Representation Of Stimuli Research Articles

Task phase-specific involvement of the rat posterior parietal cortex in performance of the TUNL task.

The posterior parietal cortex (PPC) participates in cognitive processes including working memory (WM), sensory evidence accumulation, and perceptually guided decision making. However, surprisingly little work has used temporally precise manipulations to dissect its role in different epochs of behavior taking place over short timespans, such as WM tasks. As a result, a consistent view of the temporally precise role of the PPC in these processes has not been described. In the present study, we investigated the temporally specific role of the PPC in the Trial-Unique, Nonmatching-to-Location (TUNL) task, a touchscreen-based, visuospatial WM task that relies on the PPC. To disrupt PPC activity in a temporally precise manner, we applied mild intracranial electrical stimulation (ICES). We found that intra-PPC ICES (100 μA) significantly impaired accuracy in TUNL without significantly altering response latency. Moreover, we found that the impairment was specific to ICES applied during the delay and test phases of TUNL. Consistent with previous reports showing delay- and choice-specific neuronal activity in the PPC, the results provide evidence that the rat PPC is required for maintaining memory representations of stimuli over a delay period as well as for making successful comparisons and choices between test stimuli. In contrast, the PPC appears not to be critical for initial encoding of sample stimuli. This pattern of results may indicate that early encoding of visual stimuli is independent of the PPC or that the PPC becomes engaged only when visual stimuli are spatially complex or involve memory or decision making.

Neural representations of perceptual color experience in the human ventral visual pathway

Color is a perceptual construct that arises from neural processing in hierarchically organized cortical visual areas. Previous research, however, often failed to distinguish between neural responses driven by stimulus chromaticity versus perceptual color experience. An unsolved question is whether the neural responses at each stage of cortical processing represent a physical stimulus or a color we see. The present study dissociated the perceptual domain of color experience from the physical domain of chromatic stimulation at each stage of cortical processing by using a switch rivalry paradigm that caused the color percept to vary over time without changing the retinal stimulation. Using functional MRI (fMRI) and a model-based encoding approach, we found that neural representations in higher visual areas, such as V4 and VO1, corresponded to the perceived color, whereas responses in early visual areas V1 and V2 were modulated by the chromatic light stimulus rather than color perception. Our findings support a transition in the ascending human ventral visual pathway, from a representation of the chromatic stimulus at the retina in early visual areas to responses that correspond to perceptually experienced colors in higher visual areas.

Stimulus-choice (mis)alignment in primate area MT.

For stimuli near perceptual threshold, the trial-by-trial activity of single neurons in many sensory areas is correlated with the animal's perceptual report. This phenomenon has often been attributed to feedforward readout of the neural activity by the downstream decision-making circuits. The interpretation of choice-correlated activity is quite ambiguous, but its meaning can be better understood in the light of population-wide correlations among sensory neurons. Using a statistical nonlinear dimensionality reduction technique on single-trial ensemble recordings from the middle temporal (MT) area during perceptual-decision-making, we extracted low-dimensional latent factors that captured the population-wide fluctuations. We dissected the particular contributions of sensory-driven versus choice-correlated activity in the low-dimensional population code. We found that the latent factors strongly encoded the direction of the stimulus in single dimension with a temporal signature similar to that of single MT neurons. If the downstream circuit were optimally utilizing this information, choice-correlated signals should be aligned with this stimulus encoding dimension. Surprisingly, we found that a large component of the choice information resides in the subspace orthogonal to the stimulus representation inconsistent with the optimal readout view. This misaligned choice information allows the feedforward sensory information to coexist with the decision-making process. The time course of these signals suggest that this misaligned contribution likely is feedback from the downstream areas. We hypothesize that this non-corrupting choice-correlated feedback might be related to learning or reinforcing sensory-motor relations in the sensory population.

Dissecting EXIT

Kruschke’s EXIT model (Kruschke, 2001b) has been very successful in explaining a variety of learning phenomena by means of selective attention. In particular, EXIT produces learned predictiveness effects (Le Pelley and McLaren, 2003), the inverse base rate effect (Kruschke, 1996; Medin and Edelson, 1988), inattention after blocking (Beesley and Le Pelley, 2011; Kruschke and Blair, 2000), differential cue use across the stimulus space (Aha and Goldstone, 1992) and conditional learned predictiveness effects (Uengoer et al., 2013). We dissect EXIT into its component mechanisms (error-driven learning, selective attention, attentional competition, rapid attention shifts and exemplar mediation of attention) and test whether simplified versions of EXIT can explain the same experimental results as the full model. Most phenomena can be explained by either rapid attention shifts or attentional competition, without the need for combining them as in EXIT. There is little evidence for exemplar mediation of attention when people learn linearly separable category structures (e.g. Kruschke and Blair, 2000; Le Pelley and McLaren, 2003); whether or not it is needed for non-linear categories depends on stimulus representation (Aha and Goldstone, 1992; Uengoer et al., 2013). On the whole, we believe that attentional competition—embodied in a model which we dub CompAct—offers the simplest explanation for the experimental results we examine.

Color ensembles: Sampling and averaging spatial hue distributions

Color serves both to segment a scene into objects and background and to identify objects. Although objects and surfaces usually contain multiple colors, humans can readily extract a representative color description, for instance, that tomatoes are red and bananas yellow. The study of color discrimination and identification has a long history, yet we know little about the formation of summary representations of multicolored stimuli. Here, we characterize the human ability to integrate hue information over space for simple color stimuli varying in the amount of information, stimulus size, and spatial configuration of stimulus elements. We show that humans are efficient at integrating hue information over space beyond what has been shown before for color stimuli. Integration depends only on the amount of information in the display and not on spatial factors such as element size or spatial configuration in the range measured. Finally, we find that observers spontaneously prefer a simple averaging strategy even with skewed color distributions. These results shed light on how human observers form summary representations of color and make a link between the perception of polychromatic surfaces and the broader literature of ensemble perception.

Multi-spectral oscillatory dynamics serving directed and divided attention

Attention-related amplification of neural representations of external stimuli has been well documented in the visual domain, however, research concerning the oscillatory dynamics of such directed attention is relatively sparse in humans. Specifically, it is unknown which spectrally-specific neural responses are mainly impacted by the direction and division of attention, as well as whether the effects of attention on these oscillations are spatially disparate. In this study, we use magnetoencephalography and a visual-somatosensory oddball task to investigate the whole-brain oscillatory dynamics of directed (Experiment 1; N ​= ​26) and divided (Experiment 2; N ​= ​34) visual attention. Sensor-level data were transformed into the time-frequency domain and significant responses from baseline were imaged using a frequency-resolved beamformer. We found that multi-spectral cortical oscillations were stronger when attention was sustained in the visual space and that these effects exhibited informative spatial distributions that differed by frequency. More specifically, we found stronger frontal theta (4–8 ​Hz), frontal and occipital alpha (8–14 ​Hz), occipital beta (16–22 ​Hz), and frontal gamma (74–84 ​Hz) responses when visual attention was sustained than when it was directed away from the visual domain. Similarly, in the divided attention condition, we observed stronger fronto-parietal theta activity and temporo-parietal alpha and beta oscillations when visual attention was sustained toward the visual stimuli than divided between the visual and somatosensory domains. Investigating how attentional gain is implemented in the human brain is essential for better understanding how this process is degraded in disease, and may provide useful targets for future therapies.

Decoding Stimulus-Response Representations and Their Stability Using EEG-Based Multivariate Pattern Analysis.

Goal-directed actions require proper associations between stimuli and response. This has been delineated by cognitive theory, for example, in the theory of event coding framework, which proposes that event files represent such bindings. Yet, how such event file representations are coded on a neurophysiological level is unknown. We close this gap combining temporal electroencephalography (EEG) signal decomposition methods and multivariate pattern analysis (MVPA). We show that undecomposed neurophysiological data is unsuitable to decode event file representations because different aspects of information coded in the neurophysiological signal reveal distinct and partly opposed dynamics in the representational content. This is confirmed by applying MVPA to temporal decomposed EEG data. After intermixed aspects of information in the EEG during response selection have been separated, a reliable examination of the event file’s representational content and its temporal stability was possible. We show that representations of stimulus–response bindings are activated and decay in a gradual manner and that event file representations resemble distributed neural activity. Especially representations of stimulus–response bindings, as well as stimulus-related representations, are coded and reveal temporal stability. Purely motor-related representations are not found in neurophysiological signals during event coding.

Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG.

Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-associated stimulus representations undergo plasticity in sensory cortex, thereby automatically capturing attention during early processing. To test this, we used magnetoencephalography to probe whether stimulus location and identity representations in sensory cortex are modulated by reward learning. We furthermore investigated the time course of these neural effects, and their relationship to behavioral VDAC. Male and female human participants first learned stimulus–reward associations. Next, we measured VDAC in a separate task by presenting these stimuli in the absence of reward contingency and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in posterior visual and parietal cortex from ∼260 ms after stimulus onset. This value modulation was related to the strength of participants' behavioral VDAC effect and persisted into subsequent target processing. Importantly, learned value did not influence cortical signatures of early processing (i.e., earlier than ∼200 ms); nor did it influence the decodability of stimulus identity. Our results suggest that VDAC is underpinned by learned value signals that modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual processing in cortex.SIGNIFICANCE STATEMENT Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus–reward associations, a phenomenon termed “value-driven attentional capture” (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity, which modulates early visual processing to capture attention. Although we find that learned value modulates spatial signals in visual cortical areas, an effect that correlates with VDAC, we find no relevant signatures of changes in early visual processing in cortex.

Synaptic Connections of Aromatase Circuits in the Medial Amygdala Are Sex Specific.

The brains of male and female mice are shaped by genetics and hormones during development. The enzyme aromatase helps establish sex differences in social behaviors and in the neural circuits that produce these behaviors. The medial amygdala of mice contains a large population of aromatase neurons and is a critical hub in the social behavior network. Moreover, the neural representation of social stimuli in the medial amygdala displays clear sex differences that track developmental changes in social behaviors. Here, we identify a potential anatomic basis for those sex differences. We found that sensory input from the accessory olfactory bulb (AOB) to aromatase neurons is derived nearly exclusively from the anterior AOB, which selectively responds to chemosensory cues from conspecific animals. Through the coordinated use of mouse transgenics and viral-based circuit-tracing strategies, we demonstrate a clear sex difference in the volume of synapses connecting the accessory olfactory bulb to aromatase-expressing neurons in the medial amygdala of male versus female mice. This difference in anatomy likely mediates, at least in part, sex differences in medial amygdala-mediated social behaviors.

Emotion-behavior decoupling in individuals with schizophrenia, bipolar disorder, and major depressive disorder.

Failure in translating emotional salience into effortful behavior is thought to be a core feature of anhedonia and avolition in individuals with schizophrenia (SCZ), but little is known about emotion-behavior coupling in individuals with bipolar disorder (BD) and major depressive disorder (MDD). In this study, we compared emotion-behavior correspondence in participants with SCZ, BD, and MDD. Forty-two participants with SCZ, 44 participants with MDD, 43 participants with BD, and 43 healthy controls were recruited. A computerized anticipatory and consummatory pleasure task was used to evaluate emotion-behavior correspondence. Clinical ratings of negative symptoms and self-report anhedonia questionnaires were also administered. We found that participants with SCZ, MDD, and BD exhibited different levels of negative symptoms and self-reported anhedonia, as well as emotion-behavior decoupling. In SCZ participants, both desirable and undesirable images elicited lower correspondence between self-reported liking and behavior. In MDD and BD participants, undesirable images elicited lower emotion-behavior correspondence under both direct stimulus presentation and representation conditions, whereas deficits in emotion-behavior coupling under desirable conditions were only observed when stimuli were present. Taken together, emotion-behavior decoupling showed both common and unique patterns in participants with SCZ, MDD, and BD, and showed some associations with negative symptoms and anhedonia across the combined clinical sample. This finding may be helpful for early identification and the development of novel interventions for different psychiatric diagnoses. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Attention amplifies neural representations of changes in sensory input at the expense of perceptual accuracy

Attention enhances the neural representations of behaviorally relevant stimuli, typically by a push–pull increase of the neuronal response gain to attended vs. unattended stimuli. This selectively improves perception and consequently behavioral performance. However, to enhance the detectability of stimulus changes, attention might also distort neural representations, compromising accurate stimulus representation. We test this hypothesis by recording neural responses in the visual cortex of rhesus monkeys during a motion direction change detection task. We find that attention indeed amplifies the neural representation of direction changes, beyond a similar effect of adaptation. We further show that humans overestimate such direction changes, providing a perceptual correlate of our neurophysiological observations. Our results demonstrate that attention distorts the neural representations of abrupt sensory changes and consequently perceptual accuracy. This likely represents an evolutionary adaptive mechanism that allows sensory systems to flexibly forgo accurate representation of stimulus features to improve the encoding of stimulus change.

The Dentate Gyrus Classifies Cortical Representations of Learned Stimuli

Animals must discern important stimuli and place them onto their cognitive map of their environment. The neocortex conveys general representations of sensory events to the hippocampus, and the hippocampus is thought to classify and sharpen the distinctions between these events. We recorded populations of dentate gyrus granule cells (DG GCs) and lateral entorhinal cortex (LEC) neurons across days to understand how sensory representations are modified by experience. We found representations of odors in DG GCs that required synaptic input from the LEC. Odor classification accuracy in DG GCs correlated with future behavioral discrimination. In associative learning, DG GCs, more so than LEC neurons, changed their responses to odor stimuli, increasing the distance in neural representations between stimuli, responding more to the conditioned and less to the unconditioned odorant. Thus, with learning, DG GCs amplify the decodability of cortical representations of important stimuli, which may facilitate information storage to guide behavior.

Limitations to Estimating Mutual Information in Large Neural Populations.

Information theory provides a powerful framework to analyse the representation of sensory stimuli in neural population activity. However, estimating the quantities involved such as entropy and mutual information from finite samples is notoriously hard and any direct estimate is known to be heavily biased. This is especially true when considering large neural populations. We study a simple model of sensory processing and show through a combinatorial argument that, with high probability, for large neural populations any finite number of samples of neural activity in response to a set of stimuli is mutually distinct. As a consequence, the mutual information when estimated directly from empirical histograms will be equal to the stimulus entropy. Importantly, this is the case irrespective of the precise relation between stimulus and neural activity and corresponds to a maximal bias. This argument is general and applies to any application of information theory, where the state space is large and one relies on empirical histograms. Overall, this work highlights the need for alternative approaches for an information theoretic analysis when dealing with large neural populations.

Population coupling predicts the plasticity of stimulus responses in cortical circuits.

Some neurons have stimulus responses that are stable over days, whereas other neurons have highly plastic stimulus responses. Using a recurrent network model, we explore whether this could be due to an underlying diversity in their synaptic plasticity. We find that, in a network with diverse learning rates, neurons with fast rates are more coupled to population activity than neurons with slow rates. This plasticity-coupling link predicts that neurons with high population coupling exhibit more long-term stimulus response variability than neurons with low population coupling. We substantiate this prediction using recordings from the Allen Brain Observatory, finding that a neuron's population coupling is correlated with the plasticity of its orientation preference. Simulations of a simple perceptual learning task suggest a particular functional architecture: a stable 'backbone' of stimulus representation formed by neurons with low population coupling, on top of which lies a flexible substrate of neurons with high population coupling.

A VTA to Basal Amygdala Dopamine Projection Contributes to Signal Salient Somatosensory Events during Fear Learning.

The amygdala is a brain area critical for the formation of fear memories. However, the nature of the teaching signal(s) that drive plasticity in the amygdala are still under debate. Here, we use optogenetic methods to investigate the contribution of ventral tegmental area (VTA) dopamine neurons to auditory-cued fear learning in male mice. Using anterograde and retrograde labeling, we found that a sparse and relatively evenly distributed population of VTA neurons projects to the basal amygdala (BA). In vivo optrode recordings in behaving mice showed that many VTA neurons, among them putative dopamine neurons, are excited by footshocks, and acquire a response to auditory stimuli during fear learning. Combined cfos imaging and retrograde labeling in dopamine transporter (DAT) Cre mice revealed that a large majority of BA projectors (>95%) are dopamine neurons, and that BA projectors become activated by the tone-footshock pairing of fear learning protocols. Finally, silencing VTA dopamine neurons, or their axon terminals in the BA during the footshock, reduced the strength of fear memory as tested 1 d later, whereas silencing the VTA-central amygdala (CeA) projection had no effect. Thus, VTA dopamine neurons projecting to the BA contribute to fear memory formation, by coding for the saliency of the footshock event and by signaling such events to the basal amygdala.SIGNIFICANCE STATEMENT Powerful mechanisms of fear learning have evolved in animals and humans to enable survival. During fear conditioning, a sensory cue, such as a tone (the conditioned stimulus), comes to predict an innately aversive stimulus, such as a mild footshock (the unconditioned stimulus). A brain representation of the unconditioned stimulus must act as a teaching signal to instruct plasticity of the conditioned stimulus representation in fear-related brain areas. Here we show that dopamine neurons in the VTA that project to the basal amygdala contribute to such a teaching signal for plasticity, thereby facilitating the formation of fear memories. Knowledge about the role of dopamine in aversively motivated plasticity might allow further insights into maladaptive plasticities that underlie anxiety and post-traumatic stress disorders in humans.

Hey, look over there: Distraction effects on rapid sequence recall.

In the course of everyday life, the brain must store and recall a huge variety of representations of stimuli which are presented in an ordered or sequential way. The processes by which the ordering of these various things is stored and recalled are moderately well understood. We use here a computational model of a cortex-like recurrent neural network adapted by a multitude of plasticity mechanisms. We first demonstrate the learning of a sequence. Then, we examine the influence of different types of distractors on the network dynamics during the recall of the encoded ordered information being ordered in a sequence. We are able to broadly arrive at two distinct effect-categories for distractors, arrive at a basic understanding of why this is so, and predict what distractors will fall into each category.

Persistence of EEG Alpha Entrainment Depends on Stimulus Phase at Offset.

Neural entrainment is the synchronization of neural activity to the frequency of repetitive external stimuli, which can be observed as an increase in the electroencephalogram (EEG) power spectrum at the driving frequency, -also known as the steady-state response. Although it has been systematically reported that the entrained EEG oscillation persists for approximately three cycles after stimulus offset, the neural mechanisms underpinning it remain unknown. Focusing on alpha oscillations, we adopt the dynamical excitation/inhibition framework, which suggests that phases of entrained EEG signals correspond to alternating excitatory/inhibitory states of the neural circuitry. We hypothesize that the duration of the persistence of entrainment is determined by the specific functional state of the entrained neural network at the time the stimulus ends. Steady-state visually evoked potentials (SSVEP) were elicited in 19 healthy volunteers at the participants’ individual alpha peaks. Visual stimulation consisted of a sinusoidally-varying light terminating at one of four phases: 0, π/2, π, and 3π/2. The persistence duration of the oscillatory activity was analyzed as a function of the terminating phase of the stimulus. Phases of the SSVEP at the stimulus termination were distributed within a constant range of values relative to the phase of the stimulus. Longer persistence durations were obtained when visual stimulation terminated towards the troughs of the alpha oscillations, while shorter persistence durations occurred when stimuli terminated near the peaks. Source localization analysis suggests that the persistence of entrainment reflects the functioning of fronto-occipital neuronal circuits, which might prime the sensory representation of incoming visual stimuli based on predictions about stimulus rhythmicity. Consequently, different states of the network at the end of the stimulation, corresponding to different states of intrinsic neuronal coupling, may determine the time windows over which coding of incoming sensory stimulation is modulated by the preceding oscillatory activity.

Encoding, storage, and response preparation-Distinct EEG correlates of stimulus and action representations in working memory.

Working memory (WM) allows for the active storage of stimulus- and higher level representations, such as action plans. This electroencephalography (EEG) study investigated the specific electrophysiological correlates dissociating action-related from stimulus-related representations in WM using three different experimental conditions based on the same stimulus material. In the experiment, a random sequence of single numbers (from 1 to 6) was presented and participants had to indicate whether the current number (N0 condition), the preceding number (N-1 condition), or the sum of the current and the preceding number (S-1 condition) was odd or even. Accordingly, participants had to store a stimulus representation in S-1 and an action representation in N-1 until the onset of the next stimulus. In the EEG, the storage of stimulus representations (S-1) was reflected by a fronto-central slow wave indicating the rehearsal of information that was required for the response in the following trial. In contrast, the storage of action representations (N-1) went along with a posterior positive slow wave, suggesting that the action plan was actively stored in WM until the presentation of the next stimulus. Crucially, preparing for the next response in N-1 was associated with increased contralateral mu/beta suppression, predicting the response time in the given trial. Our findings, thus, show that the WM processes for stimulus- and action representations can be clearly dissociated from each other with a distinct sequence of EEG correlates for encoding, storage, and response preparation.

Visualization of a Distributed Synaptic Memory Code in the Drosophila Brain

During associative conditioning, animals learn which sensory cues are predictive for positive or negative conditions. Because sensory cues are encoded by distributed neurons, one has to monitor plasticity across many synapses to capture how learned information is encoded. We analyzed synaptic boutons of Kenyon cells of the Drosophila mushroom body γ lobe, a brain structure that mediates olfactory learning. A fluorescent Ca2+ sensor was expressed in single Kenyon cells so that axonal boutons could be assigned to distinct cells and Ca2+ could be measured across many animals. Learning induced directed synaptic plasticity in specific compartments along the axons. Moreover, we show that odor-evoked Ca2+ dynamics across boutons decorrelate as a result of associative learning. Information theory indicates that learning renders the stimulus representation more distinct compared with naive stimuli. These data reveal that synaptic boutons rather than cells act as individually modifiable units, and coherence among them is a memory-encoding parameter.

Reward Association Enhances Stimulus-Specific Representations in Primary Visual Cortex.

SummaryThe potential for neuronal representations of external stimuli to be modified by previous experience is critical for efficient sensory processing and improved behavioral outcomes. To investigate how repeated exposure to a visual stimulus affects its representation in mouse primary visual cortex (V1), we performed two-photon calcium imaging of layer 2/3 neurons and assessed responses before, during, and after the presentation of a repetitive stimulus over 5 consecutive days. We found a stimulus-specific enhancement of the neuronal representation of the repetitively presented stimulus when it was associated with a reward. This was observed both after mice actively learned a rewarded task and when the reward was randomly received. Stimulus-specific enhanced representation resulted both from neurons gaining selectivity and from increased response reliability in previously selective neurons. In the absence of reward, there was either no change in stimulus representation or a decreased representation when the stimulus was viewed at a fixed temporal frequency. Pairing a second stimulus with a reward led to a similar enhanced representation and increased discriminability between the equally rewarded stimuli. Single-neuron responses showed that separate subpopulations discriminated between the two rewarded stimuli depending on whether the stimuli were displayed in a virtual environment or viewed on a single screen. We suggest that reward-associated responses enable the generalization of enhanced stimulus representation across these V1 subpopulations. We propose that this dynamic regulation of visual processing based on the behavioral relevance of sensory input ultimately enhances and stabilizes the representation of task-relevant features while suppressing responses to non-relevant stimuli.