFP responses: the more the target response exceeded the distractor response, the better the animals were at identifying the side of the target frequency. Reducing the evoked response of either frequency through stimulus-specific adaptation affected performance in the expected way: target localization accuracy was degraded when the target frequency was adapted and improved when the distractor frequency was adapted. Target frequency eLFPs were stronger on hit trials than on error trials. Our results suggest that the degree to which one stimulus stands out over others within A1 activity may determine its perceptual saliency for the animals and accordingly bias their behavioral choices.SIGNIFICANCE STATEMENT The brain must continuously calibrate the saliency of sensory percepts against their relevance to the current behavioral goal. The inability to ignore irrelevant distractors characterizes a spectrum of human attentional disorders. Meanwhile, the connection between the neural underpinnings of stimulus saliency and sensory decisions remains elusive. Here, we record local field potentials in the primary auditory cortex of rats engaged in auditory discrimination to investigate how the cortical representation of target and distractor stimuli impacts behavior. We find that the amplitude difference between target- and distractor-evoked activity predicts discrimination performance (rrm = 0.68). Specific adaptation of target or distractor shifts performance either below or above chance, respectively. It appears that recent auditory history profoundly influences stimulus saliency, biasing animals toward diametrically-opposed decisions.

Permanent damage or temporary silencing of retrosplenial cortex impairs the expression of a negative patterning discrimination.

The retrosplenial cortex (RSC) is positioned at the interface between cortical sensory regions and the hippocampal/parahippocampal memory system. As such, it has been theorized that RSC may have a fundamental role in linking sensory stimuli together in the service of forming complex representations. To test this, three experiments were carried out to determine the effects of RSC damage or temporary inactivation on learning or performing a negative patterning discrimination. In this procedure, two conditioned stimuli are reinforced when they are presented individually (i.e., stimulus elements) but are non-reinforced when they are presented simultaneously as a compound stimulus. Normal rats successfully discriminate between the two types of trials as evidenced by more responding to the elements compared to the compound stimulus. This is thought to reflect the formation of a configural representation of the compound stimulus; that is, the two cues are linked together in such a fashion that the compound stimulus is a wholly different, unique stimulus. Permanent lesions of RSC made prior to training (Experiment 1) had no effect on learning the discrimination. However, lesions (Experiment 2) or temporary chemogenetic inactivation (Experiment 3) of RSC made after training impaired subsequent performance of the discrimination. We argue that this pattern of results indicates that RSC may normally be involved in forming the configural representations manifested in negative patterning, but that absent the RSC, other brain systems or structures can compensate sufficiently to result in normal behavior.