Stimulus History Research Articles

Mapping the effects of stimulus history on perception

Mapping the effects of stimulus history on perception

Phasic and sustained interactions of multisensory interplay and temporal expectation

Every moment organisms are confronted with complex streams of information which they use to generate a reliable mental model of the world. There is converging evidence for several optimization mechanisms instrumental in integrating (or segregating) incoming information; among them are multisensory interplay (MSI) and temporal expectation (TE). Both mechanisms can account for enhanced perceptual sensitivity and are well studied in isolation; how these two mechanisms interact is currently less well-known. Here, we tested in a series of four psychophysical experiments for TE effects in uni- and multisensory contexts with different levels of modality-related and spatial uncertainty. We found that TE enhanced perceptual sensitivity for the multisensory relative to the best unisensory condition (i.e. multisensory facilitation according to the max-criterion). In the latter TE effects even vanished if stimulus-related spatial uncertainty was increased. Accordingly, computational modelling indicated that TE, modality-related and spatial uncertainty predict multisensory facilitation. Finally, the analysis of stimulus history revealed that matching expectation at trial n-1 selectively improves multisensory performance irrespective of stimulus-related uncertainty. Together, our results indicate that benefits of multisensory stimulation are enhanced by TE especially in noisy environments, which allows for more robust information extraction to boost performance on both short and sustained time ranges.

A novel concept for dynamic adjustment of auditory space

Traditionally, the auditory system is thought to serve reliable sound localization. Stimulus-history driven feedback circuits in the early binaural pathway, however, contradict this canonical concept and raise questions about their functional significance. Here we show that stimulus-history dependent changes in absolute space perception are poorly captured by the traditional labeled-line and hemispheric-difference models of auditory space coding. We therefore developed a new decoding model incorporating recent electrophysiological findings in which sound location is initially computed in both brain hemispheres independently and combined to yield a hemispherically balanced code. This model closely captures the observed absolute localization errors caused by stimulus history, and furthermore predicts a selective dilation and compression of perceptional space. These model predictions are confirmed by improvement and degradation of spatial resolution in human listeners. Thus, dynamic perception of auditory space facilitates focal sound source segregation at the expense of absolute sound localization, questioning existing concepts of spatial hearing.

A Forward Genetic Screen in Zebrafish Identifies the G-Protein-Coupled Receptor CaSR as a Modulator of Sensorimotor Decision Making

Animals continuously integrate sensory information and select contextually appropriate responses. Here, we show that zebrafish larvae select a behavioral response to acoustic stimuli from a pre-existing choice repertoire in a context-dependent manner. We demonstrate that this sensorimotor choice is modulated by stimulus quality and history, as well as by neuromodulatory systems-all hallmarks of more complex decision making. Moreover, from a genetic screen coupled with whole-genome sequencing, we identified eight mutants with deficits in this sensorimotor choice, including mutants of the vertebrate-specific G-protein-coupled extracellular calcium-sensing receptor (CaSR), whose function in the nervous system is not well understood. We demonstrate that CaSR promotes sensorimotor decision making acutely through Gαi/o and Gαq/11 signaling, modulated by clathrin-mediated endocytosis. Combined, our results identify the first set of genes critical for behavioral choice modulation in a vertebrate and reveal an unexpected critical role for CaSR in sensorimotor decision making.

Adaptation to stimulus orientation in mouse primary visual cortex.

Information processing in the visual system is shaped by recent stimulus history, such that prolonged viewing of an adapting stimulus can alter the perception of subsequently presented test stimuli. In the tilt-after-effect, the perceived orientation of a grating is often repelled away from the orientation of a previously viewed adapting grating. A possible neural correlate for the tilt-after-effect has been described in cat and macaque primary visual cortex (V1), where adaptation produces repulsive shifts in the orientation tuning curves of V1 neurons. We investigated adaptation to stimulus orientation in mouse V1 to determine whether known species differences in orientation processing, notably V1 functional architecture and proportion of tightly tuned cells, are important for these repulsive shifts. Unlike the consistent repulsion reported in other species, we found that repulsion was only about twice as common as attraction in our mouse data. Furthermore, adapted responses were attenuated across all orientations. A simple model that captured key physiological findings reported in cats and mice indicated that the greater proportion of broadly tuned neurons in mice may explain the observed species differences in adaptation.

Neural Integration of Stimulus History Underlies Prediction for Naturalistically Evolving Sequences.

Forming valid predictions about the environment is crucial to survival. However, whether humans are able to form valid predictions about natural stimuli based on their temporal statistical regularities remains unknown. Here, we presented subjects with tone sequences with pitch fluctuations that, over time, capture long-range temporal dependence structures prevalent in natural stimuli. We found that subjects were able to exploit such naturalistic statistical regularities to make valid predictions about upcoming items in a sequence. Magnetoencephalography (MEG) recordings revealed that slow, arrhythmic cortical dynamics tracked the evolving pitch sequence over time such that neural activity at a given moment was influenced by the pitch of up to seven previous tones. Importantly, such history integration contained in neural activity predicted the expected pitch of the upcoming tone, providing a concrete computational mechanism for prediction. These results establish humans' ability to make valid predictions based on temporal regularities inherent in naturalistic stimuli and further reveal the neural mechanisms underlying such predictive computation.SIGNIFICANCE STATEMENT A fundamental question in neuroscience is how the brain predicts upcoming events in the environment. To date, this question has primarily been addressed in experiments using relatively simple stimulus sequences. Here, we studied predictive processing in the human brain using auditory tone sequences that exhibit temporal statistical regularities similar to those found in natural stimuli. We observed that humans are able to form valid predictions based on such complex temporal statistical regularities. We further show that neural response to a given tone in the sequence reflects integration over the preceding tone sequence and that this history dependence forms the foundation for prediction. These findings deepen our understanding of how humans form predictions in an ecologically valid environment.

Sequential dependencies in pitch judgments.

Studies that measure pitch discrimination relate a subject's response on each trial to the stimuli presented on that trial, but there is evidence that behavior depends also on earlier stimulation. Here, listeners heard a sequence of tones and reported after each tone whether it was higher or lower in pitch than the previous tone. Frequencies were determined by an adaptive staircase targeting 75% correct, with interleaved tracks to ensure independence between consecutive frequency changes. Responses for this specific task were predicted by a model that took into account the frequency interval on the current trial, as well as the interval and response on the previous trial. This model was superior to simpler models. The dependence on the previous interval was positive (assimilative) for all subjects, consistent with persistence of the sensory trace. The dependence on the previous response was either positive or negative, depending on the subject, consistent with a subject-specific suboptimal response strategy. It is argued that a full stimulus + response model is necessary to account for effects of stimulus history and obtain an accurate estimate of sensory noise.

Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation

Neuronal stimulus selectivity is shaped by feedforward and recurrent excitatory-inhibitory interactions. In the auditory cortex (AC), parvalbumin- (PV) andsomatostatin-positive (SOM) inhibitory interneurons differentially modulate frequency-dependent responses of excitatory neurons. Responsiveness of neurons in the AC to sound is also dependent on stimulus history. We found that the inhibitory effects of SOMs and PVs diverged as a function of adaptation to temporal repetition of tones. Prior to adaptation, suppressing either SOM or PV inhibition drove both increases and decreases in excitatory spiking activity. After adaptation, suppressing SOM activity caused predominantly disinhibitory effects, whereas suppressing PV activity still evoked bi-directional changes. SOM, but not PV-driven inhibition, dynamically modulated frequency tuning with adaptation. Unlike PV-driven inhibition, SOM-driven inhibition elicited gain-like increases in frequency tuning reflective of adaptation. Our findings suggest that distinct cortical interneurons differentially shape tuning to sensory stimuli across the neuronal receptive field, altering frequency selectivity of excitatory neurons during adaptation.

Choosing the right bar: a complex problem.

Inputs to the central complex, the navigation center of Drosophila, are strongly modulated by the visual stimulus history. These history effects carry forward to bias turning behavior when flies choose between two visual stimuli.

Adaptation of Thalamic Neurons Provides Information about the Spatiotemporal Context of Stimulus History.

Adaptation of neural responses due to the history of sensory input has been observed across all sensory modalities. However, the computational role of adaptation is not fully understood, especially when one considers neural coding problems in which adaptation increases the ambiguity of the neural responses to simple stimuli. To address this, we quantified the impact of adaptation on the information conveyed by thalamic neurons about paired whisker stimuli in male rat. At the single neuron level, although paired-pulse adaptation reduces the information about the present stimulus, the information per spike increases. Moreover, the adapted response can convey significant amounts of information about whether, when and where a previous stimulus occurred. At the population level, ambiguity of the adapted responses about the present stimulus can be compensated for by large numbers of neurons. Therefore, paired-pulse adaptation does not reduce the discriminability of simple stimuli. It provides information about the spatiotemporal context of stimulus history.SIGNIFICANCE STATEMENT The present work provides a computational framework that demonstrates how adaptation allows neurons to encode spatiotemporal dynamics of stimulus history.

Diverse effects of stimulus history in waking mouse auditory cortex.

Responses to auditory stimuli are often strongly influenced by recent stimulus history. For example, in a paradigm called forward suppression, brief sounds can suppress the perception of, and the neural responses to, a subsequent sound, with the magnitude of this suppression depending on both the spectral and temporal distances between the sounds. As a step towards understanding the mechanisms that generate these adaptive representations in awake animals, we quantitatively characterize responses to two-tone sequences in the auditory cortex of waking mice. We find that cortical responses in a forward suppression paradigm are more diverse in waking mice than previously appreciated, that these responses vary between cells with different firing characteristics and waveform shapes, but that the variability in these responses is not substantially related to cortical depth or columnar location. Moreover, responses to the first tone in the sequence are often not linearly related to the suppression of the second tone response, suggesting that spike-frequency adaptation of cortical cells is not a large contributor to forward suppression or its variability. Instead, we use a simple multilayered model to show that cell-to-cell differences in the balance of intracortical inhibition and excitation will naturally produce such a diversity of forward interactions. We propose that diverse inhibitory connectivity allows the cortex to encode spectro-temporally fluctuating stimuli in multiple parallel ways.NEW & NOTEWORTHY Behavioral and neural responses to auditory stimuli are profoundly influenced by recent sounds, yet how this occurs is not known. Here, the authors show in the auditory cortex of awake mice that the quality of history-dependent effects is diverse and related to cell type, response latency, firing rates, and receptive field bandwidth. In a cortical model, differences in excitatory-inhibitory balance can produce this diversity, providing the cortex with multiple ways of representing temporally complex information.

A multi-second adaptive integration process underlies sound texture perception

Temporally homogenous sound textures—as produced by rain, fire or insect swarms—are thought to be represented with time-average statistics measured from early auditory representations. We explored the averaging process involved in sound texture perception using “texture steps”—stimuli whose statistics changed at some point in time. We reasoned that judgments should be biased by the stimulus history included in the averaging process. Listeners were presented with two sounds, a texture step and a probe texture (with constant statistics). Listeners were asked to compare the endpoint of the texture step to the probe and to select the sound that was most similar to a familiar reference texture. Judgments were biased by the presence of a step 1 second prior to the stimulus endpoint, but the bias was reduced when the step occurred 2.5 seconds from the endpoint. In addition, the bias was substantially larger for textures whose statistics were less homogenous (ocean waves) than textures whose statistics were more homogenous (rain). The results suggest a texture integration process operating over several seconds, but whose integration window is adapted to the homogeneity of the sound signal, averaging over longer periods of time for more variable textures.

Linear Summation of Repulsive and Attractive Serial Dependencies: Orientation and Motion Dependencies Sum in Motion Perception.

Recent work from several groups has shown that perception of various visual attributes in human observers at a given moment is biased toward what was recently seen. This positive serial dependency is a kind of temporal averaging that exploits short-term correlations in visual scenes to reduce noise and stabilize perception. To date, this stabilizing "continuity field" has been demonstrated on stable visual attributes such as orientation and face identity, yet it would be counterproductive to apply it to dynamic attributes in which change sensitivity is needed. Here, we tested this using motion direction discrimination and predict a negative perceptual dependency: a contrastive relationship that enhances sensitivity to change. Surprisingly, our data showed a cubic-like pattern of dependencies with positive and negative components. By interleaving various stimulus combinations, we separated the components and isolated a positive perceptual dependency for motion and a negative dependency for orientation. A weighted linear sum of the separate dependencies described the original cubic pattern well. The positive dependency for motion shows an integrative perceptual effect and was unexpected, although it is consistent with work on motion priming. These findings suggest that a perception-stabilizing continuity field occurs pervasively, occurring even when it obscures sensitivity to dynamic stimuli.SIGNIFICANCE STATEMENT Recent studies show that visual perception at a given moment is not entirely veridical, but rather biased toward recently seen stimuli: a positive serial dependency. This temporal smoothing process helps perceptual continuity by preserving stable aspects of the visual scene over time, yet, for dynamic stimuli, temporal smoothing would blur dynamics and reduce sensitivity to change. We tested whether this process is selective for stable attributes by examining dependencies in motion perception. We found a clear positive dependency for motion, suggesting that positive perceptual dependencies are pervasive. We also found a concurrent negative (contrastive) dependency for orientation. Both dependencies combined linearly to determine perception, showing that the brain can calculate contrastive and integrative dependencies simultaneously from recent stimulus history when making perceptual decisions.

The I/O transform of a chemical sensor

A number of sensing technologies, using a variety of transduction principles, have been proposed for non-invasive chemical sensing. A fundamental problem common to all these sensing technologies is determining what features of the transducer's signal constitute a chemical fingerprint that allows for precise analyte recognition. Of particular importance is the need to extract features that are robust with respect to the sensor's age or stimulus intensity. Here, using pulsed stimulus delivery, we show that a sensor's operation can be modeled as a linear input-output (I/O) transform. The I/O transform is unique for each analyte and can be used to precisely predict a temperature-programmed chemiresistor's response to the analyte given the recent stimulus history (i.e. state of an analyte delivery valve being open or closed). We show that the analyte specific I/O transforms are to a certain degree stimulus intensity invariant and can remain consistent even when the sensor has undergone considerable aging. Significantly, the I/O transforms for a given analyte are highly conserved across sensors of equal manufacture, thereby allowing training data obtained from one sensor to be used for recognition of the same set of chemical species with another sensor. Hence, this proposed approach facilitates decoupling of the signal processing algorithms from the chemical transducer, a key advance necessary for achieving long-term, non-invasive chemical sensing.

The effect of adding Fascial Manipulation® to the physical therapy plan of care for low back pain patients

Fig. 1 Block diagram model of the mechanobiological response of fibrous load bearing tissue under biophysical stimuli including the impact of viscoelasticity/viscoplasticity. (R stands for repair, ED for enzymatic degradation, MD for mechanical degradation of the extracellular matrix). chanical behaviors, FT mechanical reaction to biophysical stimuli is influenced by the type of stimulus input and the stimulus history; 3) Under macroscopic biophysical stimuli, ECM molecules are subjected to stress and strain, and could thus undergo mechanical degradation (MD). Changes to mechanical properties and ECM structure related to MD in FT and non-linear over time and heterogeneous across the tissue; 4) When FLBT are subjected to macroscopic biophysical stimuli, these stimuli are scaled down to microscopic biophysical stimuli which are, in turn, transformed into biochemical signals that the cells can sense. In response to these signals, the cell can degrade the ECM via enzymatic degradation (ED) or repair (R) it and 5) The tissue global mechanobiological response is the result of competitive dynamics between degradation and repair leading to an inverse-U relationship between stimulation and tissue quality. Conclusion: Our analysis showed that viscoelasticity and viscoplasticity of live FLBT could influence tissue mechanobiological response, but experiments are required to confirm it. The impact of viscoelasticity and viscoplasticity may prove to have significant implications for in vivo clinical applications.

Frequency-specific adaptation and its underlying circuit model in the auditory midbrain

Receptive fields of sensory neurons are considered to be dynamic and depend on the stimulus history. In the auditory system, evidence of dynamic frequency-receptive fields has been found following stimulus-specific adaptation (SSA). However, the underlying mechanism and circuitry of SSA have not been fully elucidated. Here, we studied how frequency-receptive fields of neurons in rat inferior colliculus (IC) changed when exposed to a biased tone sequence. Pure tone with one specific frequency (adaptor) was presented markedly more often than others. The adapted tuning was compared with the original tuning measured with an unbiased sequence. We found inhomogeneous changes in frequency tuning in IC, exhibiting a center-surround pattern with respect to the neuron's best frequency. Central adaptors elicited strong suppressive and repulsive changes while flank adaptors induced facilitative and attractive changes. Moreover, we proposed a two-layer model of the underlying network, which not only reproduced the adaptive changes in the receptive fields but also predicted novelty responses to oddball sequences. These results suggest that frequency-specific adaptation in auditory midbrain can be accounted for by an adapted frequency channel and its lateral spreading of adaptation, which shed light on the organization of the underlying circuitry.

Perceptual adaptation: Getting ready for the future

Perceptual systems continually adapt to changes in their sensory environment. Adaptation has been mainly thought of as a mechanism to exploit the spatiotemporal regularities of the sensory input in order to efficiently represent sensory information. Thus, most computational explanations for adaptation can be conceptualized as a form of Efficient coding. We propose a novel and more holistic explanation. We argue that perceptual adaptation is a process with which the perceptual system adjusts its operational regime to be best possible prepared for the future, i.e. the next sensory input. Crucially, we assume that these adjustments affect both the way the system represents sensory information (encoding) and how it interprets that information (decoding). We apply this idea in the context of a Bayesian observer model. More specifically, we propose that the perceptual system tries to predict the probability distribution from which the next sensory input is drawn. It does so by exploiting the fact that the recent stimulus history is generally a good predictor of the future and that the overall long-term stimulus distribution is stationary. We assume that this predicted probability distribution reflects the updated prior belief of the Bayesian observer. In addition, we assume that the system is adjusting its sensory representation according to the predicted future stimulus distribution via Efficient coding. Because this sensory representation directly constrains the likelihood function, we can define an optimal Bayesian observer model for any predicted distribution over the next sensory input. We demonstrate that this model framework provides a natural account of the reported adaptation after-effects for visual orientation and spatial frequency, both in terms of discrimination thresholds and biases. It also allows us to predict how these after-effects depend on the specific form of the short- and long-term input histories. Meeting abstract presented at VSS 2015

Spike timing precision changes with spike rate adaptation in the owl's auditory space map.

Spike rate adaptation (SRA) is a continuing change of responsiveness to ongoing stimuli, which is ubiquitous across species and levels of sensory systems. Under SRA, auditory responses to constant stimuli change over time, relaxing toward a long-term rate often over multiple timescales. With more variable stimuli, SRA causes the dependence of spike rate on sound pressure level to shift toward the mean level of recent stimulus history. A model based on subtractive adaptation (Benda J, Hennig RM. J Comput Neurosci 24: 113-136, 2008) shows that changes in spike rate and level dependence are mechanistically linked. Space-specific neurons in the barn owl's midbrain, when recorded under ketamine-diazepam anesthesia, showed these classical characteristics of SRA, while at the same time exhibiting changes in spike timing precision. Abrupt level increases of sinusoidally amplitude-modulated (SAM) noise initially led to spiking at higher rates with lower temporal precision. Spike rate and precision relaxed toward their long-term values with a time course similar to SRA, results that were also replicated by the subtractive model. Stimuli whose amplitude modulations (AMs) were not synchronous across carrier frequency evoked spikes in response to stimulus envelopes of a particular shape, characterized by the spectrotemporal receptive field (STRF). Again, abrupt stimulus level changes initially disrupted the temporal precision of spiking, which then relaxed along with SRA. We suggest that shifts in latency associated with stimulus level changes may differ between carrier frequency bands and underlie decreased spike precision. Thus SRA is manifest not simply as a change in spike rate but also as a change in the temporal precision of spiking.

Sensory recalibration integrates information from the immediate and the cumulative past.

Vision usually provides the most accurate and reliable information about the location of objects in our environment, and thus serves as a reference for recalibrating auditory spatial maps. Recent studies have shown that recalibration does not require accumulated evidence of cross-modal mismatch to be triggered, but occurs as soon as after one single exposure. Here we tested whether instantaneous recalibration and recalibration based on accumulated evidence represent the same underlying learning mechanism or involve distinct neural systems. Participants had to localize two sounds, a low- and a high-frequency tone, which were paired with opposite directions of audiovisual spatial mismatch (leftward vs. rightward). In accordance with the cumulative stimulus history, localization in unimodal auditory trials was shifted in opposite directions for the two sound frequencies. On a trial-by-trial basis, however, frequency-specific recalibration was reduced when preceded by an audiovisual stimulus with a different sound frequency and direction of spatial mismatch. Thus, the immediate past invoked an instantaneous frequency-invariant recalibration, while the cumulative past invoked changes in frequency-specific spatial maps. These findings suggest that distinct recalibration mechanisms operating at different timescales jointly determine sound localization behavior.

Different time scales of motion integration for anticipatory smooth pursuit and perceptual adaptation.

When repeatedly exposed to moving stimuli, the oculomotor system elicits anticipatory smooth pursuit (ASP) eye movements, even before the stimulus moves. ASP is affected oppositely to perceptual speed judgments of repetitive moving stimuli: After a sequence of fast stimuli, ASP velocity increases, whereas perceived speed decreases. These two effects--perceptual adaptation and oculomotor priming--could result from adapting a single common internal speed representation that is used for perceptual comparisons and for generating ASP. Here we test this hypothesis by assessing the temporal dependence of both effects on stimulus history. Observers performed speed discriminations on moving random dot stimuli, either while pursuing the movement or maintaining steady fixation. In both cases, responses showed perceptual adaptation: Stimuli preceded by fast speeds were perceived as slower, and vice versa. To evaluate oculomotor priming, we analyzed ASP velocity as a function of average stimulus speed in preceding trials and found strong positive dependencies. Interestingly, maximal priming occurred over short stimulus histories (∼two trials), whereas adaptation was maximal over longer histories (∼15 trials). The temporal dissociation of adaptation and priming suggests different underlying mechanisms. It may be that perceptual adaptation integrates over a relatively long period to robustly calibrate the operating range of the motion system, thereby avoiding interference from transient changes in stimulus speed. On the other hand, the oculomotor system may rapidly prime anticipatory velocity to efficiently match it to that of the pursuit target.